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Comparative Anatomy of the Cerebral Convolutions The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series BY

Paul Broca

1. THE LIMBIC CONVOLUTION IN THE HUMAN BRAIN The cerebral hemisphere is made up of a very heterogeneous central mass in which there are groupings of extremely diverse components and of an external layer that I along with Burdach call the mantle of the hemisphere. The folds in the mantle are what form the convolutions. In lissencephalic animals (without convolutions), the mantle is smooth over the greatest extent of its area; in gyrencephalic animals, the mantle is composed of a set of convolutions.1 The mantle completely envelops the central mass or body of the hemisphere, with the exception of a very well-defined area visible on the medial surface after the hemisphere has been isolated by a medial cut and the cerebral peduncle has then been severed. This region is roughly oval in shape and is bordered above and in front by the groove of the corpus callosum and below and in back by the great cleft of Bichat. Foville and Gratiolet have referred to this region as the great window of the hemisphere because a large opening can be seen above, behind, and below the optic layer and peduncle; this opening leads to the cavity of the lateral ventricle. A different opening, the foramen of Monro, is also visible in this area; however, these two openings form only a minimal part of the region in question. This region essentially includes the cross-section of: the corpus callosum, the transparent septum, the anterior portion of the fornix, the commissures, the cerebral

peduncle, the floor of the third ventricle, the lateral wall of the third ventricle, the edge of the dentate body along the inferior margin of the cleft of Bichat, and the cleft of Bichat itself, which leads into the lateral ventricle. All of the convergent and divergent fibers that enter or exit the hemisphere pass through this area. The portion of the medial surface that is not covered by the mantle is not an opening, but in a sense it is the doorway for entering and exiting the hemisphere. I will henceforth call it the threshold of the hemisphere; this can be described in Latin nomenclature, very frequently used in other countries, by the word limen. The threshold of the hemisphere is surrounded on all sides by the mantle, which forms an edge around it that can be compared with the circular edge at the opening of a purse. I therefore call this edge the limbus of the hemisphere (edge), and I call the convolution that forms it the limbic convolution. This large convolution is composed of two arcs. The complete length of the superior arc runs along the convex surface of the corpus callosum; the inferior arc follows along the cleft of Bichat up to the tip of the temporal lobe. The superior arc is called the convolution of the corpus callosum, whereas the inferior arc is called the hippocampal convolution or the uncinate convolution and constitutes the final convolution of the temporal lobe. The usual distinction that is made between these two arcs is motivated to some extent by their locations in two different regions and also by the dividing line formed between them by the extension of the calcarine fissure (fissure of the hippocampus

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The words lissencephalic and gyrencephalic are attributed to Mr. Owen, who used them to refer to two subclasses of the class of mammals. This classification is not acceptable, though, because sometimes animals with convolutions and animals without them (edentates, rodents, primates) can be found in the same zoological order. However, the words lissencephalic and gyrencephalic, when taken in a purely descriptive sense in accordance with their etymology, are very useful for describing animals that have convolutions and animals that do not.

C 2015 Wiley Periodicals, Inc. V

Translated by Donna Furlani; technical revision by Patrick R. Hof and Luiz Pessoa Received June 12, 2015; Revised July 14, 2015; Accepted July 14, 2015. DOI 10.1002/cne.23856 Published online in Wiley Online Library (wileyonlinelibrary.com)

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minor).2 This dividing line is only superficial, however; it cuts only into a small portion of the full depth of the limbic convolution. Most often, it does not even take up the full width and does not reach the concave edge. The continuity of the convolution of the corpus callosum with the hippocampal convolution is never interrupted in any case. Gerdy and Foville recognized this completely. In 1838 in their Recherches sur l’encephale [Research on the Encephalon], not appreciated nearly enough today, Gerdy described the limbic convolution in these terms: “The medial sides of the lateral lobes (hemispheres) show an annular convolution that is constant in its presence but variable in its regularity; it begins in front of the corpus callosum or floor of the brain in merging with the medial olfactory convolution. From there it travels toward the back along the superior surface of the floor up until its posterior edge, which it hugs closely as it curves below to come to an end toward the obtuse medial tuberosity of the temporal lobe in the inferior part of the brain. . . . Consequently, this convolution forms a long, oval ring that encircles the corpus callosum as it travels from the tuberosity of the temporal lobe behind, above, and in front of the corpus callosum; it then continues forward below the temporal lobe, merging with the medial olfactory convolution. . . . This ring is interrupted only by the medial part of the temporal fissure.”3 The medial part of the temporal fissure, or the fissure of Sylvius, is what we today call the valley of Sylvius. The medial tuberosity of the temporal lobe is none other than the hippocampal lobule. A passing comment: Gerdy made a weak effort to rid science of the absurd and bothersome term corpus callosum, which the term floor would replace to great

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This extension, common to the calcarine fissure and the medial occipital fissure in humans and in the gibbon, is actually part of the calcarine fissure; in all monkeys other than the gibbon, a superficial annectant convolution that runs from the cuneus lobule to the convolution of the corpus callosum (the cuneolimbic annectant convolution) separates the extension from the inferior extremity of the occipital fissure. The cuneolimbic annectant convolution exists in humans and gibbons as well, but it is deep; it is visible only after the edges of the medial occipital fissure have been spread apart, and this fissure is thus connected with the calcarine fissure. The set of fissures thus forms a Y with its stem extending to the concave edge of the limbic convolution. Gratioles [sic] clearly saw that this stem of the Y must be related to the calcarine fissure. However, he incorrectly believed that it completely separated the hippocampal convolution from the convolution of the corpus callosum, that it penetrated the cleft of Bichat, and that it extended along the inferior edge of this cleft, i.e., along the medial surface of the temporal lobe, between the hippocampus major and the dentate body. He therefore incorrectly incorporated two completely different crevices into a single fissure that he called the hippocampal fissure. I attest that they are in fact completely separate: the calcarine fissure or fissure of the hippocampus minor, visible externally, and the groove of the hippocampus major, hidden inside the cleft of Bichat. 3 Gerdy, Recherches sur l’encephale [Research on the Encephalon] In Journal des connaissances medico-chirurgicales [Journal of Medical and Surgical Knowledge], Dec. 1848. Reprinted in Gerdy, Melanges d’anatomie, de physiologie et de chirurgie [Compilation of Anatomy, Physiology, and Surgery], ed. Broca and Beaugrand. Paris, 1875, in-8. Vol. I, p. 357.

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benefit, but the term is so deeply rooted in the language that I do not dare propose abandoning it. One year after Gerdy, in a thesis submitted to the Academy of Medicine and the Academy of Sciences in 1839, Foville also provided a description of the annular convolution, which he deemed the only “major” convolution, and called it the hem convolution. According to Foville, the hem was a small band of white fibers extending along the full length of the base of the convolution; he compared it with the border or hem at the opening of a purse. The first volume (and the only published volume) of his work on the nervous system contains the following description of the hem convolution: “The principal characteristic of the only convolution of major importance, which we shall call the hem convolution, is that it forms a complete circle on the boundary of the margin, the border of the cortical layer of the hemisphere. The hem convolution is curved and pulled in close around the corpus callosum, the peduncular section, and the perforated quadrilateral, and it tightly encloses all these parts within its circumference. Regarded as a whole, this convolution can be compared with the casing of a headband that has a ribbon running through the casing; the two ends of the ribbon exit through a small slit in the headband. The entire part of this convolution that represents the casing of the headband is located on a vertical plane and is tightened around the corpus callosum and the peduncular section; the places where the two cords would come out are located in the medial portion of the anterior edge of the perforated quadrilateral and in the lateral part of its posterior edge. We could even push this everyday comparison further, which is exactly what I intend to do, and correlate one of the two cords of the headband with the optic nerve and the other with the olfactory nerve.”4 The optic nerve, or rather the small band of the optic nerve, insofar as this is the only thing that could possibly be intended, has only a contiguous relationship with the system Foville describes; he was therefore incorrect in attaching it. However, he saw very clearly that what is described in humans with the flawed term olfactory nerve is a part of this system, and that the circle of the hem convolution is completed by the lateral olfactory root as it curves around the lateral edge of the locus perforatus of Vicq d’Azyr and then plunges into the hippocampal convolution. Foville also saw that, as a consequence, this circle is not interrupted by the valley of Sylvius as Gerdy had believed. In addition, Foville saw that the locus perforatus itself belongs to the system of the hem convolution. This important fact is easily

4 Foville. Anatomie, physiologie et pathologie du syste`me nerveux [Anatomy, Physiology, and Pathology of the Nervous System]. Paris, 1844, in-8. Vol. I, p. 195.

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

proved once comparative anatomy is involved, but Foville studied humans exclusively, so it took a great deal of wisdom on his part to discover this based on the human brain. In primates, after the atrophy of the olfactory lobe, a deep transverse depression is formed in front of the hippocampal lobule; this is known as the valley of Sylvius, and it appears to interrupt the continuity of the “hem” convolution. Because of this, Foville’s successors were unable to find the connections that he had described, and they were unaware of the significance and the nature of the locus perforatus. Meanwhile, in studying the typical primate brain based on the green monkey ([C]ercopithecus sabaeus),5 Gratiolet thought he noticed that the fissure of the hippocampus minor, or calcarine fissure, in this animal extended as far as the cleft of Bichat in such a way as to completely separate the convolution of the corpus callosum from the hippocampal convolution. This, however, was a false impression, as I have already remarked (see note on p. 386 [p. 2502 of the English translation]). Nevertheless, because of Gratiolet’s great expertise, it was widely accepted that the hem convolution was interrupted in back by the calcarine fissure and thus said to be “hippocampal.” The convolution of the corpus callosum and the hippocampal convolution were thus described as being completely separate; such is the force of habit that even today we continue to think of these two convolutions as being entirely independent of one another, even though general consensus recognizes that the calcarine fissure does not enter the cleft of Bichat. I propose to apply contributions from comparative anatomy in examining the great cerebral system that encircles the limbus of the hemisphere, the importance of which has long since been recognized by Gerdy and by Foville, despite its considerably diminished significance in humans. I was obliged to start by citing the works of these anatomists, Foville’s works especially, but I felt it necessary to replace the terms they used with a term more appropriate for the subject. In the majority of mammals, the system in question is completed in front by a long extension called the olfactory lobe, and the word annular (Gerdy) would give an imprecise idea of its form. This term lacks accuracy even for primates, because the path of the convolution is interrupted by the valley of Sylvius. As for the term hem convolution, it is utterly flawed because the hem from which this name is taken is not a distinct element; this

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“As Mr. de Blainville, my illustrious master, had chosen the green monkey as the osteological model of the primates, I believed I should follow his example, and I will use the green monkey brain as my starting point” (Gratiolet. Memoire sur les plis cerebraux de l’homme et des primates [Thesis on the brain folds of humans and primates]. Paris, 1854, in-4, p. 22).

is the artificial product of dissection guided by a preconceived notion. Along the anteromedial edge of the locus perforatus, the medial white root of the olfactory nerve travels inside and then above, where it can be followed as far as the origin of the convolution of the corpus callosum; the lateral white root of the same nerve, meanwhile, travels along the anterior edge and then the lateral edge of the locus perforatus, crosses the valley of Sylvius, and plunges into the hippocampal convolution. Do the white fibers of these two nerve roots penetrate into the depth of the convolutions where they end, to connect deeper in with the white matter of the convolutions? The majority of anatomists doubt this to be the case; the fact is that the roots seem to disappear into the outermost layer of the gray matter. The soft mass of the brain is so easily separated in all directions that Foville, with much skill and a little eagerness to oblige, was able to reveal tracts along the lengths of these roots that he followed through the cortical layer into the white matter. Other anatomists who wanted to repeat this procedure, however, were unsuccessful, with the result that the portion of the hem that corresponds to the locus perforatus is generally considered to be completely different from the portion that, according to Foville, follows along the base of the hem convolution. The characteristics that Foville attributed to this second section were unable to be confirmed. The continuity of the hippocampal convolution with the convolution of the corpus callosum must imply the continuity of their white matter, as is the case everywhere else where two convolutions connect with one another. It is therefore very simple to use simple cuts without any dissection to demonstrate that the white matter continues uninterrupted from the origin of the convolution of the corpus callosum to the terminus of the hippocampal convolution, thereby forming an almost complete ring below the limbus of the hemisphere; the ring is interrupted only at the valley of Sylvius. In this mass of white matter, however, it is not possible to follow the fibers that Foville claimed run throughout the entire length of the white matter and form the small annular band of the hem. The name for the convolution that forms the limbus of the hemisphere cannot be based on the name of a small band that is purely theoretical. The name limbic convolution that I have adopted indicates the constant connections between this convolution and the limbus of the hemisphere, and it does not involve any theories. Because the name does not express a set form, it is applicable to all mammalian brains: to those that have a true corpus callosum and to those in which the corpus callosum is nonexistent or rudimentary (Owen’s lyencephalic animals); to those that have a true olfactory lobe, and to those in which

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the olfactory lobe is only vestigial. Finally, it has the benefit of allowing the parts related to the description of this convolution to be described without having to change the adjective: the great limbic lobe, the limbic fissure, the superior or inferior limbic arc, etc. Until now, I have expressed myself as if the area surrounding the limbus of the hemisphere were a true convolution. This was necessary so that I could conform to the description provided by Gerdy and by Foville. After having reproduced their texts, however, and thereby having conceded that the convolution of the corpus callosum and the hippocampal convolution are continuous with one another and constitute one single system, I must add that, in the current cerebral nomenclature, the term convolution is no longer applicable to this system. The term convolution, which at one time could be used to refer to any part of the folded surface of the hemisphere, now has a specific meaning; it applies to subdivisions of lobes, and, although in some cases a lobe can (as we will see Further on) be formed from only a single convolution, a convolution can never extend beyond the borders of its lobe, even though it may continue more of less directly with one of the convolutions of a neighboring lobe. However, in humans, and I add, in all primates, the “annular” or “hem” convolution, which I call limbic, belongs to the temporal lobe because of the hippocampal convolution that constitutes its inferior arc, but its superior arc, called the convolution of the corpus callosum is clearly not a part of this lobe. These two convolutions, even though they are continuous with one another, cannot be combined into a single convolution. Furthermore, I would comment that the convolution of the corpus callosum forms an utterly unique region in the hemisphere that cannot be associated with of any of the lobes accepted so far; this region should be considered as constituting a special lobe to itself, the lobe of the corpus callosum. This consideration already seems necessary in primates, but it becomes even more indispensable once other mammals are considered as well. I will therefore speak no more of the “limbic convolution.” I will use other terms in studying the individual parts of which it is composed and in grouping these parts into a single system. In primates, this system is only a minor development, but, in the brains of other land mammals, it constitutes an entire vast region that is more distinct from the rest of the hemisphere than any of the divisions known as lobes. In the mantle, it constitutes a primary division, a fundamental division that is more than a lobe, and furthermore encompasses several lobes; the simple term lobe is not sufficient to describe it, so I will call it the great limbic lobe. Its evolution in the mammalian series is closely linked with the evolution of the olfactory lobe.

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It would therefore be useful first to provide some commentary on the olfactory lobe and the sense of smell.

2. THE OLFACTORY LOBE AND THE SENSE OF SMELL Philosophers and physiologists who refuted that vision was the first of the senses never doubted the superiority of the information that vision provides, but they did hold, correctly, that this information would be unreliable and would give us only very imperfect and even very wrong ideas about the objects that resolve themselves on our retinas if we did not have other senses, especially the sense of touch, to help us. It is only once we understand the shape and the main properties of an object that we manage to recognize it, not with our eyes, which receive only an image, nor with the corpora quadrigemina, which receive only impressions, but rather with the intelligence that corrects the image, interprets it, and transforms these deceptive impressions, most often into positive information. Those who believed they were lowering the status of the sense of sight by these perfectly valid comments unwittingly proclaimed its superiority instead, in that they thereby proved that sight is the most intellectual of the senses. The value of vision to an animal is the value of its intelligence. Recognizing prey or enemies from a distance and measuring the distance in preparation of attack, defense, or flight: is this not one of the primary needs in the struggle for survival? Vision can fulfill this need provided that it is auxiliary to a welldeveloped intelligence. It provides all animals with copious concepts of great importance, but precise and complete knowledge can be derived from them only by the animals that know how to observe and reflect, analyze and compare the various parts of an image, be wary of errors of perspective, calculate distance based on the apparent size of an object whose actual size is known, and thus attain an exact idea of the area, etc. In such animals, vision is both the main guard and the main guide; it is the most useful sense, and the role of the other senses is diminished. The sense of smell in particular loses a great extent of its importance, and we know that the olfactory system in primates has atrophied considerably. By contrast, this system is extremely well-developed in the majority of other mammals. For them, the sense of smell plays a role that is equal if not superior to the role of sight. It is smell that guides these animals in selecting food, in pursuing prey, in fleeing from danger, in seeking out females, and in returning to their dens. The use of this sense is simple and requires only a

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

minor intellectual task. The sense of smell perceives a certain odor that is specific to a certain thing; a little experience is enough to recognize the thing, and estimating distance requires only estimating the intensity of the scent. The animal that is most successful at this process is not the most intelligent one but rather the one with the most well-developed olfactory system; the stupidest quadrupeds are often far superior to humans in this regard. This fact alone sufficiently shows the complete inferiority of the sense of smell. We cannot say it is inversely related to intelligence, but we can at least attest that this sense is predominant in beasts, and we can acknowledge it as a bestial sense: its significance results from the degree of perfection of the olfactory system attributed to it much more than from intellectual tasks that it triggers in the cerebral system. This system can even function independently from the brain proper, since, in inferior vertebrates, it is not connected at all with the part of the brain that correlates with the cerebral hemisphere in mammals. The central mechanism of the olfactory system is made up of two parts, 1) the olfactory lobe and 2) a certain section of the brain where there are connections with this lobe. The olfactory lobe is in turn made up of two parts, 1) a terminal bulb, a bulge of gray matter from which issues the neural networks of the olfactory membrane in the nasal cavities, and 2) a peduncle of greatly variable length and width, formed entirely and in part by the white fibers that connect the lobe to the rest of the brain. The olfactory lobe usually projects forward from the base of the brain, and the majority of its area is isolated. The lobe is almost always located within the cranium, but in certain fish (sheatfish, carp, etc.) it is outside and in front of the cerebral cavity; the peduncle is thus very long, and even much longer than the brain proper. In most fish, this peduncle passes below the cerebral lobe without joining it and continues to insert into the transverse commissure formed by the anterior extremities of the inferior nerves (or motor nerves) of the spinal cord. The conger eel is the only fish in which Desmoulins had seen this peduncle issue a small network in the cerebral lobe as well.6 This exception is probably not unique, but, at least as a general rule, the olfactory lobe in fish is not connected to the other lobes of the brain and connects only with the motor nerve bundles of the spinal cord. It derives its full function from them, and the information that it provides the animal is immediately transformed

into choices that go into effect without participation from other cerebral systems. A similar arrangement can be observed in some birds (birds of prey, ducks, etc.). The olfactory lobe is not connected at all to the cerebral lobe; it terminates at the inferior surface of the optic layer, which is distinct from the cerebral lobe.7 It is even doubtful that it penetrates into this layer, because it seems to insert exclusively into a special layer formed by the inferior nerve bundles of the spinal cord. In other birds such as passerines and gallinaceous birds, however, the olfactory peduncle inserts exclusively into the cerebral lobe, and this is also the case in anurans and reptiles. In this second category, so different from the first, the true olfactory center is no longer the olfactory lobe; it is the cerebral lobe. This is where psychological events occur as a result of the sense of smell. The olfactory lobe does not therefore fall to the level of a simple organ of transmission, however. The large quantity of gray matter that it contains proves that it is also an organ that processes. It does more than receive an impression; it perceives it and extracts information from it, but it does this in order to transmit this information to the cerebral lobe, which evaluates the information and makes decisions as a result. To summarize, in classes lower than the class of mammals, the olfactory lobe is sometimes attached to the part of the brain that corresponds to the cerebral peduncle in mammals and sometimes to the part of the brain that corresponds to the cerebral hemisphere. It is only in very rare exceptions that the olfactory lobe is integrated with both parts (conger eel). This exception becomes the rule in mammals, however; their olfactory lobe is continuous with both the cerebral peduncle and the mantle of the hemisphere. Among these two connections, only the second is constant (unless the olfactory system has vanished completely, as is the case in many cetaceans). The first connection can disappear; this is what we see in primates and amphibious mammals. This trend proves that the olfactory lobe has lost a significant part of its function, the part that made it a major organ, and indeed we see that it has been reduced to a very small size. This is but an exception, however, and we will soon examine its cause. The mammalian brain model generally entails the existence of a large olfactory lobe, where one part connects directly to the motor nerve fibers of the cerebral peduncle and

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6 Desmoulins. Anatomie des syste`mes nerveux des animaux a verte`bres [Anatomy of the Nervous Systems of Vertebrate Animals]. Paris, 1825, 2 vol. in-8. Vol. I, p. 166.

We know that the optic layer in birds forms the base of the optic lobe, whereas the base of the cerebral lobe is formed by the corpus striatum. In mammals, the optic lobe is considerably atrophied (corpora quadrigemina) and separated from the optic layer. The optic layer is joined to the corpus striatum and attaches in the same way to the cerebral lobe, which is called the cerebral hemisphere.

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another part connects to the mantle of the hemisphere. Consequently, the olfactory lobe can switch back and forth between functioning as an autonomous center and as a servant of the hemisphere, or it can perform both functions at once. Because in the lowest vertebrates, and even in some birds, the role of a true olfactory center is fulfilled by a second-rank organ that is distinct from the cerebral lobe, we can confidently conclude that once part of this role is attributed to the cerebral lobe, i.e., the hemisphere, the intellectual involvement needed in exercising the sense of smell is rather slight, and the part of the hemisphere where this occurs likely ranks low in the cerebral hierarchy. This part of the hemisphere constitutes the great limbic lobe in mammals. It differs from the rest of the mantle of the hemisphere because of a completely unique evolution. It was this part that was first to differentiate itself in the most inferior brains (lissencephalic brains); its contours were already defined before any other division became visible on the surface of the mantle. As the brain was perfected and complicated in gyrencephalic animals, this lobe remained untouched by the folding that created the convolutions, and it remained stationary as everything progressed around it. Finally, it retreated and largely atrophied when the major development of the anterior convolutions provided primates with a preeminent frontal lobe, the site of the highest intellectual functions. Considered from the perspective of the formation of the great limbic lobe, mammals are divided into two highly unequal categories that we will be continually obliged to compare. The first includes mammals in which the olfactory lobe is highly developed and the great limbic lobe is thereby complete. The vast majority of mammals belong to this first category. The second category, characterized by the rudimentary state or complete absence of the olfactory lobe, includes only cetaceans, carnivorous amphibious mammals, and primates. It is clearly a very heterogeneous group. This is because atrophy of the olfactory system can occur as a result of two very different influences, one related to the environment and the other to the animal itself. Mammals that live mostly or constantly in the water receive little if any benefit from the sense of smell. Odor particles are definitely carried by water and can be registered by appropriate systems; we see that the olfactory lobe is almost constant, and often highly developed, in fish. Mammals’ olfactory systems are unsuitable for smelling in water, however. In adapting to an aquatic life, cetaceans and carnivorous amphibious mammals kept the mammalian anatomical structure, and, like their lungs, their nasal cavities receive

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only air. Their sense of smell does not provide them information about the conditions of the environment where they hunt their prey, so it is no more than an accessory or useless sense; consequently, the olfactory lobe atrophies. In most cetaceans, no vestige of this lobe remains; in other cetaceans and in carnivorous amphibious mammals, it is so far reduced that it could be mistaken for a nerve. The atrophy of the olfactory system in the preceding case is the consequence of disuse brought on by the environment. In primates, it is due to a completely different cause, as mentioned previously. Smelling is based on air for these animals as it is for all land vertebrates, but it plays only an accessory role in their lives. Intelligence, fed by all the senses at once, gained supremacy over this bestial sense, and the physiological change is demonstrated by two concurrent anatomical events, the advanced development of the frontal lobe and the atrophy of the olfactory lobe. The conditions that diminish the importance of the olfactory lobe are therefore very diverse; we can therefore understand why animals as different as aquatic mammals and primates are brought together by a common characteristic that sets them apart from all other mammals. This characteristic is not in the least bit zoological, as we have just seen. The two categories of mammals that have been established do not correspond to any natural division; they exist only in reference to the study of the great limbic lobe. Nevertheless, it is necessary to give them names to allow them to be distinguished in descriptions. I will therefore call ordinary mammals in which the supremacy of the sense of smell is substantiated by the advanced development of the olfactory system osmatic mammals (osmatic is derived from orlg, odor). Mammals in which this sense has lost its dominance for one reason or another can be called anosmatic by contrast. These terms can be further applied to describe brains as well as the animals themselves. The great limbic lobe exists, with varying degrees of distinctness, size, and completion, in all mammals. Before examining its various modifications, I should first provide a general overview, for which purpose I will use the otter brain as a model. This brain is best suited for comparisons because, of all the osmatic brains, it differs the least from others. We know that the otter is not part of the families of amphibious mammals; it is a carnivore in the marten family. It hunts for food primarily in the water, but it lives on land, and although the sense of smell is a weak aid in pursuing prey, it is very helpful in avoiding the otter’s numerous enemies. According to Buffon, “upon leaving the water, otters shake themselves and go to sleep curled up on the

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

Figure 1. Diagram of the medial and inferior surface of the right hemisphere of the otter brain. 1, The rostrum of the corpus callosum; 2, its genu; 3, its splenium, below which can be seen the posterior pillar of fornix and the origin of Ammon’s horn; 4, medial surface of the optic layer; 5, cut of the cerebral peduncle, separated from the great limbic lobe by the cleft of Bichat; 6, the optic band breaks free at the anterior portion of the cleft of Bichat and enters the optic layer and the hippocampal lobe. P, P, P, parietal lobe; F, frontal lobe; S, fissure of Sylvius; O, olfactory lobe; O0 , olfactory peduncle; C, origin of the lobe of the corpus callosum; C, C0 , C00 , lobe of the corpus callosum; H, H0 , hippocampal lobe. a, b, lateral root of the olfactory lobe; a, b, c, inferior arc of the limbic fissure; c, retrolimbic annectant convolution; c, d, subparietal fissure; e, subfrontal sulcus; f0 , medial root of the olfactory lobe.

ground, like dogs; before falling asleep, however, they attempt to determine by their sense of smell more than by their sense of sight, which is weak and limited in range, whether there are enemies to fear in the surroundings.” The otter’s olfactory system is therefore not atrophied as in amphibious mammals; its great limbic lobe is still complete. However, it represents no more than mediocre development, and the description of this intermediate level will provide us with an excellent starting point for later comparisons.

3. THE GREAT LIMBIC LOBE IN MAMMALS DESCRIBED BASED ON THE OTTER BRAIN The great limbic lobe can be compared with a racket. Like an elongated ring, it completely surrounds the entirety of the roughly oval-shaped region that I called the threshold of the hemisphere. An extension composed of the olfactory lobe stretches out from the anterior extremity of the oval; this represents the handle of the racket. The various parts of the great limbic lobe are not arranged on the same plane, however; its superior region spreads over the medial surface of the hemisphere, and its inferior region and extension are on the

inferior surface. It is therefore not possible to see everything at once: this makes describing the system very difficult. Readers can easily follow along with this description using a plaster model of a carnivore hemisphere or an actual hemisphere that has first been hardened in alcohol (because soft brains become deformed when they are manipulated). Ordinary diagrams would be insufficient beause they show only a single perspective of the hemisphere. I am therefore including a diagram that is somewhere between the norma medialis and the norma basalis, and I am even simplifying it somewhat by implying that the two surfaces are more spread out than they really are. The otter brain is better suited than any other brain for this trick because the great limbic lobe is smaller than it is in most other mammals and does not obstruct the rest of the mantle as completely. The included diagram (Fig. 1) represents both the medial surface, in the upper part of the diagram, and the inferior surface, in the lower part of the diagram, of the right hemisphere of the otter brain. It shows the entire great limbic lobe, which has been left white. Light, uniform shading has been added to the rest of the diagram, namely, the threshold of the hemisphere in the middle and, around the edges, the parts of the mantle that surround the great limbic lobe. This great lobe surrounding the entire threshold of the hemisphere is continuous with itself throughout, but three sections are distinguished that constitute three lobes. They are 1) above, the lobe of the corpus callosum, which forms the superior arc C, C0 , C00 of the great lobe; 2) below, the hippocampal lobe, H, H0 , which forms the lower arc; 3) in front, the olfactory lobe O, of which the base, O0 , is continuous with the anterior portion of the two arcs, in the manner of the handle of a racket. The anterior portion of the olfactory lobe is free, below the anterior extremity of the hemisphere. The rest of the great limbic lobe is encircled by a fissure that separates it from the cerebral convolutions; I call this the limbic fissure. The different parts of the limbic fissure can be studied from the norma basalis and the norma lateralis of the hemisphere, but the limbic fissure is seen in its entirety only in our diagram. It is composed of three arcs. The inferior arc begins at a, below the lateral edge of the base of the olfactory lobe, travels backward and slightly outside the length of the lateral root of this lobe, reaches the lateral (inferior in the diagram) edge of the hippocampal lobe at b, and extends backward to a short distance from the posterior extremity of the hemisphere at c. The inferior arc stops there, and after a short interruption the superior arc begins. This arc curves around the lobe of the corpus callosum, rises, and then curves forward and gradually climbs the

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Figure 2. Inferior surface of the otter brain. The right half of the cerebellum has been removed from the protrusion and from the bulb in order to show the inferior surface of the right hemisphere. O, olfactory lobe; O0 , its base; H, hippocampal lobe; C00 , posterior extremity of the lobe of the corpus callosum; R, fissure of Rolando; S, fissure of Sylvius. 2, lateral olfactory root; 3, medial olfactory root; 4, quadrilateral space; 5, optic band ending in the chiasm, which has been cut; 9, retrolimbic annectant convolution. The other numbers are explained in the text.

medial surface of the hemisphere to the superior or sagittal edge, which it reaches at d and passes in such a way as to extend more or less on the convex surface. The inferior and superior arcs that have just been described encircle the great limbic lobe above and below; they also enclose it behind, where, granted, they do not meet, but are separated by only a short gap c, and where without this slight interruption they would form a single curve. In front, however, they are spread wide apart, and their anterior extremities, a and d, are separated from one another by the entire height of the hemisphere. In the large space between these two ends, however, opposite the genu of the corpus callosum, the limbic fissure is embodied by a third arc, the anterior arc, e, which in the otter is rather short and not very deep. This arc forms only a very incomplete dividing line in front of the corpus callosum. This third arc, as we will see later, in actuality is just the anterior portion of the system of the superior arc, with which it is directly continuous in some animals. Then it forms a deep fissure, but in the otter, as in other carnivores and also in many other mammals, this vestige of the limbic fissure is only a slight crease.

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Now that we have shown the entirety of the great limbic lobe in our diagram, we will study its different components using accurate images drawn with a diagraph. The olfactory lobe and the hippocampal lobe are seen from the norma basalis (Fig. 2). The olfactory lobe, located below the frontal lobe, which it overlaps slightly in front, is made up of a small anterior bulb, O, of which the relatively very large peduncle, 1, is free and simply rests against the inferior surface of the frontal lobe. The base, O0 , of this is continuous with the rest of the hemisphere, however. This base immediately widens and spreads out; three parts can be distinguished, which are the three roots of the olfactory lobe. The sizeable lateral root, 2, travels outward and back to lie along the lateral border of the hippocampal lobe, with which it merges soon after. This root is whitish in color owing to the superficial longitudinal fibers coming from the olfactory peduncle. Below this superficial layer, the longitudinal fibers are enclosed in a rather large quantity of gray matter. The thinner and much shorter medial root, 3, travels inward and soon reaches the medial-inferior border of the hemisphere in front of the optic chiasm. It reaches the medial surface, where it plunges into the anterior and inferior extremity of the lobe of the corpus callosum (see Fig. 4 and Fig. 1, f). The color of the medial root is also whitish, but a little grayer than the color of the lateral root. Finally, the middle root or gray root is located in the space between the two other roots and fills a quadrilateral space (4; Fig. 2). It is bordered behind by the anterior edge of the hippocampal lobe and by the optic band, 5, which breaks away from the medial edge of this lobe to progress into the chiasm. This space is slightly sunken in comparison with the two olfactory roots and even more sunken in comparison with the hippocampal lobe. It forms the depression known as the valley of Sylvius and is coated with a layer of cortical substance that gives it a gray color, hence the name gray root. However, below this gray layer, which adheres to the borders of the two white roots and continues onto the surface of the hippocampal lobe, there is a layer of white fibers. These white fibers originate in the olfactory peduncle, run from the front to the back of the quadrilateral space, pass under the optic band as if it were a bridge, and continue on to merge with the most inferior fibers of the anterior extremity of the cerebral peduncle, 6. The deepest fibers of the middle olfactory root progress to the anterior cerebral commissure, in the part of the commissure that crosses the corpus striatum. Desmoulins believed that the volume of the anterior commissure in the mammalian series

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appeared to be in relation to the degree of development of the olfactory lobes.8 More deeply still, the middle root rests on the inferior surface of the corpus striatum; it is tightly adhered to it, but its fibers do not appear to penetrate it. Thus, when examined from bottom to top, the olfactory lobe shows a double connection; on one hand, it connects the two other limbic lobes through its two lateral roots; on the other hand, it connects the cerebral peduncle and the anterior commissure through its middle root. When the lobe is flipped front to back to study the superior surface of its base, however, we discover a third connection, between it and the frontal lobe of the hemisphere. This connection is established through a transverse insertion that can be called the superior olfactory root. This insertion occurs at the posterior extremity of the inferior surface of the frontal lobe, by means of a short strip made up of a superficial gray layer, which is continuous with the cortical layer of the frontal lobe, and a subjacent white layer, which is continuous with the white matter of the frontal lobe. In animals that have a large olfactory lobe, the depth of this lobe often contains a cavity that extends upward and back, passes between the frontal lobe and the corpus striatum, and merges with the anterior extremity of the lateral ventricle. This can be seen in Figure 3, which represents a longitudinal cut of the brain of a horse. The section of the olfactory peduncle that lies above this cavity constitutes the superior olfactory root or fourth root, and the section that lies below provides the three other roots.9 Now we return to the brain of the otter. The hippocampal lobe (Fig. 2) begins behind the quadrilateral space with a rather significant bulb, H, flattens in back, and merges directly with the lobe of the corpus callosum, C00 , below and behind the cerebral peduncle. It runs along the lateral portion of the great cleft of Bichat, filling the entire space between this cleft, 7, and the inferior arc of the limbic fissure, 8. This space, which is rather narrow in the otter, is by contrast very large in most other mammals. Because of this, the hippocampal lobe sometimes completely obscures the lateral surface of the hemisphere, as seen in the brain below. In the otter, however, the inferior convolutions of the lateral surface are still visible beyond the lobe, as is the fissure of Sylvius, S,

8

Desmoulins, Loc. cit., Vol. I, p. 264. In primates, the superior root is extremely diminished and joins the gray root, which is also greatly diminished. Together, they form a very short and very thin strip that is extremely fragile. This strip inserts into the border of the frontal lobe and the perforated quadrilateral space and continues along with them as the gray root.

9

Figure 3. Horse. Longitudinal cut, 6 mm from the median line, of the anterior portion of the left hemisphere. O, olfactory lobe; O0 , its base; Q, cut of the quadrilateral space and the middle olfactory root; R, cut of the optic band; F, cut of the frontal lobe; S, cut of the corpus striatum; V, cut of the lateral ventricle, of which the anterior extension V0 , curving around the corpus striatum, extends [into] V00 in the olfactory lobe; a, superior or frontal root of the olfactory lobe.

which runs obliquely to join with the limbic fissure near the anterior extremity of the hippocampal lobe. The surface of the hippocampal lobe is almost completely smooth; nevertheless, outside, there is a slight longitudinal depression, a very superficial crease of sorts that soon disappears, that follows along the medial edge of the lateral olfactory nerve. Furthermore, within this first crease, there is sometimes a second longitudinal crease that is even more superficial and definitely wider. This crease divides or, rather, tends to divide the hippocampal lobe into two parts, a medial one and a lateral one. This subdivision, which is always very vague, does not exist in the otter. The lobe of the corpus callosum, C00 , begins on the inferior surface of the hemisphere, behind the cerebral peduncle. It is directly continuous with the hippocampal lobe, without any dividing line. The border is therefore not established on the lobes themselves; rather, it is indicated in the limbic fissure, by an annectant convolution, 9, that connects the great limbic lobe with the posterior portion of the parietal lobe (I say the parietal lobe because the occipital lobe does not exist in mammals other than primates). This annectant convolution, which is absolutely constant throughout the entirety of the mammalian series, although it is not always superficial, merits a specific name; I will call it the retrolimbic annectant convolution. It is often a simple structure, as

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Figure 4. Otter. Medial surface of the right hemisphere. O, olfactory lobe; H, hippocampal lobe; C, origin of the lobe of the corpus callosum; C, C0 , C00 , lobe of the corpus callosum; F, frontal lobe; P, P, parietal lobe. 9, retrolimbic annectant convolution; 11, frontolimbic annectant convolution. See text for the other letters [sic].

we see in the otter, but it is also often divided into two juxtaposed and more or less parallel folds. In the latter case, it has been confirmed that the anterior fold connects with the hippocampal lobe and the posterior fold with the lobe of the corpus callosum. Consequently, when there is a single annectant convolution, it belongs to both lobes at once and is used to indicate the border between them. From this point, the lobe of the corpus callosum runs along the posterior edge of the great cleft of Bichat until the median line, then curves around the splenium of the corpus callosum and reaches the medial surface of the hemisphere (see Fig. 4), where it completely surrounds the corpus callosum, first resting, C00 , on its superior edge, where it is separated from the corpus callosum by a rather deep groove (groove of the corpus callosum). It then curves in front of the genu, where the groove stops, and finally descends along the rostrum of the corpus callosum until the inferior edge of the medial surface of the hemisphere, where it is continuous with the medial root of the olfactory lobe at C. This point C can be considered as the origin of the lobe of the corpus callosum, and we would then say that the lobe ends at C00 , on the inferior surface of the hemisphere, where it merges with the hippocampal lobe. Located on the medial surface of the hemisphere, the lobe of the corpus callosum gradually increases in size from back to front. In back, it occupies only a part of the expanse of the medial surface, allowing the innermost convolution of the parietal lobe (P, P), the sagittal convolution, to be seen above it. In front, however, it takes up the entire medial surface of the hemisphere up to the convex or sagittal border and even extends slightly onto the convex surface, where we will soon revisit it. Its anterior extremity, in front of the

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genu of the corpus callosum, is mostly continuous with the frontal lobe, F; it is, however, separated by a very superficial depression, 10. This depression is so indistinct in the otter that it could be mistaken for a vascular impression, but it is often much deeper. It constitutes the anterior arc of the limbic fissure and is the vestige of the subfrontal fissure in primates, but in carnivores it is so rudimentary that at most it could be called the subfrontal sulcus. Above and below this sulcus, the frontal lobe and the lobe of the corpus callosum connect together for the most part. The superior connection, 11, can be seen in many mammals, including the otter; I will call this the prelimbic or frontolimbic annectant convolution. Its position and size can vary according to the expanse and the depth of the subfrontal sulcus. It is thin and deep enough in some animals to lead one to believe that it is missing entirely; with a bit of attention, however, at least the vestige of it can be found. As for the inferior connection, 12, it is constant and invariable, given that the anterior arc of the limbic fissure never extends to the inferior edge of the hemisphere. Consequently, the most inferior and medial part of the frontal lobe always inserts directly at the origin of the lobe of the corpus callosum, immediately above point C, where the lobe receives the medial root of the olfactory lobe. Between the retrolimbic annectant convolution, 9, and the prelimbic annectant convolution, 11, the convex edge of the lobe of the corpus callosum is traced by the superior arc of the limbic fissure, which separates it from the most medial parietal convolution, P, P. This fissure, 13, 13, is long, deep, and uninterrupted. It is located entirely below the parietal lobe, which earns it the name of subparietal fissure. It climbs to the sagittal edge of the hemisphere, makes a deep cut in it, and extends into the convex surface. This terminal extension (14, 14; Fig. 5) is quite variable in length and direction; in the otter it is rather long and also very angled, but in other carnivores and many other mammals it travels in a transverse direction, i.e., perpendicular to the great cleft between the hemispheres. When this is the case, the two fissures, emerging in the same area in the sagittal edge of the two hemispheres, form a cross with the medial cleft, which they cut through perpendicularly. Leuret calls this the cruciate sulcus, but this name is defective because the shape is not always cross-like. The name is widely used, however, and is convenient; it would perhaps be difficult to replace, so I will continue to use it. I will, however, note that it is not a simple sulcus, but rather a true fissure. In considering that the cruciate fissure establishes the anterior border of the parietal lobe, or at least of its most medial convolution, several authors have

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Figure 5. Superior surface of the otter brain. The part left in white, 15, is formed by the lobe of the corpus callosum; 14, the cruciate sulcus formed by the anterior extremity of the subparietal fissure; R, fissure of Rolando; S, fissure of Sylvius; 16, frontal lobe; p, primary parietal sulcus.

believed this fissure to be analogous to the fissure of Rolando in primates. The fissure of Rolando belongs to the convex surface, however, whereas the subparietal fissure, of which the cruciate fissure is only an extension, belongs to the medial surface. Furthermore, what characterizes the fissure of Rolando anatomically is the boundary that it establishes between the frontal lobe and the parietal lobe, but the anterior edge of the cruciate fissure is not formed by the parietal lobe. Rather, it is formed by the superior part of the lobe of the corpus callosum, which, taking up the full height of the hemisphere at this point, reaches up to the convex surface, 15. As for the frontal lobe, it is located much further forward; it barely appears, if at all, at the tip of the hemisphere, 16, in front of Fissure R, which is the true fissure of Rolando and must be examined from the norma lateralis (see Fig. 6). From this view, it becomes clear that the parietal convolutions, of which there are three in the otter, originate at the posterior part of the lateral edge of the hemisphere, above the limbic fissure. They rise toward the sagittal edge and turn from back to front while circumscribing the fissure of Sylvius, S, in the shape of three more or less abruptly bent arcs. They then extend in a posterior to anterior direction up to a sharply angled fissure located all the way in front. All three convolutions stop here and are separated from the fissure by only a fold, P0, which is analo-

gous to the ascending parietal convolution in primates. This fissure, R, thus establishes the anterior border of the parietal lobe and separates it from the frontal lobe, F, which is extremely small. Consequently, it is this fissure that represents primates’ fissure of Rolando. It originates along the inferior-lateral edge of the hemisphere, immediately above the limbic fissure, with which at first glance it seems connected. This is only an illusion, though, and, by spreading apart the edges of the two fissures, we see that they are separated from each other by an annectant convolution, 17, that extends from the frontal lobe to the most inferior convolution of the parietal lobe, P1, or the Sylvian convolution. This point of origin of the fissure of Rolando is located significantly in front of the origin of the fissure of Sylvius. Starting from there, the fissure of Rolando first travels forward at a sharp angle, and then rises while adopting an almost transverse direction. It ends a short distance from the sagittal edge of the hemisphere. Above this termination, the frontal lobe connects, 16, both with the anterosuperior portion of the lobe of the corpus callosum and with the superior parietal convolution, P3, or, rather, with the superior portion of the ascending parietal. The fissure that we have just described as analogous to the fissure of Rolando in primates had been interpreted completely differently by Mr. Meynert. This author, who had not examined the limbic fissure in its entirety, considered the entire part of the limbic fissure in front of the fissure of Sylvius as belonging to the fissure of Sylvius in carnivores. In other words, he

Figure 6. Lateral surface of the right hemisphere of the otter brain. O, olfactory lobe; H, hippocampal lobe; L, inferior arc of the limbic fissure; S, fissure of Sylvius; R, fissure of Rolando; F, frontal lobe; T, temporal lobule of the parietal lobe; p, primary parietal sulcus; P1, Sylvian convolution or first parietal convolution; P2, second parietal convolution; P3, third parietal convolution or sagittal convolution; P0, post-Rolandic parietal convolution. The parts left in white belong to the great limbic lobe.

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extended the fissure of Sylvius along the hippocampal lobe and from the base of the olfactory lobe to below the frontal lobe. Furthermore, not having seen the deep annectant convolution that, in otters and most other mammals, separates the limbic fissure from the fissure of Rolando, he considered the first to be a ramus of the second, i.e., a ramus of the fissure of Sylvius. Based on this, he drew an analogy with the ascending ramus of the fissure of Sylvius in humans.10 This interpretation has already been refuted above. I add that the ascending ramus of the fissure of Sylvius is an effect of the culmination of the frontal lobe, as is the fissure’s anterior ramus. These two rami, which are formed in the folds of the third frontal convolution, are not consistently present except in humans. Both are sometimes seen in orangutans and chimpanzees; gorillas and gibbons have only one of them, the anterior ramus; monkeys that are not apes, Old World monkeys, or New World monkeys do not have either, despite having an incomparably more well-developed frontal lobe than the carnivores. It would therefore be very strange for either of these fully evolved rami to be found in carnivores (I would add ruminants and pachyderms as well) when they are not present in tailed monkeys. For further detail, I refer to my Memoire sur le cerveau du gorille [Thesis on the Gorilla Brain], in which I defined the distinction between the ascending ramus and the anterior or horizontal ramus of the fissure of Sylvius and discussed the main pertinent issues.11 Returning to the otter brain, note that the three parietal convolutions originate in a small area, T, enclosed between the posterior edge of the fissure of Sylvius, the superior edge of the limbic fissure, 8, and the retrolimbic annectant convolution, which is not visible in Figure 6 but did appear in Figures 2 and 4 (No. 9). This small area contains some of the components of the primate temporal lobe and can be considered the rudiment of it. However, it also gives rise to some of the components of the primate occipital lobe; it is also so manifestly a part of the parietal lobe that it is impossible to distinguish it from the parietal lobe. The otter thus has no temporal lobe or occipital lobe. This holds true for all mammals other than primates; their undivided parietal lobe contains the entire mass of convolutions except for the small frontal lobe. It is nevertheless useful to distinguish this small part of the parietal lobe located at T, between the fissure of Sylvius and the posterior section of the limbic fissure,

10

Archiv f€ur Psychiatrie [Psychiatry Archive]. Berlin, 1877, Vol. VII, p. 262 et seq. 11 Revue d’Anthropologie [Journal of Anthropology]. January, 1878, 2nd series, Vol. I, p. 18–25.

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with a special name to facilitate descriptions and comparisons. Although it is not yet a distinct lobe, we can at least designate it as a lobule, and I will call it the temporal lobule of the parietal lobe or, more simply, the temporal lobule, thus observing its important role in the formation of the temporal lobe in primates. In summary, the hemisphere of the otter, which we used as a model in the preceding description, is composed of two clearly distinct parts, 1) the great limbic lobe, formed by the joining of the olfactory lobe, the hippocampal lobe, and the lobe of the corpus callosum, and 2) the mass of convolutions, which makes up the rest of the mantle and in which only two lobes can be distinguished, a completely rudimentary frontal lobe and an immense parietal lobe, separated from each other by the fissure of Rolando. Now that we are familiar with the formation, the relationships, and the connections of the great limbic lobe, we can easily study the variations present in the mammalian series. We will first discuss osmatic mammals, beginning with lissencephalic mammals.

4. LISSENCEPHALIC OSMATIC BRAINS I have already explained (see page 385 [p. 2501 in the English translation], note 1) that I am using the word lissencephalic in a purely descriptive sense to designate mammals that do not have true convolutions; I do not imply the zoological meaning that Mr. Owen has attributed to it. If taken literally, this word would indicate a completely smooth hemisphere without any external subdivision; it therefore would not apply to any mammal. First, osmatic mammals always have a very distinct olfactory lobe, and, second, anosmatic mammals always have a deep separation, in the form of the fissure and valley of Sylvius, between the frontal and temporal lobes. However, although some dividing lines of varying intensity are consistently found on the inferior surface of the hemisphere, the same is not true for the convex surface, which is sometimes creased in well-defined convolutions and sometimes completely smooth or barely indented here and there with scarce, very superficial and incomplete sulci that do not establish any true subdivisions. In the first case, the brain is said to be gyrencephalic; in the second case, by contrast, the brain is said to be lissencephalic. Lissencephalic brains are lissencephalic to different degrees, and gyrencephalic brains likewise contain different quantities of convolutions that vary in distinction. There are therefore cases in which we hesitate to call the brain lissencephalic or gyrencephalic. These intermediate states are seen especially in the primate order,

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which further includes completely gyrencephalic genera and completely lissencephalic genera. These states are also found in the order Edentata, in which the anteater is completely lissencephalic, the sloth and the pangolin are gyrencephalic, and the aardvark and armadillo have rudimentary convolutions.12 From this we can conclude that the presence or absence of convolutions does not constitute a fundamental characteristic for zoological classification. This characteristic is nevertheless highly important, and Mr. Owen very correctly remarked that it usually is maintained throughout all the genera of the same family and all the families of the same order. This is what inspired him to create the subclasses of lissencephalic animals and gyrencephalic animals within the class of mammals.13 He classified edentates, rodents, bats, and insectivores into the first subclass and cetaceans, ruminants, pachyderms, carnivores, and primates (except humans) into the second. We see that the lissencephalic orders generally include only small species. By contrast, the gyrencephalic orders include all the very large animals, and, although there are small ones as well, we must at least acknowledge that the main representatives of these orders are much larger than the majority of lissencephalic animals. Moreover: Mr. Dareste has noted that, in the same order and the same family, the size of the various species has a very clear influence on the presence or absence of convolutions and on their degree of development.14 This important discovery, which dates back to 1852, has been confirmed by the preceding information. Also, although in general rodents are lissencephalic, the largest of the rodents, the capybara, is gyrencephalic.15 Meanwhile, the

12

See the beautiful plates in George Pouchet’s Memoire sur l’encephale des edentes, The`se de la Faculte des sciences [Thesis on Edentate Brains, Dissertation of the Faculty of Sciences]. Paris, 1869, in-4, 6 pl. (very significant work). 13 According to Mr. Owen, the two other subclasses of mammals are lyencephalic animals and archencephalic animals. The first subclass includes animals in which the corpus callosum is rudimentary or nonexistent, i.e., monotremes and marsupials. The second includes only humans, which are classified as archencephalic because of the relative perfection of their brains. This superiority is purely psychological, though, and in anatomical characteristics humans clearly belong to the order of primates. In any case, humans have numerous convolutions and therefore ought to be qualified as gyrencephalic. As for lyencephalic animals, some, such as the echidna, have true convolutions, but most of them are more or less lissencephalic. 14 See Dareste. Troisie`me memoire sur les circonvolutions du cerveau chez les mammife`res [Third Thesis on the Convolutions in Mammal Brains]. (Annales des Sciences Naturelles [Annals of the Natural Sciences] Zoologie [Zoology] (4th series, Vol. III, 1855). The first two theses can be found in the same collection, the 3rd series, Vol. XVII, 1852, and the 4th series, Vol. I, 1854. See also Bulletins de la Societe d’Anthropologie [Anthropological Society Reports], 1862, 1st series, Vol. III, p. 26, and Comptes Rendus de l’Academie des Sciences. [Proceedings of the Academy of Sciences], 1870, Vol. 70, p. 193. 15 Dareste. Note sur le cerveau des rongeurs, et particulie`rement sur le cerveau du Cabiai [Note on the Rodent Brain, Especially the Capybara Brain]. In Annales des Sciences Naturelles [Annals of the Natural Sciences], 4th series, Zoologie [Zoology], Vol. III, p. 355, pl. XI, Figs. (1 and 3) (Paris, 1855, in-8).

Java mouse-deer, the smallest of the ruminants (rabbitsized), is nearly lissencephalic.16 The influence of size is especially manifest in the primate order, where the general trend, which is gyrencephalic, cedes to a lissencephalic model in the smallest species of the New World monkey families. These striking differences in the brain observed in animals that are closely related by their zoological characteristics but very different in size can be explained by a very simple comment made by Mr. Baillarger with regard to a very similar issue. In his thesis De l’etendue de la surface du cerveau et de ses rapports avec l’intelligence [On the Surface Area of the Brain and its Relation to Intelligence], Mr. Baillarger commented after having compared the surface of the human brain with that of the rabbit brain that “the difference between the relation of volumes and surface areas is the result of the mathematical law that states that the volumes of similar bodies are to one another as are the cubes of their diameters, whereas their surface areas are to one another as are the squares of their diameters, which results in very different proportions. The brain is subject to this law, which it thwarts in part by the existence of the convolutions.”17 The geometrical hypothesis invoked by Mr. Baillarger is irrefutable; it provides a very satisfactory explanation of the influence of size on the development of convolutions. Convolutions are formed by the folding of the cerebral cortex, where the effect is proportional to its surface area; thus, all other things being equal, a smooth brain is inferior to a folded brain, because it has less surface area. Given two animals that are very different in size but very similar to one another in other qualities, the larger of the two should have the brain with the larger volume. Provided that these two brains have roughly the same shape, their volumes would be proportional to the cubes of their diameters, in accordance with the law of similar solids. For example, if the diameters are to each other as one is to two, the volumes would be to each other as one is to eight. What then would be the relation between the surface areas? We know that they are to each other as are the squares of their diameters, and thus their relation would be not one to eight, but only one to four. The cerebral surface in this scenario has increased two times less than the

16

Loc. cit. pl. II, Figs. 4–6. Baillarger. De l’etendue de la surface du cerveau et de ses rapports avec l’intelligence [On the Surface Area of the Brain and its Relation to Intelligence] (Thesis presented to the Academy of Medicine on August 15, 1845). Reprinted in the author’s Collection of Theses. (Recherches sur l’anatomie, la physiologie et la pathologie du syste`me nerveux [Research on the Anatomy, Physiology, and Pathology of the Nervous System]. Paris, in8, p. 54, 1872). See also Bulletin de la Societe d’anthropologie [Anthropological Society Report], 1861, 1st series, Vol. II, p. 206.

17

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Figure 7. Marmot. No. I, inferior surface; No. II, medial surface of the left hemisphere; No. III, lateral surface of the left hemisphere; No. IV, superior surface. O, olfactory lobe; H, hippocampal lobe; Q, quadrilateral space; C, C0 , C00 , lobe of the corpus callosum; L, L0 , L00 , limbic fissure; b, optic band; p, vestige of the primary parietal sulcus.

cerebral volume, and the larger of the two brains would thereby be quite inferior to the smaller one if not for the folding of the cortical layer providing compensation for this inferiority. In other words, a growing brain has to develop folds or risk diminishing. Thus, in the same zoological category, for equal intelligence, the largest animals must have the most folded brains. It can therefore result that sometimes, in an order in which the normal model is a gyrencephalic brain, the smallest species are lissencephalic, and, sometimes, in an order in which the normal model is a lissencephalic brain, the largest species become gyrencephalic. This does not at all imply that the mantle of the hemisphere is not composed of the same parts in the diverse species of the same order, however; it means only that these parts are sometimes flat and sometimes raised in folds, sometimes unclear on the surface, sometimes outlined by sulci or fissures. What determines the nature and functions of a part of the mantle is the connections deep within, not its external form and appearance. This explanation of the influence that size has on the development of convolutions diminishes the physiological importance of the distinction between lissencephalic and gyrencephalic brains, but the full anatomical importance remains. After all, the folding of the surface of the brain does not happen by chance; a convolution’s

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shape, direction, position, and relationships are determined by the connections of various points of the cortex with the central parts. These connections are somewhat variable from one species to the next but are fixed within the same species. The highly diverse morphology of the convolutions, therefore, provides very valuable zoological characteristics. Nevertheless, in the midst of these excessive varieties, there is one portion of the hemisphere that in osmatic mammals undergoes only very slight modifications, and its main characteristics are independent of the presence or absence of convolutions. This is the great limbic lobe. We will study it first in lissencephalic animals. No matter how smooth or simple the brain, there is always a limbic fissure (although its depth and length vary) that allows us to distinguish the great lobe, even if no other part is defined in the rest of the hemisphere. This fissure is always incomplete in lissencephalic animals; some of its parts may be only rudimentary, thus making the borders of the great lobe unclear in some areas. The marmot provides such an example. From the norma basalis (Fig. 7, No. I), we can make out the olfactory lobe, O, in front, with both its medial and its lateral roots, as well as the middle or gray root located in the quadrilateral space, Q. Further back, a rather

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

large bulb forms the hippocampal lobe, H; the optic band, b, emerges from the medial edge of the lobe. The optic band is very large and forms the posterior and medial borders of the quadrilateral space as it runs into the optic chiasm. To this point, there is no difference between this description and the description of the otter brain, but the inferior arc of the limbic fissure is well-defined only in front of L and behind L0 . Its middle section, which corresponds to the anterior one-third of the hippocampal lobe, is sometimes reduced to a very superficial depressed line, as can be seen at L00 on the right hemisphere. Sometimes this section disappears completely, as can be seen by the left side; the hippocampal lobe thus merges into the rest of the mantle in this area. In a second marmot brain that we have, the inferior limbic arc is continuous on both sides, but it is still very indistinct in the middle section. The posterior section of this arc, L, just barely reaches the posterior edge of the hemisphere. It therefore does not extend onto the medial surface (No. II), but the limbic fissure reappears further in front, at L00 , in the form of a superficial longitudinal depression located above the corpus callosum and very close to the sagittal edge of the hemisphere. This is what the superior arc of the limbic fissure has been reduced to. The result of this is that the lobe of the corpus callosum, C, C0 , C00 , is very indistinct because its posterior-superior portion merges with the rest of the mantle. It is even much less distinct than the hippocampal lobe. Only the olfactory lobe is welldefined; without the guide of comparative anatomy, the cohesiveness of the three lobes that form the great limbic lobe would never be suspected. Nonetheless, we would still notice that the lobe of the corpus callosum (Fig. 7, No. II, C00 ) is continuous in back and below with the hippocampal lobe, and in front and below, C, with the medial root of the olfactory lobe. The union of these three parts forms a complete circle around the threshold of the hemisphere18 and consequently embodies the great limbic lobe. The boundaries of the great lobe are a little more obvious in the beaver (Fig. 8). From the norma basalis (No. I), we see that the olfactory lobe and the hippocampal lobe, both very well-developed, are circumscribed by a horizontal fissure, L, L0 , which is interrupted only for an expanse of a few millimeters

18

In the posterior half of the limbus of the hemisphere (Fig. 7, No. II), two rounded bodies can be seen that are almost equal in size. The anterior one is the optic layer; the posterior one is the anterior colliculus of the corpora quadrigemina, very large in rodents and particularly in the marmot; it carves out a space in the mantle of the hemisphere. The posterior colliculus of the corpora quadrigemina is much smaller and was removed in the cut.

toward the middle portion of the hippocampal lobe. The posterior section, L0 , is just as deep as the other section and constitutes a true fissure. It continues (No. II) on the posterior surface, L0 , and climbs to the medial surface, where it extends for only a few millimeters. After a second interruption, however, it reappears at L00 , above the splenium of the corpus callosum. This superior section of the limbic fissure is much less deep than the other two. It extends only for about one-third of the length of the medial surface. The limbic fissure is thus less incomplete in the beaver than in the marmot. We also find it once again in a vestigial state, in front of the genu of the corpus callosum in the form of a slight, curved, linear depression, L000 , which is analogous to the subfrontal sulcus in the otter. This is a boundary that begins to form between the lobe of the corpus callosum and the portion of the mantle that corresponds to the frontal lobe. The lobe of the corpus callosum is thereby almost entirely circumscribed, behind at C00 , above at C0 , and in front at C. Finally, another linear depression sometimes traces along the lateral edge of the hippocampal lobe in such a way that it completes the inferior arc of the limbic fissure. This arrangement is seen in the left hemisphere (No. I) of the adult male beaver brain shown in Figure 8. The arrangement is not present in the right side of this brain or in either side of the brain of the younger beaver in our collection. The superior ramus of the limbic fissure, No. III, L00 , is not always positioned as it is in Figure 8. It is located much further forward in the other hemisphere of the same brain as well as in both hemispheres of our young beaver brain. From these variations, we can conclude that the limbic fissure is present essentially all the way around the great lobe. Two of its sections, L and L0 , are constant; they are deep enough to be independent of the conditions of local development. The other sections take shape more or less under the influence of these conditions, which can vary not only from individual to individual but even from one hemisphere to the other within the same brain. In the rabbit (Fig. 9, No. I), the full extent of the inferior arc of the great limbic lobe is distinct. The limbic fissure, L, L0 , runs uninterrupted along the entire lateral edge of the olfactory lobe and hippocampal lobe. It then extends on the posterior surface (No. II, L0 ) but does not reach the lateral surface, where the superior arc of the fissure is represented by a linear depression, L00 , located above the genu of the corpus callosum and by another longitudinal indentation, which is short, superficial, and located above the splenium. All in all, the limbic fissure is a little more complete in the rabbit than in the beaver. However, the superiority of the

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Paul Broca

Figure 8. Beaver. No. I, inferior surface; No. II, medial surface of the left hemisphere; No. III, lateral surface of the left hemisphere; No. IV, superior surface. O, olfactory lobe; H, hippocampal lobe; Q, quadrilateral space; B, optic band; C, origin of the lobe of the corpus callosum; C, C0 , C00 , lobe of the corpus callosum; L, L0 , L00 , limbic fissure; L000 , vestige of the subfrontal sulcus, p, vestige of the primary parietal sulcus.

beaver brain is made clear by the great size and great depth of the anterior extremity of the hemisphere, i.e., the region corresponding to the frontal lobe in gyrencephalic animals. We observe that this region is comparatively much thinner and much narrower in the marmot and especially in the rabbit. It would be superfluous to review the other lissencephalic brains. The limbic fissure can easily be found bordering the great limbic lobe in all of them, even the smallest brains, to one of the extents that I have just described. The great limbic lobe is sometimes relatively enormous (for example, in the hedgehog). I have taken my examples from the rodent order; the same characteristics can be observed in other lissencephalic animals, however—in Insectivora, Chiroptera, and Edentata. They are even found in marsupials, although the formation of the threshold of the hemisphere is

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notably different in these animals because of the nearly complete absence of the corpus callosum.19

5. GYRENCEPHALIC OSMATIC BRAINS The great limbic lobe in lissencephalic brains, as we have just seen, is always distinct enough for its formation to be determined and its connections recognized. Nevertheless, this requires some amount of attention,

19

The corpus callosum is very rudimentary in marsupials or even nonexistent in some; it is missing entirely in monotremes. These two groups of mammals make up the subclass of lyencephalic animals according to Mr. Owen. I have not yet been able to examine any monotreme brains myself, but the drawings of the echidna brain published by Mr. Eydoux and Mr. Laurent in Magasine de Zoologie [Zoology Magazine] (1838, 8th year, Paris, in-8, p. 174 and pl. 30) lead me to believe that the great limbic lobe in these animals is reduced to its inferior arc and includes only the olfactory lobe and the hippocampal lobe.

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

Figure 9. Rabbit. No. I, inferior surface; No. II, medial surface of the right hemisphere; No. III, lateral surface of the right hemisphere; No. IV, superior surface. Letters as in Figure 8.

in part because the limbic fissure is incomplete and in part because the surface of the great lobe, with the exception of the olfactory lobe, looks almost the same as the surface of the rest of the mantle. However, the great limbic lobe’s distinction and utterly unique nature become completely obvious in gyrencephalic brains because of the convolutions. The folding that creates the convolutions takes place throughout the entire extent of the mantle except for the great lobe; the mantle can thus be separated into two essentially different parts, the great lobe and the mass of convolutions. In very complex brains, i.e., brains with many folds, the lobe of the corpus callosum, which forms the superior arc of the great lobe, can undergo a mild amount of folding as evidenced by the presence of an isolated and relatively very superficial longitudinal groove. It still is much more simplistic than the mass of convolutions, however, and does not take on the serpentine appearance of the convolutions. As for the inferior arc of the great lobe, it retains the simplicity it has in lissencephalic brains and is completely excluded from the evolution observed in the surrounding parts of the brain. The corpus callosum does not

engage in this evolution except in very rare cases and to a relatively imperceptible extent. At the same time, the limbic fissure becomes much deeper and also much more complete; it is no longer interrupted except at very limited points. There is therefore a very obvious anatomical dividing line all around the great lobe, and what attracts attention right away is the contrast between the appearance of this part of the hemisphere and the appearance of the mass of convolutions. To provide an idea of this, I have reproduced a drawing borrowed from the excellent paper on The Comparative Anatomy of Domestic Animals by Mr. Chauveau and Mr. Arloing. This drawing appeared in 1871 and, consequently, was not created specifically for this purpose. The contrast is such that it becomes clear that these two parts of the hemisphere not only differ greatly in structure but also differ in the nature of their functions. If we consider that one of them remains fixed and unchangeable while the other evolves and develops, and that the one loses its importance as the other progresses, we are made to recognize that the first is the site of inferior skills that dominate in the beast and the second is the site of superior skills that dominate in

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Figure 10. Inferior surface of the horse brain. Image taken from the paper on the comparative anatomy of domestic animals, by Mr. `re et fils). Chauveau and Mr. Arloing; 2nd ed., p. 719 (J.B. Baillie

the intelligent animal. Furthermore, we can express this opposition of their respective natures by saying that the mantle of the hemisphere is composed of two parts: the bestial, represented by the great limbic lobe, and the intelligent, represented by the rest of the mantle. I emphasize these names to mark the physiological significance, but the anatomical terms should be derived from the anatomy itself. Of the two parts of the mantle of the hemisphere that must be distinguished, the first is sufficiently described by the term great limbic lobe. The other can be called the mass of convolutions in gyrencephalic animals, but this term is not applicable to brains that do not have true convolutions. We can therefore replace this term with the term extra-

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limbic mass, since this part is located outside the great limbic lobe. The great limbic lobe in all osmatic mammals displays the characteristics described above with regard to the otter brain, although the two lobes of the inferior arc are generally larger and thicker. The width of the hippocampal lobe sometimes equals the width of the hemisphere itself, which means that, from the norma basalis, the lobe entirely hides the mass of convolutions. The degree to which the anterior portion of this lobe sticks out, and consequently the depth of the transverse depression in front of it (valley of Sylvius), can vary rather greatly. The same is true of the size of the lateral olfactory root, which, after running along the lateral edge of the quadrilateral space, plunges into the lateral edge of the hippocampal lobe. This lobe is composed of three parts, even though from the outside it almost always appears to be singular. There is a lateral part, into which the lateral olfactory root extends; a medial part, which the horn of Ammon enters deeply; and a middle part, which is contained between the other two. Most often, there is no external indication of the succession of these three zones. If there is a lateral relief following the olfactory root that marks the extension of this root up front along the lateral edge of the hippocampal lobe, it is barely noticeable. Sometimes this relief is more welldefined, however, and it extends considerably further; then it is limited by a type of superficial longitudinal sulcus parallel to the corresponding section of the limbic fissure. This occurs in the horse, for example. In the horse, there is even a second longitudinal depression within the first sulcus; it marks the dividing line between the middle zone and the medial zone. Despite these variations, the hippocampal lobe presents only relatively slight differences in osmatic mammals. The lobe of the corpus callosum is almost equally as set. In small animals it is just as simplistic as it is in the otter; in large animals, it is more or less subdivided lengthwise by a longitudinal sulcus that is still incomplete and, moreover, not very deep at all. We see that these differences are of minor importance. All in all, amidst the extensive changes that take place in the rest of the mantle, the great limbic lobe conserves all of its essential qualities with remarkable consistency in the series of osmatic mammals. This does not rule out some variations, but they are slight and completely secondary in nature. What are greatly varied, at least externally, are the connections of the great limbic lobe with the mass of convolutions. We begin by recalling that the mass of convolutions forms only two lobes in the otter. The anterior lobe is very small and located all the way up front; it is called

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

the frontal lobe. The other lobe contains all the other convolutions and is called the parietal lobe. These two lobes are separated from each other by the fissure of Rolando. The fissure of Sylvius, which penetrates the parietal lobe, is shaped by the parietal convolutions but does not interrupt them. It does not prevent them from following their paths from back to front up to the fissure of Rolando, or rather up to a fold that forms the posterior edge of the fissure and is analogous to the ascending parietal convolution in primates. The fissure of Rolando exists in all gyrencephalic animals, and all gyrencephalic animals consequently have a frontal lobe that is distinct from the parietal lobe. In osmatic brains, however, the frontal lobe is almost always very small, very simple, and most often reduced to a single convolution. Its only noticeable subdivision is formed by a longitudinal depression that is located on the inferior surface and is wide and usually not very deep. The peduncle of the olfactory lobe lies in this depression. In the most complex brains (horse, camel, cattle, and tapir), though, the frontal lobe is a little larger and is subdivided by one or two sulci.20 Also, the fissure of Rolando is sometimes higher or lower, but its inferior extremity is always pointed backward. The point of the limbic fissure corresponding to this extremity is always located in front of the anterior extremity of the hippocampal lobe. The fissure of Sylvius does not have the constancy of the fissure of Rolando. It exists in all carnivores exactly as in the otter, and it is found in the same form in many other mammals, such as the boar. In ruminants and in most pachyderms, however, it is completely different, and sometimes it is even lacking entirely, as in the tapir, for example. These great differences indicate that the fissure of Sylvius is not an essential part of the composition of gyrencephalic brains. It is the usual, but not necessary, consequence of the way in which the convolutions are formed. I have already mentioned that the folding of the mantle is the effect of the expansion of the cerebral cortex: its surface, having grown larger than the volume of the underlying mass can hold, rises up and forms wrinkles of varying depths. To get an idea of the mechanism here, we can examine the part of a person’s skin that has been under a poultice for several days. The epidermis is swollen from the moisture and becomes longer and wider than the dermis that it covers; it becomes wrinkled as it forms true convolutions that sometimes are strikingly reminiscent of cerebral convolutions. This

20

In the immense brain of the elephant, the frontal lobe is relatively much larger and much more complex.

folding does not occur randomly; the shape and direction of the folds, and their anastomoses, are determined by the connections of the epidermis with the underlying dermis. These connections vary according to the area but are always the same in the same place. I have made molds of the skin on the anterior part of the knee under these conditions many times; the appearance of the serpentine convolutions of the epidermis is exactly the same on all of these molds. It is completely different in the instep, the elbow, the forearm, etc. This example shows us how the expansion of the cerebral cortex produces convolutions. Because the nature of the folding depends on the connections of the cortex with the underlying and surrounding parts, the convolutions should be set within a single species, analogous with closely related species, and different in distant species, just as the connections themselves are. This is in fact what happens. The great limbic lobe, as I have already said, is nearly entirely excluded from this folding. The rest of the mantle therefore forms the entire mass of convolutions, which surrounds the limbic fissure on all sides and which is always continuous with the great limbic lobe at a minimum of two points. First, the frontal lobe is essentially continuous with the origin (see above, p. 405 [p. 2514 in the English translation]) of the lobe of the corpus callosum. Second, the parietal lobe merges with the posterior part of the lobe of the corpus callosum and of the hippocampal lobe through the retrolimbic annectant convolution (p. 404 [p. 2514 in the English translation]). The cortex of the mass of convolutions is thus attached at both ends to the great limbic lobe and has its two medial and lateral edges pushed against the edges of the great lobe. Furthermore, the cortex is connected through its deep surface with the various bundles of white fibers blossoming in the body of the hemisphere. Consequently, when the expansion of its surface forces it to fold, the cortex does not fold randomly; the folding that occurs in each species does so in a way determined by its connections. Furthermore, this expansion of the cortex does not always occur to the same degree crosswise as it does lengthwise. As it lengthens, the larger cortex produces folds that are more or less transverse; as it widens, it produces folds that are more or less longitudinal. In lissencephalic animals, the extension of the cortex is never that great, and it is possible for folding to occur almost exclusively or even completely exclusively in a single direction. I of course am not referring to small, completely smooth brains such as those of insectivores, bats (except for the fruit bat), and some smaller rodents. The small ridges that sometimes exist on their

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Figure 11. Sloth brain. No. I, superior surface, according to Georges Pouchet; No. II, lateral surface of the right hemisphere of a younger sloth, according to the same author. O, olfactory lobe; H, hippocampal lobe; R, fissure of Rolando; F, frontal lobe; S, Sylvian fossa occupied by the subsylvian lobule; b, Sylvian convolution; a, sagittal convolution; p, primary parietal sulcus.

surfaces are vascular impressions and not sulci.21 In larger lissencephalic animals, however, we find some sulci, which are incomplete, isolated, usually very widely spaced and very superficial; they indicate a rough outline of the convolutions. These sulci introduce many transitional stages between lissencephalic brains and gyrencephalic brains as they develop further and further in certain species. In gyrencephalic animals, the extralimbic cortex is greatly enlarged in all directions and forms folds both lengthwise and crosswise. It increases more in width than it does in length, however, so the longitudinal folding is much more pronounced than the transverse folding. This is always the result for the front of the brain, at least, close to the tip of the hemisphere. It produces the fissure of Rolando, the lateral section of which is ordinarily quite oblique, but the other end of which always rises pointing toward the medial edge of the hemisphere. The identifying characteristic of transverse folding is not so much the absolute direction of the fold as it is its connections with the great limbic lobe, which remains untouched by folds. The extralimbic cortex, which forms the convex surface of the mantle, has its superior and medial edge running along the superior

21

The vascular ridges are always extremely superficial and correspond to the veins of the pia mater. They often have a characteristically branched shape. In brains that are dissected while fresh, the ridges are not very marked and often even disappear after a few days, but in brains hardened in alcohol with their membranes, they are much better defined, as the veins indent the brain matter as they retract. The ridges are easily distinguished from sulci because, after the pia mater is removed, we observe that each of them is covered by one of the veins in the membrane.

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arc of the great lobe. The inferior and lateral edge of the cortex runs along the inferior arc of the great lobe. Every fold that issues from one of these edges and travels toward the other, whether directly or somewhat obliquely, interrupts or deflects the longitudinal folds and consequently must be related to a fold caused by excess length, i.e., a transverse fold. This is the fold that creates the fissure of Rolando, between the small frontal lobe that forms the tip of the hemisphere and the immense parietal lobe that, uninterrupted, extends from there to the posterior end. Transverse folding most often manifests in the parietal lobe as well, where it provides the origin of the fissure of Sylvius, as we will see further on. The longitudinal fold is much more pronounced; it is substantiated by the presence of sulci that fully divide the parietal lobe lengthwise into a number of parallel convolutions. The sloth brain demonstrates this arrangement in utmost simplicity. The sloth is an edentate, but like many other members of the order, it has true parietal convolutions. We see in Figure 11 (No. I), taken from the excellent thesis by Mr. G. Pouchet, that there are a total of four convolutions. The innermost convolution, a, which I call the sagittal convolution, runs along the cleft between the hemispheres, which corresponds to the sagittal suture. It is also visible on the medial surface of the hemisphere, where it rests against the lobe of the corpus callosum. The outermost convolution, b, which I call the Sylvian convolution, forms the lateral edge of the hemisphere. If a portion of the hemisphere is observed outside of this convolution, it is

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

because the convolution assumes an S shape in forming a more convex arc; this is the first sign of excess length that, as it intensifies further, gives way to a true fold and produces the fissure of Sylvius in most gyrencephalic animals. When this fissure is not present, there is always at least a somewhat deep depression under the concave edge of the lateral convolution. This is analogous to what is known in human embryology as the Sylvian fossa (No. II, S). We will see later on that this fossa is filled by a part of the mantle called the subsylvian lobule. The outermost convolution, b, therefore merits the name I have given it, the Sylvian convolution.22 The sagittal convolution and the Sylvian convolution are consistent in gyrencephalic animals. The intermediate convolutions are located between them and vary in number from one to three. There are normally two, as in the sloth, but sometimes there is only one, as in the otter (see above, p. 408 [p. 2511 in the English translation], Fig. 6, P2), and there are three in large dogs. The intermediate convolutions can be considered to be subdivisions of the previous two convolutions. The parietal lobe is actually divided into two longitudinal zones separated by a sulcus that can be called the primary parietal sulcus. This is sulcus p in Figure 11, No. I. These two zones are simple in some lissencephalic animals that do not have true convolutions but do have a single longitudinal sulcus. This sulcus establishes a boundary that is evident, albeit still incomplete, between the medial, or Sylvian, region of the extralimbic mass and its medial, or sagittal, region. This vestige of the primary parietal sulcus is seen in the marmot (Fig. 7, No. IV, p), the adult male beaver (Fig. 8, No. IV, p), and the rabbit (Fig. 9, No. IV, p). It is very pronounced in the agouti and in the guinea pig, but it is absent entirely in the mole, the rat, the hedgehog, etc. In gyrencephalic animals, the Sylvian zone is always subdivided into two convolutions, the inferior one being the Sylvian convolution proper. As for the sagittal zone, it is sometimes simple (weasel, ferret, marten, otter, badger) but most often is divided into two parallel convolutions. The medial one is the sagittal convolution proper, and the lateral one is sometimes split by a longitudinal sulcus.23 Thus, the number of parietal convolutions can vary from

22

Having been unable to obtain a sloth brain, I was obliged to take the two numbers in Figure 11 from the thesis by Mr. Pouchet cited above (Memoire sur l’encephale des edentes [Thesis on Edentate Brains], Paris, 1889, in-4, pl. III, Fig. 6 and 7). You will observe that these drawings are of two different brains, where one (no. II) is from a very young animal and therefore displays some differences in the convolutions. 23 The sagittal convolution itself can be subdivided into two or even three secondary folds (as in the horse) by longitudinal sulci, but these folds occur only in the posterior section of the convolution and only on its medial surface, which rests against the falx cerebri.

three to five and the number of parietal sulci from two to four. These subdivisions more or less hide the essential distinction between the two zones; it can nevertheless be found through attentive examination, as the grouping of the two convolutions of the Sylvian zone is separated from the sagittal grouping by a sulcus that is larger and deeper than the others. Furthermore, the convolutions of each grouping still tend to unite with one another. In cats, the two convolutions of the Sylvian zone are joined in their middle sections. A less extensive union is observed slightly further back in some breeds of dog. In primates, in which the parietal lobe is considerably diminished as a result of the expansion of the frontal lobe, as we will see further on, the convolutions’ tendency to merge is accentuated. The two convolutions of the sagittal zone are now only one, the first parietal convolution. The two convolutions of the Sylvian zone combine in front to form the second parietal convolution and are separate only in back, where they are continuous with the two first temporal convolutions. There is only one longitudinal sulcus left, the parietal sulcus, which represents the primary parietal sulcus in osmatic gyrencephalic animals and the only parietal sulcus of some lissencephalic animals. Now we come back to osmatic gyrencephalic mammals. Until this point we have discussed their parietal convolutions as if they were parallel. Sometimes they are indeed just about parallel, as seen in the sloth brain. This would always be the case were the expansion of the cortex only in width; most often, however, the length also increases. Thus, the convolutions become longer than the great limbic lobe against which they rest and which represents the string to their bow. The convolutions become more sinuous, but they do so unequally. Because they do not have the same shapes, lengths, or connections, they end up subjected to different conditions with regard to how they should lengthen. Clearly, the effects of this lengthening from a morphological perspective are even more pronounced when the convolutions are shorter or, rather, when their two extremities are closer together. However, the parietal convolutions are even shorter when they are further out. It is therefore the Sylvian convolution that bends the most and the sagittal convolution that bends the least. This is what we have seen already in the otter brain (p. 408[p. 2511 in the English translation], Fig. 6) and can be seen even more clearly in the fox brain (Fig. 12), in which the Sylvian convolution forms an abrupt and deep fold, and the following convolutions form arcs of lesser and lesser inflection, out to the sagittal convolution, which is the least curved. The sharp inflection of the Sylvian convolution produces the fissure of Sylvius (Fig. 12, S), which is

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Figure 12. Fox. Lateral surface of the right hemisphere. O, olfactory lobe; H, hippocampal lobe; L, L, limbic fissure; RR, fissure of Rolando; S, fissure of Sylvius; F, frontal lobe; P1, Sylvian convolution, first parietal convolution according to Leuret; P4, sagittal convolution, fourth parietal convolution according to Leuret; p, primary parietal sulcus; P0, post-Rolandic fold, analogous to the ascending parietal convolution in primates; T, temporal lobule of the parietal lobe.

sometimes almost vertical and sometimes sharply angled back and upward but is always the effect of a transverse fold, because it is a result of the lengthening of this convolution. The fissure of Sylvius is the crevice that forms the inferior edge of the Sylvian convolution through its sudden folding in such a way that it comes into contact with itself, which allows it to increase greatly in length within a small space. This fissure is an almost constant feature, but it is not always laid out in the same way; its connections, its direction, and its very existence depend on the layout of the parts located below the inferior edge of the Sylvian convolution. The Sylvian convolution, like the other parietal convolutions, comes to an end up front at the post-Rolandic fold, P0, which is analogous to the ascending parietal convolution in primates and which borders the fissure of Rolando. The fissure of Rolando, although it separates the parietal lobe from the frontal lobe superficially, does not interrupt the continuity of the two lobes deep down. Furthermore, above the inferior arc of the limbic fissure there is an annectant convolution, which is at times superficial and at times deep,24 that joins the Sylvian convolution with the inferior and lateral edge of the frontal lobe. The frontal lobe is attached to the great lobe at the base of the olfactory lobe. From

24

This annectant convolution is sometimes completely superficial; it is almost superficial in the otter (see above, Figs. 2 and 6, No. 17, p. 401 and 418). When this fold is deep, the fissure of Rolando appears to connect with the limbic fissure.

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another perspective, the posterior extremity of the Sylvian convolution is attached to the posterior extremity of the hippocampal lobe by the retrolimbic annectant convolution. The Sylvian convolution thus forms an arc that is completed in front by the inferior edge of the frontal lobe and attached at both ends to the great limbic lobe. I will call this arc the arc of Sylvius. If the arc of Sylvius were not longer than the corresponding edge of the great lobe, it would fit along it exactly, and the limbic fissure would be utterly simplistic, as is the case in many lissencephalic animals. In gyrencephalic animals, however, the arc of Sylvius has excess length and can thus no longer match up with the great lobe; it must separate from it. Since it is attached to it at both ends, the separation occurs in its middle section, which corresponds to the anterior portion of the hippocampal lobe. In the gyrencephalic fetus, this divergence results in a depressed interval that roughly takes on the shape of a half-oval, and this corresponds exactly to the Sylvian fossa in human fetuses at 5 months. The inferior edge of this fossa is formed by the lateral edge of the great limbic lobe and its superior edge by the arc of Sylvius. The floor of the fossa is formed by a layer of the cerebral cortex that covers the lentiform nucleus or extraventricular nucleus of the corpus striatum and constitutes the subsylvian lobule, analogous to the insular lobe in primates (see p. 426 [p. 2520 in the English translation], Fig. 11, No. II, S). The subsylvian lobule shows an extremely variable degree of development. When it is large, it is more or less visible from the exterior and continues to separate the middle section of the arc of Sylvius from the great limbic lobe throughout the entire lifetime. When it is very small, the Sylvian convolution covers it as it grows and goes back to attach to the great lobe after executing the turns that produce the fissure of Sylvius. In the first scenario, the Sylvian fossa remains in existence, although its size and the extent to which it is filled by the subsylvian lobule vary. It is always more or less pressed below the part of the arc of Sylvius that surrounds it, however. In the second scenario, the fossa closes entirely, and it is necessary to move apart the edges of the fissure of Sylvius and the section of the limbic fissure in front of it in order to locate the rudimentary subsylvian lobule. The connections between the subsylvian lobule and the parts around it are always the same. The inferior edge of the cortex of the subsylvian lobule merges with the cortex of the great lobe, and the superior edge merges with the cortex of the arc of Sylvius. These connections adapt further at some points, though, when the lobule is developed enough to split into secondary

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

Figure 13. Tapir. Lateral surface of the left hemisphere. O, olfactory lobe; H, H, hippocampal lobe; L, L0 , L00 , inferior arc of the limbic fissure, interrupted by the inferior subsylvian fold; R, fissure of Rolando; F, frontal lobe; S, S, inferior edge of the Sylvian convolution (P1P1) that forms the superior edge of the Sylvian fossa; a, a0 , inferior subsylvian fold or temporofrontal fold; b, b0 , superior subsylvian fold or temporoparietal fold, which ends at the parietal post-Rolandic fold, P0; p, primary parietal sulcus; P1, P2, P3, P4, the four parietal convolutions, numbered according to Leuret’s nomenclature.

folds. There are two of these subsylvian folds, a superior fold and an inferior fold, and they are longitudinal. It is rare for both of them to be developed enough to be superficial; nonetheless, this arrangement is sometimes observed, as in the tapir, for example (Fig. 13). I will call the inferior fold the temporofrontal fold and the superior fold the temporoparietal fold. To justify these terms, which will greatly help in studying analogies, I will state in advance that the temporal lobe in primates is the result of the fusion of the atrophied hippocampal lobe with the part of the parietal lobe located behind the fissure of Sylvius or the Sylvian fossa; I have referred to it as the temporal lobe of the parietal lobe (see p. 410 [p. 2512 of the English translation]). As we study the subsylvian folds of osmatic mammals, I will above all be comparing them with the analogous parts in primate brains; it is therefore beneficial for the names I have established here to later be applicable to the description of the brains of superior mammals. Now, the enclosure of Sylvius in primates is composed of three parts, which correspond to the temporal, parietal, and frontal lobes. The temporal part is located behind and below the fissure of Sylvius, the frontal part is the section of the superior margin located in front of the fissure of Rolando, and the parietal part is the rest of the superior margin, between the fissure of Rolando and the terminal end of the fissure

of Sylvius. I will thus use the same terms for the analogous parts of the Sylvian region in osmatic brains. That said, I will describe the two subsylvian folds by referring to the tapir brain (Fig. 13), in which they are both superficial. The inferior or temporofrontal fold, a, a0 , originates in back, a, at the posterior portion of the lateral edge of the hippocampal lobe with a root that interrupts the path of the limbic fissure, L, L0 , L00 . From there, it runs forward and horizontally along the limbic fissure, and eventually, at a0 , it joins the frontal lobe, F, where it ends. This fold constitutes the insula in primates. The superior or temporoparietal fold originates, at b, from the posterior portion of the Sylvian convolution, P1, P1, and runs along and above the Sylvian convolution’s inferior edge, S, S, until it ends at b0 in the anterior part of the parietal lobe, behind the fissure of Rolando. This second fold is analogous to the temporoparietal annectant convolution, which in primates crosses the bottom of the fissure of Sylvius behind the insula and extends from the first temporal convolution to the lateral parietal convolution or Sylvian convolution. These two folds are large and superficial in the tapir, and the subsylvian lobule almost entirely fills the Sylvian fossa, which nonetheless remains slightly depressed. The result is that the Sylvian convolution, P1, strongly deviated upward, describes an arc around a sizeable lobule, and its excess length does not translate into the abrupt and deep fold that constitutes the fissure of Sylvius in

Figure 14. Horse. Lateral surface of the right hemisphere. O, olfactory lobe; H, hippocampal lobe; L, L, inferior arc of the limbic fissure; R, R, fissure of Rolando; F, frontal lobe; a, b0 , subsylvian lobule, which is superficial in front; a, temporofrontal fold; b0 , temporoparietal fold; S, S, fissure of Sylvius not communicating with the limbic fissure; p, p, middle or primary parietal sulcus; e, e, e, e, lateral parietal sulcus; f, medial parietal sulcus; P0 , P0 , P0 , Sylvian convolution or first convolution according to Leuret; P4, sagittal convolution or fourth convolution according to Leuret, obscured in front by the profile of the convolution P3. P0, postRolandic parietal convolution.

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most gyrencephalic animals. Its inferior edge, S, S, is simply curvy. Nevertheless, two grooves that are deeper than the others are noticeable at S0 and S00 , without either of them being able to be considered over the other as the rudiment of the fissure of Sylvius. In the horse, these two subsylvian folds are still rather large but are not superficial except in their anterior sections (see Fig. 14). The temporofrontal fold, a0 , is less well-developed than the other fold; up front at its frontal extremity, it forms a thick and very distinct fold attached to the lateral edge of the great lobe at L0 . A little further back, however, it becomes thinner, contracts, and inserts into the edge from L0 to L00 , across the limbic fissure, which here is no more than 1 millimeter deep. This insertion does not occur via a defined root, as in the tapir, but rather via a wide, thin strip of cortical substance. This strip is analogous to the strip that extends from the temporal lobe to the inferior edge of the insula in humans, below the inferior furrow of the insula. The temporoparietal fold, b0 , is thicker and certainly longer; in front, it ends at the inferior extremity of the fissure of Rolando, R, R, and merges behind the fissure with the anterior portion of the parietal lobe, P0, which is comparable to the ascending parietal convolution in primates. However, it is also continuous with the frontal lobe via a second anterior root that passes below and in front of the fissure of Rolando. This frontal root, which incidentally is very narrow in the horse, is lacking in all the other brains I have studied. From there, the temporoparietal fold, which is large and slightly serpentine, runs back and enters the arc of Sylvius, from which it is separated by a deep furrow (superior furrow of the insula in primates). It then plunges into the Sylvian fossa and finally inserts into the deep surface of the temporal lobe, behind the fissure of Sylvius, S, S. Although it is partially hidden in the bottom of the Sylvian fossa, the subsylvian lobule of the horse is still large enough to raise the edge of the arc of Sylvius significantly. The Sylvian convolution is so long, though, that even with this detour it still must fold, forming a long and deep fissure of Sylvius, S, S. This fissure is almost vertical (if it is angled upward and back slightly, it is just barely) and issues from the superior furrow of the subsylvian lobule. It does not reach the limbic fissure, from which it is separated by the temporal root of the temporoparietal fold or superior subsylvian fold. We note that the fissure of Rolando in the horse is not very angled, and it leaves a rather large frontal lobe in front of it. Thus far, we have examined the two subsylvian folds in the tapir and the horse, in which they are both developed enough to divide the Sylvian fossa into two separate regions, a superior one and an inferior one. The formation

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Figure 15. Roe deer. Lateral surface of the right hemisphere. O, olfactory lobe; H, hippocampal lobe; L, L0 , inferior arc of the limbic fissure; R, R, fissure of Rolando; F, frontal lobe; S, S, fissure of Sylvius not connecting with the limbic fissure; a, a0 , superior subsylvian fold or temporoparietal fold; b, pole of the hemisphere; p, primary parietal sulcus; P1, P1, Sylvian convolution, or first parietal convolution according to Leuret; P3, P3, second parietal partially fused with the previous one; P4, sagittal convolution, or fourth according to Leuret; P5, P5, third parietal according to Leuret; P0, post-Rolandic convolution.

of this fossa is simplified in ruminants as a result of the atrophy of the temporofrontal fold, but their temporoparietal fold is very large and is superficial throughout. Figure 15 shows the lateral surface of the hemisphere of a roe deer. The fissure of Rolando, R, R, is sharply angled and leaves only an extremely small frontal lobe, F, in front of it. The frontal lobe’s posterior and inferior extremity, which ends in a point, becomes thinner and almost immediately disappears into the bottom of the limbic fissure, L, while adhering to the great limbic lobe, along the edge of which it disappears. The subsylvian lobule is thereby reduced, so to say, to the temporoparietal fold. This fold originates at a as a superficial root from the posterior section of the Sylvian convolution. It fills the entire Sylvian fossa, which it crosses from back to front as it runs along the limbic fissure, L0 , L, and ends at a0 in the anterior extremity of the parietal lobe, behind the fissure of Rolando. Because the Sylvian fossa is very narrow, the arc of Sylvius is lowered considerably and provides only minimal development for the Sylvian convolution, P1, P1, which forms a great, nearly vertical fissure of Sylvius, S, S, by folding very deeply. The fissure of Sylvius is a manifestation of the superior Sylvian furrow, which is separated from the limbic fissure (or inferior furrow) throughout by the temporoparietal fold. This description holds for all ruminants, with the exception of the Java mouse-deer, the smallest of the ruminants. In the Java mouse-deer, the two subsylvian folds seem to be lacking, and, consequently, the very rudimentary fissure of Sylvius ends at the limbic fissure. I have chosen the very simple

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

brain of the roe deer for my model of the ruminant brain. In the roe deer, the Sylvian convolution, P1, and the convolution on top of it, P2, are joined in the middle. Meanwhile, the Sylvian grouping, P1, P2, and the sagittal grouping, P3, P4, are completely separated by a long, deep sulcus, p, which is the primary parietal sulcus. We have just seen that the temporoparietal fold is always large and superficial in ruminants. The decrease in the size of this fold leads to changes in the nature of the Sylvian fossa that can be studied in the porcine family of the pachyderm order. In the babirusa, the temporoparietal fold is just as large as in ruminants, and it is superficial throughout its entire expanse. In the domestic pig, it is less well-developed and more or less completely disappears under the edge of the Sylvian convolution. In the right hemisphere of a domestic pig (see Figs. 16 and 17), this fold is superficial at its anterior or parietal end, a, and is almost entirely hidden in the middle by the Sylvian convolution. The Sylvian convolution is much lower and almost comes into contact with the great limbic lobe. It reappears a little further back, and while its temporal insertion in the deep surface of the Sylvian convolution behind the fissure of Sylvius, S, S, is indiscernible, when the edges of the fissure are spread apart and the anterior part of the arc of Sylvius is moved out of the way, the fold can be seen in its entirety. It is easily conceivable that if the temporoparietal fold were slightly smaller still, the Sylvian fossa would close over it entirely. This is what has taken place in the left hemisphere of the same subject (Fig. 17). The anterior end of the temporoparietal fold, a, is the only visible part of it; as it runs along the limbic fissure, L0 , the fold immediately disappears beneath the Sylvian convolution, which is pressed precisely against the great limbic lobe. Consequently, the fissure of Sylvius descends down to the limbic fissure, where it branches off. There is thus no fundamental difference between instances in which the fissure of Sylvius ends directly at the limbic fissure and instances in which it stops at the superior furrow of the Sylvian fossa. The temporoparietal fold being a little larger or smaller is enough to cause this slight change, and the difference is so minimal that both arrangements can exist in the same brain, one in each hemisphere. In the two boar brains I have, which incidentally are very similar to domestic pig brains, the temporoparietal fold is deep on the right and on the left, so that the Sylvian region is organized exactly as in Figure 17. The subsylvian lobule’s diminished size means that the Sylvian convolution is no longer deviated by it and can no longer increase in length except by folding. The fissure of Sylvius, which is the result of this transverse folding, thereby becomes relatively longer. It no longer has enough room vertically (i.e., transversely), so it angles

back. The direction of this fissure and its connections are thus correlated. The fissure is angled upward and back when it ends at the limbic fissure, i.e., when the Sylvian fossa is closed over. By contrast, it is nearly vertical and positioned slightly further forward when it ends at the superior furrow of the subsylvian fossa, i.e., when the Sylvian fossa is more or less open and the subsylvian lobule is visible on the lateral surface. This correlation is constant, and we will find it again in carnivores. We have just seen that, although the temporoparietal fold in pigs is already greatly diminished, it is not yet completely covered by the arc of Sylvius, and its anterior or parietal root is still superficial. This is what we see at a (Figs. 16 and 17) above the limbic fissure, L, behind the fissure of Rolando, R, and below a horizontal crevice that breaks away from the limbic fissure and constitutes the anterior end of the superior furrow of the Sylvian fossa. This anterior root of the temporoparietal fold in turn disappears in carnivores. Figure 18 shows the lateral surface of the brain of a shepherd dog; it can be compared with Figure 6 (p. 408 [p. 2511 of the English translation]) of the otter brain and Figure 12 (p. 429 [p. 2522 of the English translation]), of the fox brain. In these animals, as in all other carnivores, the entire subsylvian lobule is deep. The fissure of Sylvius (Fig. 18, S, S) is sharply angled upward and back, and it branches off directly from the limbic fissure, L, L0 . The Sylvian convolution, P1, P1, is bent around the fissure of Sylvius; along the rest of its expanse, it is precisely attached to the lateral edge of the great limbic lobe. The Sylvian fossa is entirely closed over in such a way that there is no longer any external indication of the superior furrow of the Sylvian fossa. The fissure of Rolando, R, R0 , is thus the first crevice that branches off from the limbic fissure ahead of the fissure of Sylvius, but this does not make the fissure of Rolando a ramus of the limbic fissure. We have seen that in the otter (see above: p. 408 [p. 2511 of the English translation]. Fig. 6, No. 17) it is separated from the limbic fissure by a nearly superficial fold that is easily found once the pia mater is removed. This fold exists in the dog, as well; it is just deeper. A fresh brain, or one that has been barely hardened in alcohol for 24 hours, must be used for this fold to be visible. The Sylvian convolution will still be soft and easily lifted with the handle of a scalpel. The deep extensions of the pia mater are carefully pulled away with small forceps, and, thus spreading the fissure of Sylvius and the anterior section of the limbic fissure, the entire subsylvian lobule comes into view, i.e., the entire bottom of the Sylvian fossa. A mold of this can now be made easily. Figure 19 shows one such mold taken from the left hemisphere of a ratter. A slight linear relief, L, L0 , L00 , formed by the lateral

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Figures 16 and 17. Domestic pig. Figs. 16 and 17, lateral surface of the right hemisphere; Fig. 17, lateral surface of the left hemisphere from the same animal. Letters as in Figure 15. The Sylvian fossa, starts off open on the right side, where the vast majority of the temporoparietal fold, a, is visible, but is closed over on the left side (Fig. 17), where only the anterior extremity of the fold is noticeable and the fissure of Sylvius connects with the limbic fissure.

edge of the great limbic lobe marks the inferior lip of the limbic fissure and forms the inferior edge of the Sylvian fossa. The fossa is triangular; its two other edges are surrounded by the Sylvian convolution, P1, P1, of which the outwardly turned deep surface is marked in the diagram with light shading. At a, b, we see that the Sylvian convolution is continuous with the frontal lobe through a fold that passes below the inferior end of the fissure of Rolando, R, and separates the fissure from the Sylvian fossa,25 The subsylvian lobe, a, b, S, S0 , which forms the entire bottom of the fossa, is somewhat depressed in comparison to the limbic edge, L, L0 , L00 , over which it regularly inserts over its entire

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This fold, which is very pronounced in Figure 19, is often very rudimentary, and extra attention is then needed to find the vestige of it. Its left and right sides are sometimes very unequally developed; it is almost nonexistent in the right hemisphere of the brain whose left hemisphere is shown in Figure 19. The molds of both hemispheres are available at the Museum.

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expanse. It is continuous with the Sylvian convolution, in back below the bottom of the fissure of Sylvius, S, S0 , and above below the bottom of the superior furrow of the Sylvian fossa, a, b, S. Moreover, it is joined to the inferior posterior extremity of the Sylvian convolution by a short, wide, and relatively shallow fold, S0 , and to the anterior end by another fold, b. These two folds, b and S0 , constitute the two roots of the temporoparietal fold; the middle portion of this fold does not protrude at all. A final fold, a, located all the way up front, connects the subsylvian lobule to the frontal lobe; this is the anterior root of the temporofrontal fold. Thus, in the subsylvian lobule of the dog, there are vestiges of the two subsylvian folds found in ruminants and pachyderms. This lobule is very expansive and rather wide but is completely flat; it does not raise the edges of the Sylvian convolution. The Sylvian convolution is attached to the great limbic lobe and completely encloses the fissure of Sylvius. This model of the Sylvian region is found in all carnivores, although the number of parietal convolutions and their connections can vary between animals. In gyrencephalic primates, the subsylvian lobule is remarkably larger; in superior primates, it becomes large and complex enough to constitute a true lobe, which is the insula. Despite the insula’s size, though, the lobe does not become superficial; it remains hidden at the bottom of a deep fissure, because the Sylvian convolution is even more well-developed than the insula and covers it entirely, closing over the Sylvian fossa above it. We have just studied the connections between the inferior arc of the great limbic lobe and the mass of convolutions in osmatic gyrencephalic animals. Now we move on to the superior arc, which is formed by the lobe of the corpus callosum. We saw above that in the otter the posterior portion of the great lobe is joined to the mass of convolutions by the retrolimbic annectant convolution (p. 404 [p. 2509 of the English translation]). This annectant convolution is constant. It is almost always superficial and thus interrupts the limbic fissure and divides it into two arcs. The inferior arc runs along the hippocampal lobe; the superior arc traces the lobe of the corpus callosum. At first glance, this annectant convolution appears to be absent in the domesticated dog and the wolf, but it is easily found by spreading the edges of the limbic fissure. In one of our tapir brains, this annectant convolution is superficial on the left and deep on the right; in the other it is superficial on both sides. Whether it is superficial or deep is thus of very little importance. The retrolimbic annectant convolution originates in the great limbic lobe where the hippocampal lobe

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

Figure 18. Shepherd. Lateral surface of the left hemisphere. O, olfactory lobe; H, hippocampal lobe; L, L0 , inferior arc of the limbic fissure; R, R0 , fissure of Rolando; F, frontal lobe; S, S, fissure of Sylvius; T, temporal lobule of the parietal lobe; P0, parietal post-Rolandic convolution; P1, P1, Sylvian convolution; P3, sagittal convolution; p, primary parietal sulcus. The parietal convolutions are numbered starting at the fissure of Sylvius according to Leuret’s method. The two convolutions P3 and P4 result from the division of P3 in the fox (see Fig. 12, p. 429[p. 2522 of the English translation]).

Figure 19. Ratter. Lateral surface of the left hemisphere, in which the fissure of Sylvius has been expanded and the arc of Sylvius moved aside to reveal the Sylvian fossa. The deep surface of the Sylvian convolution, P1, P1, that becomes visible has been shaded. S0 , a, inferior or temporofrontal subsylvian fold; S0 , S, b, superior or temporoparietal subsylvian fold. Other letters as in Figure 18.

merges with the lobe of the corpus callosum. It begins with a root of varying width, sometimes rather narrow, that is sometimes singular and sometimes divided into two. We saw that it is singular in the otter (Fig. 2, No. 9, p. 401 [p. 2508 of the English translation]; Fig. 4, No. 9, p. 405 [p. 2510 of the English translation], Fig. 1, c, p. 399 [p. 2507 of the English translation]). It is also singular in the tapir, in the dog where it is deep, in the marten, the fox, the cat, etc. It is very short and does not reach the edge of the hemisphere toward which it travels, but, if we turn over the hemisphere, we see that the great primary parietal sulcus begins on this edge in roughly the same area (see p. 427 [p. 2521 of the English translation]). The primary parietal sulcus travels from there on the convex surface of the hemisphere up to the anterior end; it separates the sagittal region from the Sylvian region. This part of the posterior edge of the hemisphere can be considered a pole around which the longitudinal convolutions originate and by means of which they all connect more or less directly with one another and with the retrolimbic annectant. The norma lateralis, norma verticalis, and norma basalis of the hemisphere do not display this arrangement, but it can be observed from the norma occipitalis. We know that, in the majority of mammals other than primates, the cerebellar surface or tentorial surface of the hemisphere is greatly elevated and becomes more or less posterior, because the cerebellum is located more or less at the back of the brain. In the tapir, this surface is located completely posteriorly,

and the constitution of the pole of the hemisphere can be studied easily. Figure 20 shows the posterior surface of the left hemisphere of the tapir. The posterior extremity of the great limbic lobe, C, H, can be seen circumventing the cerebral peduncle, M, which has been cut a little on the inside of where it enters the hemisphere. The lobe of the corpus callosum, C, and the hippocampal lobe, H, are continuous with one another at the retrolimbic annectant convolution, a. The retrolimbic annectant convolution interrupts the limbic fissure, of which the inferior arc, L, travels downward and outward and the superior arc, L0 , travels upward and inward to arrive at the medial surface of the hemisphere (where it can be located again in Figure 23, p. 447 [p. 2530 of the English translation]). The retrolimbic annectant convolution ends at the pole of the hemisphere, b, b0 , b00 , from which three longitudinal sulci originate to divide the parietal lobe into four convolutions. The middle sulcus, or primary parietal sulcus, p, separates the two medial convolutions (the sagittal grouping), Sa, from the two lateral convolutions (the Sylvian grouping), Sy. It is located opposite the retrolimbic annectant convolution, but it does not reach it, being separated from it by a transverse fold, b0 , b00 , which connects the origins of the two medial convolutions with those of the two lateral convolutions. When the posterior surface of the brain is less elevated, and the mass of convolutions extends above the cerebellum, the various sulci that end at the pole are turned and twisted to some degree, but these sulci never

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Figure 21. Roe deer. Medial surface of the right hemisphere. O, olfactory lobe; H, hippocampal lobe; C, C0 , C00 , lobe of the corpus callosum; F, frontal lobe; P, parietal lobe; L, inferior arc of the limbic fissure; L0 , L00 , superior arc of the limbic fissure; L000 , subfrontal sulcus; a, retrolimbic annectant convolution; k, very short calcarine sulcus.

Figure 20. Tapir. Posterior or tentorial surface of the left hemisphere. M, cerebral peduncle, cut close to where it enters the hemisphere; B, great cleft of Bichat; H, posterior end of the hippocampal lobe; C, posterior end of the lobe of the corpus callosum; L, inferior arc of the limbic fissure; L0 , superior arc of the limbic fissure; a, retrolimbic annectant convolution; b, b0 , b00 , transverse fold of the pole of the hemisphere; p, primary parietal sulcus; Sa, origin of the two convolutions of the sagittal grouping; Sy, origin of the two convolutions of the Sylvian grouping.

extend to the limbic fissure. They are separated from the fissure by a somewhat sinuous transverse fold that establishes continuity among all the parietal convolutions at their posterior extremities, from which they originate. This fold is always connected with the great limbic lobe by the retrolimbic annectant convolution, which can consequently be considered to be the common root of the parietal convolutions. I have stated that the retrolimbic annectant convolution is singular in carnivores, as it is in the tapir, but this is not always true. Sometimes it is divided lengthwise by a longitudinal sulcus that is analogous to the calcarine fissure in primates and thus merits some attention. This sulcus is more or less well-developed in most of the pachyderms that I have been able to procure and in all of the ruminants. It is only rudimentary in the roe deer (Fig. 21). The retrolimbic annectant convolution, a, which interrupts the limbic fissure, L, L0 , travels toward the posterior edge of the hemisphere, but before it reaches the edge it is divided into two parts by a small

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sulcus, k. The superior part is located between k and L0 , and it provides, on the adjacent portion of the convex surface, the origin of the two convolutions of the sagittal grouping. The inferior part is located between k and L, and it likewise provides the origin of the two convolutions of the Sylvian grouping. As for the small sulcus k, it does not extend to the base of the fold nor to the edge of the hemisphere. The sagittal root and the Sylvian root connect behind it, and, on turning over the hemisphere, we see that the direction in which it travels is toward the pole. In Figure 15 (p. 434 [p. 2524 of the English translation]), which shows the lateral surface of the right hemisphere of the roe deer, the pole is labelled b. The bifurcated posterior extremity of the great primary parietal sulcus, p, that separates the sagittal grouping from the Sylvian grouping also ends there. The sulcus k marks the same separation on the posteroinferior surface of the hemisphere. The two sulci thus form a single system. Nevertheless, they are never continuous, because the pole of the hemisphere always comes between them in the form of a fold extending from the sagittal root to the Sylvian root. Further on, I will demonstrate that the small sulcus k is analogous to the great calcarine fissure in primates. I therefore ask leave to call it the calcarine sulcus, even though the spur (calcar), or hippocampus minor, from which its name derives exists only in primates. The calcarine sulcus is barely longer in the goat than in the roe deer and in the sheep than in the goat. In the deer and the antelope, it reaches a length of 15 millimeters by extending further and further toward the base of the retrolimbic annectant convolution. Finally,

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

in the camel and especially in the horse (Fig. 22, k), it completely divides the fold down to its base in such a way that it reaches the great limbic lobe, as the calcarine fissure does in primates. There are thereby two retrolimbic annectant convolutions, a superior annectant convolution, a, for the sagittal grouping, and an inferior annectant convolution, a0 , for the Sylvian grouping. The former represents the cuneolimbic fold in primates (which is deep in humans and gibbons); the latter represents the convolution in primates that forms the inferior edge of the calcarine fissure (and that is the fifth occipital convolution in humans and apes). At its posterior extremity, the calcarine sulcus of the horse reaches the tip of the hemisphere, where it is turned back by fold b, which connects the sagittal grouping to the Sylvian grouping. The three longitudinal sulci of the convex surface end or, rather, begin, along this long and sinuous fold: 1) the great primary parietal sulcus, p, which separates the Sylvian grouping from the sagittal grouping (sulcus p, p in Fig. 14, p. 433 [p. 2523 of the English translation]); 2) the lateral parietal sulcus, e, which separates the two convolutions of the Sylvian grouping from each other (sulcus e, e, e, e in Fig. 14, where it is interrupted by several annectant convolutions); and 3) the medial parietal sulcus, f, which separates the two convolutions of the sagittal grouping from each other (sulcus f, f in Fig. 14). In the horse, several longitudinal sulci, g, g (Fig. 22), exist independently of the sulci of the lateral surface; they all originate somewhere above the calcarine sulcus and divide the medial surface of the sagittal convolution into many secondary folds. The posterior extremity of the horse brain is thus very complex, but it is certain that all the parietal convolutions originate around the calcarine sulcus and consequently trace their origins to the posterior and inferior part of the great limbic lobe, via the intermediary of the two branches of the retrolimbic annectant convolution. The limbic fissure is interrupted by this annectant convolution and then immediately resumes its path around the superior arc of the great lobe, i.e., around the lobe of the corpus callosum, following its convexity and more or less separating it entirely from the neighboring convolutions. We have already seen (p. 405[p. 2510 of the English translation]) that this lobe originates in the inferior part of the medial surface of the hemisphere, in front of the optic chiasm and behind the base of the olfactory lobe. The medial olfactory root ends at this origin, where, incidentally, the inferior and medial part of the frontal lobe attaches (p. 406 [p. 2510 of the English translation]). From there, the lobe of the corpus callosum travels upward and forward, forming an ascending section, and then it curves around

Figure 22. Horse. Medial surface of the right hemisphere. O, olfactory lobe; H, H0 , hippocampal lobe; C, C0 , C00 , lobe of the corpus callosum; F, F, medial surface of the frontal lobe; P, medial surface of the parietal lobe; L, inferior arc of the limbic fissure; L0 , L00 , L000 , superior arc; L0 , L00 , parietal section, or subparietal fissure; L00 , L000 , frontal section, or subfrontal fissure; a, a0 , retrolimbic annectant convolution, divided in two by the calcarine sulcus, k; b, pole of the hemisphere; p, origin of the primary parietal sulcus; e, origin of the lateral parietal sulcus; f, origin of the medial parietal sulcus; i, medial frontoparietal groove.

the genu of the corpus callosum and travels toward the back, forming a horizontal section, C0 (Fig. 22). Finally, it curves a second time, behind the splenium of the corpus callosum, forming a descending section, C00 , which merges with the hippocampal lobe at the retrolimbic annectant convolution. The ascending section always increases in size from bottom to top. The descending section presents variations in size that are not very significant despite being rather extensive. The size of the horizontal section is noteworthy, however; in osmatic mammals this section increases in size from back to front,26 whereas in primates the opposite is true; it increases in size from front to back. The ascending section of the lobe of the corpus callosum is always connected to the frontal lobe, which, furthermore, extends for a variable distance on the anterior portion of the horizontal section. The parietal lobe covers the rest of the horizontal section and the entire descending section. The limbic fissure is thus composed of two parts, which correspond to the frontal lobe and the parietal lobe, respectively, and can be called the subfrontal fissure and the subparietal fissure. These two parts of the limbic fissure are sometimes continuous with one another and sometimes separated by an interruption of varying distance. In the first case,

26

There are hardly any exceptions to this rule. Although in the tapir the horizontal section maintains a nearly uniform size throughout most of its expanse, there is at least a definitive enlargement at the very front, above the genu of the corpus callosum (see Fig. 23).

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the limbic fissure forms a complete arc around the lobe of the corpus callosum; in the second case, the arc is incomplete. On this basis, I will next examine two distinct models. 1. The first model is observed in the horse, the tapir, and the elephant: I will describe it based on the horse, for which it is presented very succinctly (see Fig. 22). The inferior arc of the limbic fissure, L, comes to a stop at the retrolimbic annectant convolution, a, a0 , above which the fissure resumes its trajectory. It climbs from L0 to L00 beneath the sagittal convolution of the parietal lobe; this is its subparietal section. From L00 to L000 , its path runs beneath the medial surface of the frontal lobe; this is its subfrontal section. These two parts of the limbic fissure merge with each other without interruption; both of them are very deep. I have studied them in a brain cut into 16 transverse sections, and I kept the drawings. Their depth never measures less than 6 millimeters, and can be up to 12 millimeters. There is no difference between the subparietal section and the subfrontal section under this connection. The limbic fissure thus runs along the entire convex edge of the corpus callosum; this edge is very slightly sinuous but does not present any grooves. Many grooves, however, are observed emanating from the limbic fissure on the corresponding edge of the extralimbic mass. Among these grooves, there is one located at L00 , above the boundary between the frontal lobe and the parietal lobe; this is the medial frontoparietal groove. It is located a great distance from the anterior extremity of the hemisphere, because the frontal lobe of the horse, already large on the lateral surface, becomes very large on the medial surface. This groove points upward and forward. It is short and does not reach the sagittal edge of the hemisphere; it stops at a small annectant convolution that extends from the frontal lobe to the parietal lobe and does not exist in this area except in ungulates. Above this annectant convolution, however, the groove reappears in the form of a large slanted fissure that reaches the superior edge and continues on, ending up on the convex surface. Here it adopts a transverse direction, thus demonstrating a characteristic analogous to that of the “cruciate sulcus” in carnivores. The lobe of the corpus callosum is divided by a rather long but incomplete longitudinal sulcus; this sulcus shows that the lobe of the corpus callosum in the horse has not escaped folding entirely. The sulcus is very superficial, though, and averages only 2 millimeters in depth, whereas the sulci in the mass of convolutions are often more than 2 centimeters deep. Even in this animal, with its many convolutions, the lobe of the corpus callosum proves to be resistant to folding of the mantle.

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Figure 23. Tapir. Medial surface of the right hemisphere. O, olfactory lobe; H, hippocampal lobe; C, C0 , C00 , lobe of the corpus callosum; L, inferior arc of the limbic fissure; a, retrolimbic annectant convolution, L0 , L00 , L000 , superior arc of the limbic fissure; F, frontal lobe; P, P, parietal lobe; b, deep frontolimbic annectant convolution; i, medial frontoparietal groove.

Following the major development of the medial surface of the frontal lobe, the subfrontal fissure in the horse is not just as long as the subparietal fissure; it is in fact even longer. The opposite is seen in the tapir and the elephant. In the tapir (Fig. 23), the lobe of the corpus callosum, C, C0 , C00 , is very large and makes up nearly the entire medial surface of the hemisphere. Furthermore, the frontal lobe is very small and only rests upon the ascending section of the corpus callosum, without extending onto the horizontal section. The medial frontoparietal groove, i, is thus transported all the way forward, even a little further forward than the anterior genu of the corpus callosum. It almost reaches the sagittal edge, and it continues on to form a “cruciate sulcus” on the convex surface located right near the anterior tip of the hemisphere. By contrast, the lobe of the corpus callosum in the elephant is very narrow; in a way it is stuffed under the enormous mass of the frontoparietal convolutions that press down upon it. Moreover, the superior arc of the limbic fissure is interrupted in several places, in front, above, and behind, by several annectant convolutions that extend from the lobe of the corpus callosum to the adjacent mass of convolutions. The number, position, and size of these annectant convolutions and the limbic grooves that exist at their base are highly variable. I have studied them in both hemispheres of a young Indian elephant27 as well as in the right hemisphere of an adult of the same species; the latter was cured in nitric acid

27

This brain was given to the laboratory by Mr. Tramond, a naturalist on Rue de l’ Ecole-de-Medicine. I take this opportunity to thank Mr. Tramond very sincerely for the attentive and altruistic support he provides our research; we owe a significant portion of our collection of brains to him.

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

and given to the laboratory by Mr. Mathias Duval. They are very different in these three specimens, as well as in the brain described by Leuret. These folds are therefore completely secondary details, and the variability in their arrangement prevented me from determining exactly which of the limbic grooves in the elephant brain represents the medial frontoparietal groove in the horse and tapir. However, although the superior arc of the limbic fissure in the elephant is not continuous, in reality it forms only a single path, so it is included under the same model as the horse. In this type of animal, the relative size of the lobe of the corpus callosum is highly variable, but it is always smaller than the medial surface of the hemisphere, so this lobe and the limbic fissure surrounding it never reach the sagittal edge. Nonetheless, they get very close in the tapir (see Fig. 23), and adding 2 or 3 millimeters more to the front and top of the corpus callosum would suffice for it to reach the sagittal edge and become visible on the superior surface of the hemisphere. In the second model of the limbic fissure, this has been achieved. 2. This second model, which is incomparably more frequent than the first, is observed in many pachyderms, in all the ruminants I have studied (even in cattle, despite appearances), and finally in all carnivores, with no exceptions. It is characterized 1) by a frontolimbic annectant convolution that separates the subparietal section of the limbic fissure from the subfrontal section; 2) by the fact that the subfrontal fissure is very incomplete and very superficial, whereas the subparietal fissure is very large and very deep; and 3) by the previously mentioned fact that the anterior portion of the lobe of the corpus callosum becomes large enough to rise up to the sagittal edge and form a part of the superior surface of the hemisphere beyond that edge (see p. 407 [p. 2523 of the English translation], Fig. 5, superior surface of the otter brain). The result is that the subparietal fissure climbs at least to the sagittal edge and almost always passes it in extending some amount on the superior surface of the hemisphere, where it forms Leuret’s “cruciate sulcus.” All of these characteristics are very obvious in all carnivores. They are no less obvious in the pig, from the pachyderms, or, in the goat, sheep, deer, and antelope, from the ruminants. They are a little different in other ruminants, however. The subparietal fissure in the roe deer (Fig. 21) climbs up to the sagittal edge but does not pass it and does not produce the “cruciate sulcus.” Otherwise, it is still separated from the subfrontal fissure by a very large annectant convolution, and the subfrontal fissure is very superficial and is no more than a slight sulcus, L00 , the subfrontal sulcus. In the

camel, the anterosuperior portion of the lobe of the corpus callosum, although very voluminous and divided into subsections, barely reaches the sagittal edge and only in the very front, i.e., almost at the tip of the hemisphere. However, the very long subparietal fissure extends transversely over this area. The frontal lobe is extremely diminished, but it is nevertheless connected to the lobe of the corpus callosum via two superimposed annectant convolutions that separate the subparietal fissure from the subfrontal fissure. The subfrontal fissure is short but rather deep. The same arrangement is found in the steer, except that there is only a single frontolimbic annectant convolution, which is small and narrow, and the subparietal fissure does not extend onto the convex surface. The result is that the subparietal fissure and the subfrontal fissure describe an almost complete curve on the medial surface of the hemisphere; the curve is interrupted only by a small superficial fold located exactly in the place where a rudimentary and deep frontolimbic annectant convolution is found in the brain of the tapir (Fig. 23, b). It would even appear that this fold is not always superficial in the steer, because it is not shown in Leuret’s drawing.28 Whatever the case, the tapir and the steer present a two-part transition between the limbic model of the horse and that of the carnivores. In carnivores especially, the lobe of the corpus callosum is seen to increase in size from back to front, with its anterior portion merging with the frontal lobe. The major development of this anterior portion seems to be related to the very important role that the olfactory system plays in carnivores. The subfrontal fissure is represented only by a very superficial sulcus, the subfrontal sulcus (Fig. 24, SF); it is so greatly reduced that it would not be recognized as the vestige of the limbic fissure if not for the guidance from studying the brains of pachyderms and ruminants. The frontolimbic annectant convolution does not take on the form of a fold; rather, it is a pure and simple fusion of the lobe of the corpus callosum and the frontal lobe, with the smooth and flat surfaces merging directly with one another. By contrast, the subparietal fissure, SP, is large and deep. To examine it thoroughly, it must be expanded to push the oblique overlapping edge of the sagittal convolution outward. Figure 25 shows a mold that was taken in this state of the medial surface of the brain of a ratter [probably a terrier]. To reiterate, the dog and the wolf appear to lack the retrolimbic annectant convolution; in these animals, the inferior arc of the limbic

28 Analyse comparee du syste`me nerveux [Comparative Analysis of the Nervous System], Atlas in-fol., pl. IX. Revue d’Anthropologie [Journal of Anthropology], 3rd series, Vol. I.

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Figure 24. Fox. Medial surface of the right hemisphere. C, C0 , C00 , lobe of the corpus callosum; a, retrolimbic annectant convolution; F, frontal lobe; P, parietal lobe; SF, subfrontal sulcus; SP, subparietal fissure; b, frontolimbic annectant convolution; d, position of the anterior parietolimbic annectant convolution, which is deep.

fissure is continuous with the subparietal fissure without any visible interruption. When the subparietal fissure is dilated, however, the retrolimbic annectant convolution, a, comes into view; as always, it is located where the lobe of the corpus callosum and the hippocampal lobe come together and has its usual connections, except that it is deep.29 From L to L0 , the subparietal fissure runs along the descending section of the lobe of the corpus callosum. At L0 , it bends above the horizontal section of the lobe; here there is a deep annectant convolution, c, that extends from the lobe of the corpus callosum to the sagittal convolution. This fold is very deep in large dogs but is developed enough in small dogs (miniature bull terriers and Havanese) to become superficial. Further forward, in the vicinity of a parietal groove that is constant in dogs and is also found in the fox, another deep annectant convolution, d, crosses the limbic fissure and connects the lobe of the corpus callosum to the sagittal convolution, Sa. This annectant convolution is superficial in cats, but it is deep in all the other carnivores I have been able to examine. The two annectant convolutions, c and d, can be called the posterior and anterior parietolimbic annectant convolutions. Their existence in carnivores is the first degree of the fusion of the lobe of the corpus callosum and the sagittal fissure that occurs in primates and makes the subparietal fissure almost completely disappear. After furnishing the anterior parietolimbic annectant convolution, the subparietal fissure continues its trajec-

29

The retrolimbic annectant convolution is also deep in some cetaceans (dolphin), but it is superficial in other cetaceans (porpoise).

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Figure 25. Ratter. Medial surface of the right hemisphere. The subparietal fissure has been spread open to show the deep annectant convolutions. O, olfactory lobe; H, hippocampal lobe; C, C0 , C00 , lobe of the corpus callosum; F, F, frontal lobe; P, P, parietal lobe; T, temporal lobule of the parietal lobe; L, inferior arc of the limbic fissure, continuing with the superior arc (this continuity exists only in the dog, the wolf, and the dolphin); L, L0 , L00 , subparietal fissure; L000 , subfrontal sulcus; Sa, Sa, medial surface of the sagittal convolution; a, retrolimbic annectant convolution; it is deep; c, posterior parietolimbic annectant convolution; it is deep; d, anterior parietolimbic annectant convolution; it is deep; b, frontolimbic annectant convolution.

tory up to L00 , gradually climbing in such a way as to cross the sagittal edge and form Leuret’s cruciate sulcus (cruciate fissure) on the convex surface.

Figure 26. Fox. Superior surface of the brain. O, olfactory lobe; R, fissure of Rolando; F, frontal lobe; P, P0 , parietal lobe; C, anterosuperior extremity of the lobe of the corpus callosum, left white. L, cruciate fissure, formed by the anterosuperior extremity of the subparietal fissure; p, primary parietal sulcus; S, superior and posterior extremity of the fissure of Sylvius. 1 to 4, the four parietal convolutions, numbered according to Leuret.

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

The cruciate sulcus exists in all carnivores. It is bounded behind by the sagittal convolution and in front by the superior and anterior portion of the lobe of the corpus callosum (see Fig. 26, fox brain). This portion of the great limbic lobe that appears on the convex surface of the hemisphere, and that is left in white in the diagram, merges in front with the frontal lobe, F, and laterally with the anterior extremity of the sagittal convolution, P, P0 , and with the post-Rolandic fold, where all the parietal convolutions successively come to an end. The post-Rolandic fold is analogous to the ascending parietal convolution in primates. The anterior extremity of the subparietal fissure also forms a “cruciate sulcus” in the pig, deer, goat, sheep, and antelope. There is also a cruciate sulcus in the tapir and camel, but it is formed by the frontoparietal groove of the subparietal fissure, and not by the fissure itself. We have been obliged to carry out a detailed examination of the connections of the great limbic lobe and the limbic fissure, as well as the convolutions that end there, in osmatic gyrencephalic mammals. These developments are necessary in understanding the nature of the differences that occur when we move up to the primate brain. These differences can be classed into two groups; some result from the atrophy of the olfactory system; others result from the enormous growth of the frontal lobe. In primates, the combination of these two causes can make it difficult to determine which is responsible for each difference, but we can study the first cause in isolation in animals in which the olfactory system is rudimentary or nonexistent but in which the frontal lobe is not exaggerated in size. These animals are the aquatic mammals.

6. ANOSMATIC BRAINS OF AQUATIC MAMMALS I am not at all suggesting that I describe the brain of aquatic mammals here, or that I establish a comparison between their convolutions and those of other mammals. I believe it is possible to demonstrate that convolutions as complex as those in cetaceans, as unique as they are, can be reduced to a model that is not so different from that of ungulates and large pachyderms; those of amphibious mammals (the seal family) are associated with the carnivore model. However, this double demonstration would require lengthy development that would take us far off track, since we have to be concerned with convolutions only in terms of their relationships with the great limbic lobe. It will therefore suffice to study the modifications that are the

Figure 27. Dolphin. Inferior surface of the left hemisphere. R, R, fissure of Rolando; S, S0 , fissure of Sylvius; P, P0 , P00 , parietal lobe; F, inferior surface of the frontal lobe; D, desert lobule of the frontal lobe (olfactory desert); V, valley of Sylvius; H, atrophied hippocampal lobe; C00 , lobe of the corpus callosum; L, L0 , inferior arc of the limbic fissure; L0 , L00 , superior arc of the limbic fissure, seen foreshortened; T, temporal pole of the temporal lobule (or lobe); B, optic band. (This letter B, omitted by the engraver, was placed between T and L.)

consequence of the atrophy or destruction of the olfactory system. This system is completely nonexistent in cetaceans in the dolphin family. Everything has disappeared, not only the olfactory lobe, but even the olfactory nerve filaments, such that the “cribriform plate” of the ethmoid bone is not perforated. The great limbic lobe is therefore composed of no more than two parts, the hippocampal lobe and the lobe of the corpus callosum. Anatomists who were unaware of the anatomical and functional cohesion of the hippocampal lobe and the olfactory lobe would have reached a different conclusion had they studied the brains of dolphin-like cetaceans. In these animals, there is no olfactory system, and the hippocampal lobe is reduced to the minimum size. It is smaller not only than in amphibious mammals but even than in primates. It is very short and so narrow (Fig. 27, H) that it would be easy to confuse it with

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the numerous thin subdivisions of the adjacent convolutions. Nevertheless, its lateral edge is clearly bordered by the limbic fissure, L, L0 , which is directly continuous from L0 to L00 around the lobe of the corpus callosum, C00 . The retrolimbic annectant convolution is located, as always, where the two lobes join at L0 , but it is deep in the dolphin, as in the dog and the wolf. By contrast, this fold is superficial in the porpoise, in which the brain is otherwise very analogous to the dolphin brain. The hippocampal lobe in the dolphin is not only atrophied; it has furthermore lost some of its independence. The limbic fissure that borders it does not run along its anterior extremity, which is fused at T with the adjacent convolutions. This fusion is in a way the first stage of the formation of the temporal lobe, which is achieved only in primates. The fusion occurs on the posterior and inferior edge of the fissure of Sylvius, S, in the area that corresponds to the temporal lobule of the parietal lobe in osmatic animals. It is a matter of knowing whether this part of the mantle should continue to be called the temporal lobule in the dolphin or if it wouldn’t be more appropriate to call it the temporal lobe already, because it is certainly very close to the model observed in primates. For it to be a matter of having achieved the model of the temporal lobe primates have, it would suffice for the anterior extremity T to extend a little further forward, above the valley of Sylvius. Aside from this, the sulci located outside the limbic fissure, L, can be seen converging along with the fissure toward T, which is consequently analogous to the temporal pole in primates. The fissure of Sylvius, S, S0 , angles sharply back, climbs up to its posterior section, and extends onto the lateral surface. Slightly outside the temporal pole, a large and deep fissure breaks away from the anterior section and travels forward and slightly outward; this is the fissure of Rolando, R, which separates the great parietal lobe, P, P0 , P00 , from the frontal lobe, F. The frontal lobe, although rather wide, does not fill the entire width of the inferior surface of the hemisphere. It is divided by many sulci in front, but it is completely smooth in back, over an expanse that makes up roughly one-third of its total length. The absolute simplicity of this wide surface contrasts quite drastically with the great complication of the rest of the mantle. The smooth surface is comparable to a desert surrounded by fertile lands on a geographic map. This portion of the frontal lobe of cetaceans can therefore be called the desert lobule or even the olfactory desert. There is no doubt that the lack of any kind of convolution or sulcus is the consequence of the total absence of the olfactory system. Recall that, every time the olfactory lobe is present, it inserts into the posterior extremity of

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the orbital surface of the frontal lobe, immediately in front of the quadrilateral space, by means of a double strip (gray and white) of brain matter that I call the superior olfactory root (p. 402 [p. 2509 in the English translation]). The posterior portion of the frontal lobe, where this insertion occurs, must therefore play a part in olfactory function, because it is through this area and through this area only that the olfactory lobe communicates directly with the intellectual brain. It is likely that the area’s role consists of interpreting, analyzing, and transforming the olfactory impressions that it receives into ideas. This role is independent of the size of the olfactory system, and, indeed, we see that in amphibious mammals and primates, in which the olfactory system is greatly atrophied, the posterior portion of the orbital surface of the frontal lobe is no more or less complicated than the rest of the mantle. The convolutions and sulci extend into the area, and it does not form a special lobule,30 because its constitution is no different from the constitution of the anterior portion. In cetaceans, however, this portion of the frontal lobe, the olfactory function of which has been wiped out, undergoes the most complete atrophy possible; its cortex no longer shows even the slightest fold, and its surface, now totally smooth, seems to indicate that it has lost its activity and that no new function has come to take the place of the one that was suppressed. The nature of this change is expressed in the term olfactory desert. In the porpoise, the olfactory desert extends further forward and back than in the dolphin; it nevertheless does not fill the entire length of the orbital surface, insofar as a longitudinal sulcus dominates the anterior half of this surface. Just as the absence of the superior olfactory root leads to the flattening of the desert lobule, the absence of the three inferior roots, and particularly the gray or middle root, leads to the depression of the valley of Sylvius. This transverse depression corresponds to the quadrilateral space in osmatic mammals, which is not very deep; properly described, it is not actually a depression but rather no more than a difference in elevation resulting from the great depth of the hippocampal lobe, which forms a projection over the posterior edge of the quadrilateral space. In cetaceans, however, the atrophied hippocampal lobe has only a slight thickness, and, if the valley of Sylvius is hollowed out, it is because the quadrilateral space is deeply caved in. The

30

Nevertheless, we note that, in gyrencephalic primates, the transverse groove called the H-shaped sulcus is always present. We can posit that the part of the orbital lobule located behind this groove is involved in olfaction and represents the desert lobule in dolphin-like cetaceans.

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

thick layer of gray matter and white fibers that formed the middle olfactory root is now reduced to a very thin layer of gray matter that intermingles with the inferior surface of the corpus striatum, the vessels of which span the layer as if forming a sieve. The quadrilateral space is thus transformed into the locus perforatus. The valley of Sylvius is therefore deep and wide; inside, it extends as always to the medial edge of the optic chiasm, but its connections are different at its lateral extremity. The lateral olfactory root that borders it in osmatic mammals and separates it from the fissure of Sylvius is absent. Consequently, the large and deep valley of Sylvius is directly continuous with the large and deep fissure of Sylvius under the tip of the temporal lobule. These two crevices now form only a single crevice that begins behind the lateral surface of the hemisphere, descends at an angle to the base of the brain, crosses it transversely, and continues on to end at the lateral edge of the chiasm. On the medial surface of the cetacean brain, the lobe of the corpus callosum goes around the limbus of the hemisphere as usual. It is bordered along its entire length by a large and deep limbic fissure that travels uninterrupted under the parietal lobe and under the frontal lobe, describing a complete arc, in accordance with the first limbic model described above (p. 446 [beginning on p. 2529 in the English translation]) in the horse, tapir, and elephant. In this aspect and in several others as well, the cetacean brain model is linked to the pachyderm model, and we could wonder whether cetaceans are not modified pachyderms, as amphibious mammals are modified carnivores. I should highlight a fact here that is rather difficult to reconcile with the cohesion that I feel exists in other animals between the olfactory system and the anterior portion of the lobe of the corpus callosum. This anterior portion, neighboring the origin of the medial olfactory root, is highly developed in osmatic mammals and is larger than the posterior portion of the lobe. In primates, however, this is the part that is the narrowest, and it seems likely that the atrophy that has occurred there is related to the atrophy of the medial olfactory root. However, although this root has not just atrophied but actually vanished completely in cetaceans, the anterior portion of the lobe of the corpus callosum has not atrophied at all; it is just as well-developed as in osmatic mammals. It is even traversed by numerous grooves, indicative of very pronounced functional activity. Is the advanced anterior development of the lobe of the corpus callosum due to the extremely small size of the frontal lobe, which is almost reduced to its orbital stage and extends only a very small amount on the convex surface of the hemisphere? The lobe of the corpus callosum would, in a

kind of compensation, fill the empty space left after this extreme reduction of the frontal lobe. Could we even accept that some other function would have developed in this part of the lobe of the corpus callosum that became available when olfactory function disappeared? Whatever the answer, it is noteworthy that, both in physical structure and in the nature of the limbic fissure surrounding it, the lobe of the corpus callosum in cetaceans proves highly analogous to this lobe in pachyderms. Now we will focus on amphibious mammals. Their olfactory function has not vanished; but it has atrophied considerably. Nevertheless, it is less rudimentary than it is in primates, and the [anterior] portion of the lobe of the corpus callosum is a little less atrophied as well. To appreciate this decrease in size, we have to imagine that the seal brain is associated with the carnivore model; we must therefore compare it with carnivore brains. The medial surface of the hemisphere of a seal brain is shown in Figure 28. We have not forgotten that the lobe of the corpus callosum increases significantly in size from back to front in carnivores; the anterior portion is developed to the point that it rises to the sagittal edge of the hemisphere and even appears on the convex surface in such a manner that the subparietal fissure goes on the form the “cruciate sulcus” (see p. 452 [p. 2532 in the English translation], Fig. 26, fox brain, and p. 407 [p. 2511 in the English translation], Fig. 5, otter brain) on the convex surface. Furthermore, the subfrontal fissure, L000 (Fig. 25, p. 451 [p. 2532 in the English translation]), is no longer anything but a slight sulcus (S, F, Fig. 24). It does not connect with the subparietal fissure, L00 ; it is separated from it by the frontolimbic annectant convolution, b. The essential qualities of these characteristics are found again in amphibious mammals. However, the subparietal fissure does not rise to the sagittal edge, and consequently it does not go on to form the “cruciate sulcus”; the anterior portion of the lobe of the corpus callosum therefore does not extend to the convex surface of the hemisphere. This proves that it has undergone a great reduction in size. Despite this reduction, it remains as large as the rest of the lobe of the corpus callosum in the seal. In the sea lion, however, it is narrower, and the lobe of the corpus callosum decreases in size from back to front as in primates. As for the frontolimbic annectant convolution, it is divided into two secondary folds, b and b0 , by a rather large sulcus, d, d0 . This sulcus extends into the depth of the lobe of the corpus callosum up to a short distance from the groove of the corpus callosum and consequently divides the lobe through almost its full depth. In the seal, there is still a flap of some size between the groove and the posterior

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extremity of the sulcus d, d0 . This flap is already thinner in the right hemisphere of our sea lion brain, however, and it is lacking entirely in the left hemisphere, where the sulcus d, d0 connects with the groove of the corpus callosum. In this last case, which might be abnormal, it is the only time I have seen the continuity of the lobe of the corpus callosum interrupted by a sulcus (moreover, this is only superficial). Whatever the situation, the sulcus d, d0 that extends into the depth of the lobe of the corpus callosum is a characteristic that is specific to amphibious mammals. It establishes a very distinct dividing line between the subfrontal portion of the lobe, C, C0 , and the subparietal portion of the lobe, C00 , and I am inclined to believe that this arrangement is related to the atrophy of the olfactory lobe. If this were the case, we could hypothesize that the dividing line that the sulcus d, d0 establishes between the two parts of the lobe of the corpus callosum in amphibious mammals is not only anatomical but also functional and that the subfrontal portion C, C0 is involved in olfactory function to the exclusion of the other portion. Finally, the analogy would lead us to presume that in other animals, when the anatomical dividing line does not exist, the distribution of functions nevertheless remains the same and that the olfactory function of the lobe of the corpus callosum is still limited to the subfrontal portion. Examining the inferior surface of the cetacean brain has already shown us how the lack of the olfactory lobe changes the constitution of the valley of Sylvius and transforms it into a very deep transverse fissure that continues outward with the fissure of Sylvius. The simple atrophy of the olfactory lobe leads to a similar change in amphibious mammals. Figure 29 shows the inferior surface of the right hemisphere of the seal brain. The olfactory lobe forms no more than a small ganglion, O, the narrow peduncle of which divides into two divergent roots in the back, one medial and the other lateral. The lateral root follows a sharply angled path outward and joins the lateral part of the anterior extremity of the hippocampal lobe, H. The point where this junction occurs is not visible in Figure 29; it is located deep along the medial edge of the anterior extremity of the limbic fissure, L, L0 . Between these two olfactory roots, on one hand, the chiasm, X, and the anterior extremity of the hippocampal lobe, there is the quadrilateral space, Q. In osmatic mammals, this quadrilateral space is formed by the middle olfactory root, a thick layer of gray matter crossed by the most anterior peduncular fibers that rests on the inferior surface of the corpus striatum. In amphibious mammals, there are no longer any peduncular fibers, the layer of gray matter is much thinner, and it merges with the inferior surface of the corpus striatum. Some number of small

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Figure 28. Seal. Medial surface of the right hemisphere. C, origin of the lobe of the corpus callosum; C, C0 , subfrontal portion of the lobe separated from the subparietal portion, C00 , by the sulcus d, d0 ; b, b0 , prelimbic annectant convolution, divided by sulcus d, d0 into two folds: the inferior or frontolimbic fold, b, and the superior or parietolimbic fold, b0 ; L0 , L00 , subparietal fissure; L000 , subfrontal fissure; F, frontal lobe; P, P0 , parietal lobe; m, optic band. The atrophied hippocampal lobe is not visible on the medial surface.

vessels (veins, I believe) issue from the corpus striatum and cross the layer as if forming a sieve. The quadrilateral space thus acquires the term perforated space in cetaceans and primates. The thin layer of gray matter that covers it receives a small gray flap up front that issues from the superior surface of the olfactory peduncle near where the two white roots meet31; the flap is very thin, very short, and very fragile. This is all that is left of the gray olfactory root of osmatic mammals. The locus perforatus is quite depressed and is located well below the level of the hippocampal lobe; it forms a very deep valley of Sylvius in front of it. In osmatic mammals, this transverse valley does not end at the limbic fissure; it is separated from it by the lateral olfactory root. In amphibious mammals, however, the lateral olfactory root is atrophied and no longer provides this separation. The valley, V, thus extends outward to the limbic fissure, L, which is met at this same place by the fissure of Sylvius, S, S0 . The result is that the fissure of Sylvius and the valley of Sylvius are directly continuous with one another, but when the edges of this crevice are spread apart, we see that the vestige of their separation still exists. It is represented by the long, thin lateral olfactory root, which descends

31

This small gray root is not visible in Figure 29; to see it, the olfactory peduncle must be lifted from front to back with utmost care. Then we see that the root inserts transversely into the posterior edge of the frontal lobe; it thus represents both the gray olfactory root and the superior olfactory root of osmatic brains. This arrangement is exactly the same in primates.

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

Figure 29. Seal. Inferior surface of the right hemisphere. O, olfactory ganglion (lobe); O0 , olfactory ribbon (peduncle) and its two white roots; H, hippocampal lobe; C00 , posterior extremity of the lobe of the corpus callosum; L, L0 , inferior arc of the limbic fissure; L0 , L00 , superior arc of the limbic fissure or the subparietal fissure; a, retrolimbic annectant fold; k, calcarine sulcus; d, position of a deep annectant convolution (which is superficial in the sea lion); X, chiasm; Q, locus perforatus; R, R0 , fissure of Rolando; V, valley of Sylvius, continuous outside with the fissure of Sylvius, S, S0 ; F, frontal lobe; P, parietal lobe; N, subsylvian lobule, partly superficial.

into the bottom of the valley, crosses it, and eventually plunges into the most lateral and anterior part of the hippocampal lobe. This alteration of the valley of Sylvius produces an arrangement that exactly resembles the one in primates in general and humans in particular except that, because the olfactory lobe is usually even further atrophied in primates than in amphibious mammals, the lateral olfactory root is diminished more in back and its

insertion into the hippocampal lobe is harder to see. This insertion can still be seen in brains that have been slightly hardened in nitric acid or even just in alcohol. Although we consider that the primate brain differs greatly from the amphibious mammal brain in other aspects, we are obliged to acknowledge that the utter similarity of their valley of Sylvius is the consequence of a common cause, and that this cause is the atrophy of the olfactory system. In amphibious mammals, the anterior edge of the valley of Sylvius, V, and of the lowermost part of the fissure of Sylvius is formed by the frontal lobe, F, as in primates. The frontal lobe extends outward to the fissure of Rolando, R, R0 , which extends almost to the fissure of Sylvius but does not reach it. The posterior lip of the Sylvian crevice is formed outside by the Sylvian parietal convolution, P, which is analogous to the first temporal convolution in primates, and inside by the hippocampal lobe, H, which is analogous to the hippocampal convolution in primates. The hippocampal lobe in amphibious mammals is small and flat, and, in comparison with the hippocampal lobe in osmatic mammals, we see that it has lost much of its importance. Furthermore, it is less distinct from the mass of convolutions because the limbic fissure, L, L0 , is very shallow; its depth especially decreases at point d in front of a small transverse sulcus, which borders a small annectant convolution that is deep in the seal but large and superficial in the sea lion. The sea lion hippocampal lobe is even smaller than the seal’s; the annectant convolution I have just mentioned therefore shows that it is less distinct as well. We see therefore that the hippocampal lobe tends to merge with the mass of convolutions as it atrophies, and this tendency toward fusion tells us that its function becomes less and less specialized. We will soon see that in primates, as the hippocampal lobe diminishes further and further in size, it forms no more than a convolution of the temporal lobe and that it merges more and more with the adjacent convolution. I do not believe I need to describe the rest of the inferior surface of the seal brain in detail. The meaning of the other explanatory letters is already familiar. Nevertheless, I add that the three elusive folds indicated by N are part of the subsylvian folds. These folds, which are deep in true carnivores, are partially superficial in amphibious mammals.

7. PRIMATE BRAIN We now have all the components we need to ascertain the distinctive characteristics of the primate brain. The order of primates includes four families—hominids,

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apes, Old World monkeys, and New World monkeys32— and constitutes a completely natural grouping characterized more by analogous structures than by morphological similarity. Naturalists who wanted to withdraw humans from the group to create their own separate order followed a fully sentimental idea that no anatomist could ever accept. If we wished to divide this grouping in the name of anatomy, the cut would have to be made between the fourth family (New World monkeys) and the three higher families. The characteristics that distinguish New World monkeys from other primates are so inconsequential compared with the characteristics that connect them to other primates, however, and are so far from having any ordinal value, that the order of primates seems to be one of the most natural orders in zoology. Nevertheless, there are differences in cerebral characteristics in this order that seem extensive at first glance. Essentially, we find the simplest lissencephalic brains alongside the most complex gyrencephalic brains, and, between these two extremes, all the intermediate stages of convolution development. Of course, if we were content with quickly glancing at the smooth brain of the marmoset, it would be tempting to believe it to be more similar to the brain of a small rodent than to the brain of the great apes, or even than to the brain of the capuchin monkeys. We could conclude not only that the layout of the brain was not in line with the ordinal characteristics but even that it was in flagrant contradiction of them. Many have reached this rather unsatisfying conclusion, and it would be irrefutable if we continued to view convolutions as the most essential component and the primary element in the constitution of the mantle of the hemisphere. However, we know now that this is not true. As previously explained (p. 413 [p. 2513 in the English translation] and p. 425 [p. 2519 in the English translation] et seq.), the folding of the mantle is not a primary phenomenon; it is the consequence of the expansion of the cerebral cortex, which, although guided by the connections of the cortex with the body and with the limbus of the hemisphere, is determined by the geometric law of the relationship between surfaces and volumes. In this respect, it is greatly influenced by the variations in size among the genera of the same family and the families of the same order. Without a doubt, the influence of size is not the only influence to affect the folding of the mantle; it is limited to acting on a given model in such a way as to

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The lemur family has been associated with the order since Linnaeus’s time, but cannot be kept there any longer. They are separated from this group by decisive embryological characteristics, as established by Mr. Alphonse Milne-Edwards.

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exaggerate or diminish the characteristics without ever having the power to transform them into another model. It therefore has limited effects, but it is sufficient to demonstrate that the presence or absence of convolutions and the degree of their simplicity or complexity are not an essential part of the constitution of a brain model. The primary division of the hemisphere is not the division that takes place in the extralimbic mass and creates its convolutions; it is the division between the great limbic lobe and the rest of the cerebral cortex. There can therefore be no greater difference between two brains than those concerning the constitution, connections, and degree of independence of the great lobe. These comments allow for a radical distinction to be made between the brain of lissencephalic primates and other lissencephalic animals. In the latter, the olfactory lobe is highly developed, and the relatively enormous hippocampal lobe is separated from the extralimbic mass by a limbic fissure that is still very apparent and very extensive and that often exists in the absence of any other cerebral crevice. This means that the hippocampal lobe is already distinct from the rest of the mantle even though all the other parts are still intermingled. In lissencephalic primates, however, these characteristics are replaced by a completely different set of characteristics. There is no longer a true olfactory lobe but rather a tiny ganglion that is no more than a rudiment of it. There is no longer a distinct hippocampal lobe; that is, the lobe is merged with the extralimbic mass, and the corresponding section of the limbic fissure has disappeared completely. This fusion shows that, as the hippocampal lobe lost its individuality, it lost its importance. We cannot attribute this just to a greater simplicity in the hemisphere, because the hemisphere has two large fissures that are absent in osmatic lissencephalic animals. These are the calcarine fissure and the fissure of Sylvius, which is directly continuous with the valley of Sylvius. The brain of lissencephalic primates thus belongs to a completely different model than the brain of osmatic lissencephalic mammals does. It differs in characteristics of major importance, and these characteristics link it definitely to the brain model of gyrencephalic primates. In moving up the series of monkeys from bottom to top—from the marmoset to the squirrel monkey, from the squirrel monkey to the capuchin, to the saki monkey, then to superior New World monkeys, to Old World monkeys, and finally, to apes and to humans—it would be easy to follow the development of the lobes and convolutions of the hemisphere throughout this long series. This is not the objective I have planned,

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

however. The comparative anatomy of the primate brain is already rather well known; the facts that I could add on the topic could be the subject of a specialized project, but they do not fit in here. What I propose to establish is that the fundamental characteristics of the brain remain the same throughout the entire series of primates amidst the great changes caused by the degree of folding of the mantle and also that the brain model of primates is completely different from the model of other mammals.33 At the same time, however, I will show that all the parts of the primate brain have analogous parts in other brains and vice versa; identifying these analogies will allow us to demonstrate that there is a brain model common to all mammals, and the various specialized models are merely derived from this general model. I have already provided the initial basis for this parallel by comparing lissencephalic primates with lissencephalic osmatic mammals. To finish drawing the parallel, we must compare the gyrencephalic primates with the other gyrencephalic mammals and, more specifically, with the land-dwelling carnivores, whose set of anatomical characteristics makes them the closest to primates of all the gyrencephalic mammals. When we pass from the order of carnivores (not including the amphibious carnivores) to the order of primates, we see a sudden change in the brain model. The model also distinguishes itself by a double series of characteristics, of which some take place in the great limbic lobe and others in the rest of the mantle. The first characteristics are the result of the atrophy of the olfactory system; we have already studied them in amphibious carnivores and can therefore simply list them. 1. The olfactory lobe, now rudimentary, is reduced to a small bulb (olfactory ganglion), and the olfactory peduncle has become long and thin and no longer forms anything more than a small ribbon (olfactory strip) that is improperly called the “olfactory nerve.” 2. The hippocampal lobe, considerably atrophied, loses its independence and more or less merges with the adjacent convolution; it ceases to form a distinct lobe and now forms only the last convolution of the temporal lobe. 3. The lobe of the corpus callosum is well-developed; it is much less diminished than the other two portions of the great lobe. The posterior portion has not decreased in size at all, but its anterior portion is rel-

33

I do not discuss lemurs, as I have so far been able to procure only a single lemur brain, and even that is incomplete.

atively atrophied; consequently, the lobe increases in size from front to back. 4. Following the atrophy of the olfactory roots, the quadrilateral space is depressed and becomes the locus perforatus. The valley of Sylvius is deeply caved in, and its lateral extremity becomes continuous with the fissure of Sylvius in such a way as to make the fissure seem to extend transversely on the inferior surface of the hemisphere to the chiasm of optic nerves. It therefore seems that the great lobe no longer forms a complete loop around the limbus of the hemisphere; nevertheless, the continuity of the lobe of the corpus callosum and the hippocampal lobe (or convolution) is preserved in front by the two white olfactory roots. The medial root travels toward the origin of the lobe of the corpus callosum, and the lateral root crosses the bottom of the valley of Sylvius and continues on to plunge into the anterolateral extremity of the hippocampal convolution. These first four characteristics are not exclusive to primates; as we saw above, they are also found in amphibious carnivores. In primates, however, the olfactory roots and especially the lateral one are further atrophied, and the hippocampal lobe is further diminished and more consolidated with the adjacent convolution. I add that the temporal lobe with which it merges is formed differently than it is in amphibious mammals, but this last difference does not affect the great limbic lobe, as I will soon explain. For now, I am moving on to the cerebral characteristics that only the primates have. These characteristics appear in the extralimbic mass, i.e., in the lobes and convolutions. They nevertheless are related to a certain extent to the changes in the great limbic lobe, if not from the perspective of its formation then at least from the perspective of its connections. These characteristics are as follows. 1. Enormous development of the frontal lobe, causing the fissure of Rolando to move back and change its trajectory 2. Subdivision of the parietal lobe into three lobes, the occipital lobe, the temporal lobe, and the parietal lobe proper 3. Constitution of the occipital lobe following the formation of the occipital fissure; enlargement of the calcarine sulcus, which becomes the calcarine fissure 4. Constitution of the temporal lobe following the increase in length of the temporal lobule and the partial disappearance of the inferior arc of the limbic fissure 5. Constitution of the parietal lobe proper following the formation of the two previous lobes

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6. Specific constitution of the lobe of the insula in the Sylvian fossa 7. Considerable development of the subfrontal fissure 8. Nearly complete eradication of the subparietal fissure Now we must study these various characteristics in succession. 1. Enlargement of the frontal lobe. The first of these characteristics dominates all the others in importance and provides the point from which most, and maybe all, of them depart; it is the excessive development of the frontal lobe in primates. This lobe varies greatly in size in other mammals, but even in the horse and the elephant, which have the most favorable ratio, the frontal lobe is still of a relatively mediocre size. In the carnivores, which we are comparing with the primates, the lobe is very rudimentary; the fissure of Rolando, which borders it, is located all the way up front, well in front of the anterior extremity of the fissure of Sylvius. The fissure is still sharply angled, at least in its inferior and lateral section, and this diagonal trajectory runs from below to above and from back to front. The result is that the frontal lobe, the lateral portion of which is already very short, is even shorter still in its medial portion, which forms only a very small section of the sagittal edge of the hemisphere. In primates, however, the lobe is very large throughout its entirety, but especially in its medial portion, which forms more than half of the sagittal edge of the hemisphere. The fissure of Rolando is pushed much further back. The inferior and lateral extremity of the fissure is no longer located in front of the anterior extremity of the fissure of Sylvius but rather above the middle section of it, and the superior extremity is pushed back much further still, resulting in a trajectory that no longer angles up and forward, but up and back. The enlargement of the frontal lobe in primates occurs simultaneously in length, width, and depth. The deepening of the lobe raises the plate of the frontal bone; its widening spreads it transversely, and the anterior extremity of the brain grows larger and rounder than in most other animals. Despite the enlargement of the anterior cranial fossa, there is still insufficient width in view of the great transverse enlargement of the cortex of the frontal lobe. The cortex thus becomes the site of longitudinal folding, which produces the frontal convolutions. The effects of the increase in length are even more remarkable. This increase, hindered in front by resistance from the cranial wall, translates into an anterior to posterior push on the rest of the hemisphere. On the inferior or orbital surface of the frontal lobe, however, the connections of the base of the brain with the base

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of the cranium are in opposition to the posterior edge of the orbital lobule being pushed back. The effects of the lengthened frontal convolutions appear almost exclusively on the convex surface of the frontal lobe. There, the increase in length faces no obstacle other than resistance from the parietal convolutions, which is inferior to the push from the front, and so the frontal lobe develops at the expense of the parietal lobe. In most mammals, the frontal lobe extends only minimally on the convex surface of the hemisphere; in some cases it slightly covers the most anterior part of the lateral ventricle, but only barely. Its orbital portion is thus generally much larger than its superior portion, and the superior portion is in essence only the extremity of the orbital portion; there is no need to distinguish two levels of the frontal lobe. In primates, however, the superior portion of the frontal lobe is enormously enlarged and extends far onto the convex surface of the hemisphere, above the lateral ventricle. The frontal lobe now consists of two levels: a superior one that is very large and is located above the centrum semiovale and an inferior or orbital one that is much smaller and is located below the centrum semiovale. The convolutions continue directly from one level to the other, bending back on themselves in the anterior portion of the lobe. 2. Division of the parietal lobe. After the excessive development of the frontal lobe, the parietal lobe, which until now formed almost the entire mass of convolutions, is pushed back considerably. After losing a vast amount of length, its convolutions fold, extend back and downward, and form three groups that constitute three distinct lobes: the occipital lobe, the temporal lobe, and the parietal lobe proper or the primate parietal lobe. 3. Constitution of the occipital lobe. The separation of the occipital lobe results from transverse folding made necessary by insufficient room lengthwise. The postRolandic portion of the hemisphere, pushed back by the frontal lobe, recuperates part of the ceded space by extending above the cerebellum, which it covers entirely and sometimes even spills over. This is not enough, however: the longitudinal convolutions are still too long for the space that is left for them, and they become the site of transverse folding that occurs both on the convex surface and on the medial surface. The folding produces the occipital fissure (or perpendicular fissure of Gratiolet). The section of this fissure that extends onto the medial surface is called the medial occipital fissure, and the section that extends onto the lateral surface is called the lateral occipital fissure, but these two sections are most often continuous with one another without any interruption.

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

The part behind the occipital fissure makes up the occipital lobe. We saw above (p. 441 [p. 2528 in the English translation]) that the parietal convolutions in osmatic brains originate in the posterior portion of the hemisphere in a small region where they connect with one another and also with the retrolimbic annectant convolution. This region, which we have called the pole of the hemisphere, naturally forms part of the occipital lobe in primates, and in primates it is called the occipital pole. We also saw that the retrolimbic annectant convolution is usually simple in carnivores but that in most ruminants and pachyderms it is divided lengthwise by a sulcus that we called the calcarine sulcus, having considered it in advance to be analogous to the calcarine fissure in primates. In primates, the sulcus becomes large and deep; it is a typical feature in a set position, and it acquires the significance of true fissures. The anterior extremity of the calcarine fissure is straight or minimally winding and ends at the great limbic lobe. It extends into the depth of the great lobe and establishes a separation between the hippocampal lobe (now the hippocampal convolution) and the lobe of the corpus callosum. This separation is often so deep that it appears to be complete and the calcarine fissure appears to continue all the way to the great cleft of Bichat. This is in particular seen in Cercopithecus sabaeus, which Gratiolet used as a model in describing primate brains. Gratiolet concluded from it that the calcarine fissure continued into the cleft of Bichat with the hippocampal fissure, all along the dentate body, to the uncus of the hippocampal convolution. Thus, he joined two crevices that are essentially distinct into a single crevice that he called the fissure of the hippocampi. This played no small part in misunderstanding the continuity of the hippocampal convolution and the convolution of the corpus callosum, which even so had already been demonstrated by Gerdy and Foville’s research (see above, p. 389 [p. 2502 in the English translation]). The fact is, in the majority of monkeys, and sometimes even in humans, when the calcarine fissure is examined before the membranes are removed, it does look like it ends at the cleft of Bichat, B (see Fig. 30 and 31, K). If the pia mater is removed, though, and the cleft of Bichat dilated and the edges of the calcarine fissure spread apart, we see (Fig. 31) that the fissure only dips into the great limbic lobe superficially and that a more or less thick tract of brain tissue maintains the continuity of the hippocampal convolution, H0 , and the lobe of the corpus callosum, C000 . Figures 30 and 31 both show the medial surface of the right hemisphere of a Humboldt’s woolly monkey, with a mold taken before and after the fissures were dilated.

Figures 30 and 31. Humboldt’s woolly monkey (a New World monkey), Medial surface of the right hemisphere of. In Figure 30 and 31, the calcarine fissure, K, and the cleft of Bichat, B, are in their natural state; in Figure 31, they have been dilated to show the continuity of the hippocampal convolution, H0 , and the lobe of the corpus callosum, C000 . H, H0 , hippocampal convolution; L, vestige of the inferior arc of the limbic fissure (limbic sulcus); C, C0 , C00 , C000 , lobe of the corpus callosum; SF, subfrontal fissure; F, F, F0 , medial surface of the frontal lobe; F0 , oval lobule of the frontal lobe; SP, subparietal sulcus; P, quadrilateral lobule, or medial surface of the first parietal convolution; O, occipital fissure; Cu, cuneus or medial occipital lobule; K, calcarine fissure; K0 , superior ramus of the calcarine fissure; K00 , inferior ramus of the calcarine fissure; So, suboccipital lobule; b, occipital pole.

The isthmus of communication here is rather narrow, but it is often much larger; in humans, it is generally sizeable enough to be superficial. It comes into view when the pia mater is removed, without it being necessary to dilate the fissure. It is just as large and superficial in the gorilla, but it is deep in many monkeys. In some New World monkeys (capuchins), it is so thin and so deep that it takes some effort to find it. Finally, it is missing in lissencephalic primates such as marmosets and tamarins. In this latter case, the calcarine fissure seems to be only an emanation of the cleft of Bichat, and the continuity of the two adjacent parts of the great limbic lobe is achieved by only a strip of gray matter that passes under

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the anterior extremity of the calcarine fissure. Human fetuses between 3 and 5 months sometimes have the same organization. This is not the most common case; most often a small and deep or even superficial fold extends from the hippocampal convolution to the convolution of the corpus callosum. I have always found this fold developed to some extent in fetuses older than 5 months, and it takes shape more and more as the convolutions form in the rest of the mantle. Whatever the case, we must acknowledge that the calcarine fissure cuts much more deeply into the great limbic lobe in primates than in other animals. This proves that the anatomical and functional cohesion of the hippocampal lobe and the lobe of the corpus callosum has diminished greatly. We can hypothesize that this relative isolation of the two arcs of the great limbic lobe at their posterior extremity and the more complete isolation of their anterior sections near the locus perforatus are the result of the atrophy of the olfactory system and the degradation of olfactory function. The hippocampal lobe and the lobe of the corpus callosum differ greatly from one another in their structure and connections, and it does not seem likely that they would have only a single shared function; each of them must have a special function that is not yet understood. In osmatic mammals, however, they have in addition a common olfactory function, as demonstrated by the continuity of their anterior extremities with the olfactory lobe and by the fusion of their posterior extremities with each other. In primates, this common olfactory function loses nearly all importance, and the two lobes that it once joined tend to separate. I insist no further upon this somewhat risky conjecture, however, and return instead to the calcarine fissure. As mentioned above, the calcarine fissure in primates originates over the great limbic lobe and soon becomes very deep. It travels almost directly backward along the very blunt edge that separates the medial surface of the hemisphere from the inferior or tentorial surface. It then reaches the tip of the hemisphere, i.e., the occipital pole (Fig. 31, b), where it ends by dividing into two rami, one ascending, K0 , and the other descending, K00 . Along its pathway, it maintains a constant connection with the posterior extension of the lateral ventricle, known as the ankyroid cavity. This cavity is completely exclusive to primates, as is the occipital lobe of which it is part. The portion of the hemisphere that is pushed back and that then forms the occipital lobe above the cerebellum, together with the ankyroid cavity, results in the posterior part of the wall of the lateral ventricle. The ventricle thus extends in the shape of a long, narrow diverticulum that has been compared with a horn (posterior horn) or the barb on an anchor (ankyroid cavity). The formation of the ankyroid cavity is therefore the consequence of the formation of

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the occipital lobe. The cavity extends in a longitudinal direction; its inferior edge is raised by a longitudinal projection that is described by Morand as a spur, calcar in Latin, and is also called the hippocampus minor. However, the bottom of the calcarine fissure corresponds to this medial protuberance precisely; this is the origin of the name of the calcarine fissure, which was suggested by Huxley and which we will also use.34 The calcarine fissure divides the occipital lobe into two parts, one superior and the other inferior. The inferior portion, or suboccipital lobule (So, Fig. 31) forms the inferior surface of the lobe; the superior portion, or medial occipital lobule, or cuneus, forms the lobe’s medial surface (Cu). The cuneus, so called because it often is shaped like a wedge, is located between the ascending ramus of the calcarine fissure, K0 , and the section of the occipital fissure, O, that extends onto the medial surface. In front, the cuneus and the suboccipital lobule are connected to the great limbic lobe by two folds that separate the anterior section of the calcarine fissure and that together represent the retrolimbic annectant convolution in osmatic mammals. In osmatic animals, the retrolimbic annectant convolution connects the great limbic lobe with the posterior portion of the parietal lobe, which is represented in primates by the occipital lobe. The occipital lobe is in a way the retrolimbic annectant convolution in full bloom, and the calcarine fissure that divides it is analogous to the calcarine sulcus that we examined earlier in the horse (page 444 [p. 2529 in the English translation], Fig. 22) and the roe deer (page 443 [p. 2528 in the English translation], Fig. 21). The deep division of the retrolimbic annectant convolution in primates thus reproduces an organization found in many other animals, with barely any changes. The inferior ramus of the subdivision connects the suboccipital lobe with the posterior portion of the hippocampal convolution (Fig. 31, H0 ), i.e., with the inferior arc of the great limbic lobe. Its typical shape gave rise to it being called the lingual lobule; I will call it the occipitohippocampal annectant convolution. The superior ramus of the subdivision of the retrolimbic annectant convolution connects the cuneus with the posterior and inferior extremity, C000 , of the lobe of the corpus callosum; I therefore call it the cuneolimbic annectant convolution. This annectant convolution passes above the calcarine fissure and below the inferior extremity of the occipital

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Gratiolet was credited with discovering the calcarine fissure, determining its connections, and highlighting its importance, but he mistakenly believed that it extended into the cleft of Bichat along the hippocampus major and that it consequently was connected successively to the two hippocampi – with the minor in back and with the major in front. He therefore called it the fissure of the hippocampi, a term that today is recognized as inaccurate, since we know that the posterior section and the anterior section of this supposed fissure are in fact two distinct crevices.

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

fissure, O. It is superficial in almost all primates, so the occipital fissure does not connect with the calcarine fissure. It is deep in humans and gibbons, and the two fissures meet in a Y, but, if the edges are spread apart where the fissures meet, the cuneolimbic annectant convolution is always visible; its connections have not changed at all. As I have said, the calcarine fissure ends in back at the posterior extremity of the hemisphere by splitting into two rami, one ascending, K0 (Fig. 31), and the other descending, K00 . The relative length of these two rami varies depending on the species. The inferior ramus, K0 , ends at the tip of the hemisphere, i.e., the most inferior and most posterior part of the occipital lobe. Sometimes it can even pass this point and extend slightly onto the convex surface of the lobe. Between the two rami K0 and K00 is a more or less curvy fold, b, which is continuous with all the occipital convolutions at once, i.e., above and inside with the cuneus, below with the convolutions of the suboccipital lobule, and outside with the more or less rudimentary convolutions of the lateral surface. This is the fold where we saw the longitudinal sulci of the parietal lobe end in osmatic mammals (see page 441 [p. 2528 in the English translation], Fig. 20, posterior surface of the tapir hemisphere); at that point we called it the pole, a term that perhaps is not accurate enough in this case because, although all the parietal sulci yield to the same fold, they do not converge toward a single point. At times they can even diverge slightly, given that the extremity of the hemisphere where the fold in question runs transversely (b, b0 , b00 , Fig. 20) is still rather large. In primates, however, this posterior extremity ends at a point upon which the occipital sulci converge more or less directly; this is actually worthy of the term pole. The occipital pole, the origin of all the occipital convolutions, thus corresponds to the tip of the hemisphere facing the extremity of the descending ramus of the calcarine fissure (K00 , Fig. 31). These convolutions are always very well-defined on the medial and inferior surfaces of the occipital lobe but in most cases are much less so on the lateral surface, where they are often fused together throughout the greatest extent of their length. Even so, there is a large longitudinal sulcus l (Fig. 32) at the border between the lateral surface and the inferior surface; it runs toward the pole and separates the suboccipital lobule, So, from the supraoccipital lobule, Su. I call this sulcus, which is constant in gyrencephalic primates, the lateral occipital sulcus (it is the third occipital sulcus in humans and apes). The suboccipital lobule is sometimes almost undivided, especially in the anterior portion, which borders the lateral occipital fissure and even extends slightly

Figure 32. Yellow baboon (Old World monkey). Lateral surface of the left hemisphere. S, S, fissure of Sylvius; R, R, fissure of Rolando; O, O, lateral occipital fissure; F, frontal lobe; P1, first parietal convolution; q, groove dividing this convolution; P2, second parietal convolution; p, parietal sulcus; T1, T1, first temporal convolution; T2, second temporal convolution; t0 , t0 , first temporal sulcus, or parallel fissure; l, lateral occipital sulcus; So, suboccipital lobule; Su, supraoccipital lobule; m, occipital cap.

above it in a cap-like fashion (occipital cap according to Gratiolet, m, Fig. 32). We could thereby believe that there are no true suboccipital convolutions and that the suboccipital lobule is not continuous with the parietal convolutions located in front of the fissure. Nevertheless, these parietal convolutions, of which there are two, sometimes cross the occipital fissure as they form Gratiolet’s superior annectant convolutions or supraoccipital annectant convolutions. Gratiolet attached a great deal of significance to these annectant convolutions; he made them out to be a feature of major importance and even used them to separate primates into three groups depending on whether they had two annectant convolutions, a single one, or none at all. However, when the full depth of the occipital fissure is dilated to prepare a wax mold, following the procedure I described in my thesis on the gorilla brain,35 there is always at least the rudiment of the two annectant convolutions.36 We thus recognize that the two parietal convolutions always continue into the supraoccipital lobule; consequently, this lobule always includes two convolutions that are more or less fused together. As a consequence of this fusion, the supraoccipital lobule appears to be very simplistic in the majority of

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Revue d’Anthropologie [Journal of Anthropology], 1878, p. 38. The first annectant convolution is normally located along the sagittal edge where the medial occipital fissure connects with the lateral occipital fissure. Sometimes it is located slightly further out and is thus easy to find; sometimes it is located further in and crosses the medial occipital fissure. It was when in this last position that Gratiolet believed it was missing entirely.

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primates; it could even be said that the absolute or relative simplicity of this lobule constitutes a typical characteristic of primate brains. It is only in the highest genera that the supraoccipital lobule, taking its turn at evolving like the rest of the hemisphere, is covered by true convolutions. In this instance, there are really two convolutions, as with the annectant convolutions, but their number is increased to three following the division of the second one, the anterior and lateral section of which merges with the temporal lobe. All three end at the occipital pole after some amount of twisting and turning. 4. Formation of the temporal lobe. This feature of the primate brain, like the formation of the occipital lobe, can be largely attributed to the exaggerated development of the frontal lobe. The aforementioned angle of the fissure of Rolando has shown us that the frontal lobe grows much larger in its superior and medial portion than in its inferior and lateral portion. Its size increases at the expense of the parietal lobe, which finds itself pushed both backward and downward. We have seen that the shift toward the back gives rise to the formation of the occipital lobe; the formation of the temporal lobe is the result of the shift downward. The lateral or Sylvian convolution of the parietal lobe thus descends toward the base of the brain, where the atrophy of the hippocampal lobe has left space available. We have not forgotten that, in the brains of carnivores, the posterior part of the convolutions of the Sylvian grouping form a sort of lobule above the hippocampal lobe and behind and below the fissure of Sylvius (which is angled) that we have called the temporal lobule of the parietal lobe (see above, p. 410 [p. 2512 in the English translation]; see also p. 429 [p. 2522 in the English translation], Fig. 12, T, fox brain, and p. 438[p. 2527 in the English translation], Fig. 18, T, dog brain). This lobule points downward and also slightly forward, like the fissure of Sylvius itself. Supposing a gradual atrophy of the hippocampal lobe in these animals, the temporal lobule, advancing to take its place, would have tended to travel not only downward but also forward. It would have been even easier for it to extend forward because the inferior and lateral region that it occupies corresponds to the smallest part of the frontal lobe. This is what occurred in primates, and the part of the parietal lobe that extends downward and forward in this way to below the posterior portion of the frontal lobe then constitutes a separate lobe, the temporal lobe. The fissure of Sylvius became very long and sharply angled through this process; it forms the superior boundary of this lobe. The lobe maintained the connections that make it continuous through its lateral surface with the parietal

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lobe and through its inferior surface with the occipital lobe (which is another extension of the same parietal lobe). Finally, the temporal lobe is completed below and medially by the remains of the atrophied hippocampal lobe, i.e., the minor hippocampal convolution, which has become the last temporal convolution. I have already mentioned the fusion that occurs between the hippocampal convolution and the penultimate temporal convolution. This fusion, however, is never complete; a vestige of the limbic fissure always remains. In all monkeys, Old World monkeys, New World monkeys, and apes, the anterior section of the limbic fissure remains open and usually even rather deep. It cuts into the tip of the temporal lobe to a variable extent (see p. 471 [p. 2541 in the English translation], Fig. 31, L), up to the valley of Sylvius, where it appears to end. If the posterior edge of this valley is lifted, however, we see that the limbic fissure extends outward and upward, curving under the tip of the temporal lobe, to reach the lateral extremity of the valley and end at the entrance to the Sylvian fossa. This vestige of the limbic fissure (limbic sulcus) tends to disappear in humans. It is commonly found in the inferior [sic] races, sometimes as pronounced as in monkeys. In most whites, it disappears altogether; the position of the limbic sulcus is nevertheless still indicated at the tip of the temporal lobe by a superficial longitudinal depression that allows the lateral boundary of the hippocampal convolution to be recognized. The anterior end of this convolution thus always remains more or less distinct. It is defined in the shape of a small, rounded lobule called the hippocampal lobule. The presence of the limbic sulcus at the tip of the temporal lobe should be considered a sign of inferiority in humans. I have found this sulcus in all the Negro brains that I have studied so far, but I imagine it must sometimes be absent in this race. I have also seen it in some whites, who for the most part, but not always, were idiots or imbeciles; I also possess several idiot and microcephalic brains in which the sulcus does not exist. In summary, of all the primates, humans are the only one in which the most advanced degree of fusion of the anterior extremity of the hippocampal lobe has been observed: it is thus the human that is furthest removed from the osmatic mammal brain model. Nevertheless, the posterior portion of the hippocampal lobe in humans still has a sulcus running along it, the last temporal sulcus, and this is analogous to the corresponding section of the limbic fissure in osmatic brains. The last temporal sulcus, whether or not it extends to the tip of the lobe, is constant in gyrencephalic primates; the first temporal sulcus that runs along the

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

Sylvian edge of the lobe (Gratiolet’s parallel fissure) is also constant. The portion of the temporal lobe located between these two sulci is normally divided into two or three folds by one or two sulci that also run longitudinally. All of the sulci head toward the tip of the lobe, which, as seen earlier, is most often undivided in humans or at least in white humans. This tip therefore merits the term temporal pole in describing the human brain. 5. Constitution of the parietal lobe. We have just seen how the posterior portion and the inferior portion of the parietal convolutions change in primates to form two distinct lobes, the occipital lobe and the temporal lobe. Following this segmentation resulting from the push from front to back and also from above to below caused by the enlarged frontal lobe, the parietal lobe in primates is considerably reduced in size. Of the vast parietal lobe that made up nearly the entire convex surface of the hemisphere in other mammals, roughly onethird becomes the occipital lobe in primates, another one-third becomes the temporal lobe, and the term ‘parietal lobe’ now only applies to the anterior and superior portion. This area is located between the fissure of Rolando and the occipital fissure on one hand and between the sagittal edge and the fissure of Sylvius on the other. Thus reduced in its dimensions, the parietal lobe also changes significantly in shape. It undergoes an evolution that is the inverse of that of the frontal lobe. The frontal lobe, so small and simplistic in other mammals in which the parietal lobe clearly prevailed, has become the main lobe of the hemisphere in primates. In a way, it seized control of the cerebral hegemony, and the growing importance of its functions is evidenced by the longitudinal folding that divides it first into two and then into three convolutions. The conduct of the parietal lobe is completely different: far from becoming more complex, it on the contrary becomes more simplified, and the convolutions that constitute it tend to fuse together. There were between three and five parietal convolutions in osmatic gyrencephalic mammals; there are no more than two in primates. This change is undoubtedly important, but it is less so than one might guess at first glance. Remember that in gyrencephalic mammals other than primates, regardless of the number of parietal convolutions, they all are distributed between two groupings, the sagittal grouping and the Sylvian grouping. The two groupings are separated from each other by the primary parietal sulcus (see above, p. 427 [p. 2520 in the English translation]). In osmatic animals that have only rudimentary convolutions, this sulcus already indicates the separation of the sagittal and Sylvian regions, which inciden-

tally have no subdivisions; in osmatic animals with true convolutions, however, the Sylvian region is always divided into two longitudinal convolutions. As for the sagittal region, it is usually divided, also into two parallel convolutions, but this is less constant. It can also be divided into three convolutions, although this is very rare, and it can remain completely undivided, as is seen in the badger, the otter, and most small carnivores, for example. The division of the sagittal region is thus less fundamental than the division of the Sylvian region because it is more variable. In primates, the parietal lobe tends to return to a rudimentary model as it simplifies. The sagittal region is reduced to a single convolution, the first parietal convolution; the Sylvian region is also reduced to a single convolution, the second parietal convolution, and there is no longer more than a single longitudinal sulcus, the parietal sulcus (Turner’s intraparietal sulcus). Despite this twofold change, the analogy between the parietal convolutions in primates and in other gyrencephalic mammals is easily demonstrated because the second convolution in primates consists of a singular unit only in front; in back, it is divided into two completely separate folds by a completely constant sulcus (Fig. 32, t0 , t0 , p. 475 [p. 2543 in the English translation]). From there, the sulcus travels downward and then toward the front and is directly continuous with the first temporal sulcus (or parallel fissure, as described by Gratiolet). The two folds resulting from this split curve over to travel downward and then toward the front, like the sulcus separating them. The anterior fold, which is also superior, goes around the extremity of the fissure of Sylvius, S, to then constitute the first temporal convolution, T1. The posterior fold, which is also inferior, C, is aptly described by the term curved fold used by Gratiolet; it curves around the extremity of the first temporal sulcus, passes in front of the lateral occipital fissure, O, O, and goes on to merge with both the second temporal convolution, T2, and the outermost supraoccipital convolution. This bifurcation of the second parietal convolution is constant in all gyrencephalic primates; it even shows up already in some New World monkeys that have almost no other divisions in their hemispheres. Granted, sometimes the posterior extremity of the fissure of Sylvius ends obliquely at the first temporal sulcus; this occurs in the capuchin (Fig. 33 and 34), for example, and among the Old World monkeys, in many guenons, macaques, and the mandrill. One might therefore believe that the second parietal (Fig. 33 and 34, P2) produces only the curved fold, C, and merges only with the second temporal convolution, T2, because the fissure of Sylvius, S, goes on to join the first temporal sulcus, t0 . However, if we spread apart the edges of the fissure of Sylvius to reveal the Sylvian fossa, as has

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Figures 33 and 34. Tufted capuchin. Lateral surface of the right hemisphere. Fig. 33: Parts are in their natural states. R, fissure of Rolando; O, occipital fissure; S, fissure of Sylvius, connecting superficially in back with the first temporal sulcus t0 ; F, frontal lobe; P1, first parietal convolution; P2, second parietal convolution; C, curved fold; T1, first temporal; T2, second temporal; l, lateral occipital sulcus; Su, supraoccipital lobule; So, suboccipital lobule; p, parietal sulcus. Fig. 34: Same hemisphere, wax mold after the fissure of Sylvius was dilated to show the Sylvian fossa and the insular lobe; s, deep fold establishing continuity between P2 and T1 between the fissure of Sylvius and the first temporal sulcus; n, i, f, insular lobe inside the Sylvian fossa; n, deep temporoparietal annectant convolution; i, insula proper; f, temporofrontal falciform fold, at the entrance to the Sylvian fossa. Other letters as in Figure 33.

been done in Figure 34, which shows a wax mold of the same hemisphere, we see that a completely separate fold, s, separates the extremity of the fissure of Sylvius from the first temporal sulcus and consequently connects the second parietal convolution with the first temporal convolution.37 The second parietal convolution in primates thus truly has two parts in back, and it is

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The superficial or deep location of the fold, m, i.e., of the superior bifurcated branch of the second parietal convolution, is of such little importance that it does not even constitute a common feature. Thus, this fold is thin and deep in the mandrill and large and superficial in the yellow baboon.

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easily seen that it represents the two convolutions of the Sylvian region in other gyrencephalic mammals. The analogy between the first parietal convolution in primates and the sagittal parietal region in other gyrencephalic mammals is easier to demonstrate again. We have effectively seen that this region is undivided in the otter, in the badger, and in most small carnivores, which in this respect do not differ from inferior primates. It is usually divided into two parallel folds in carnivores; sometimes they are partially fused together, such as in the bear, and sometimes they are completely separate, such as in the fox. This complete division is never observed in primates; this is why we count only a single sagittal convolution in them. Nevertheless, this convolution displays a tendency to split as the brain grows larger and more complex. In the yellow baboon (Fig. 32, p. 475 [p. 2530 in the English translation]), a longitudinal groove, q, traces a rudimentary dividing line on the first parietal convolution, P1. This groove is also found in the great apes; it is usually rather large and sometimes winds and turns to a degree and even splits. It can extend far enough to connect with the parietal sulcus, and the first parietal convolution is no longer singular in this case. In humans, the groove that divides it is sometimes made up of several twisting branches, and the rather complex unit gave rise to the not very useful term parietal lobule that Gratiolet used for this convolution. The first parietal convolution in humans and great apes can thus be considered analogous to the two sagittal convolutions in carnivores, the result of the fusion of these two convolutions. The fusion here is more pronounced than in the two convolutions in the Sylvian region; it should come as no surprise that the sagittal region in primates is relatively more atrophied than the Sylvian region, because the frontal lobe, the pressure from which causes this atrophy, is much more well-developed in its superior portion than in its lateral portion. 6. Constitution of the insular lobe. In our earlier examination of the formation of the Sylvian fossa in osmatic mammals (see p. 430 [p. 2530 in the English translation] et seq.), we saw that the fossa is the space on the lateral surface of the hemisphere that is located between the lateral edge of the great limbic lobe (p. 439 [p. 2527 in the English translation], Fig. 19, L, L0 , L00 ) and the concavity of the arc of Sylvius, P1, P1. More or less superficial in many pachyderms and ruminants, it is always deep in carnivores, where it is hidden by the edge of the arc of Sylvius. It is revealed upon lifting this edge and dilating the fissure of Sylvius, however, as in Figure 19. Then we see that the arc of Sylvius is formed in front by the inferior and lateral edge of the small frontal lobe, F, and that the rest of its

The Journal of Comparative Neurology | Research in Systems Neuroscience

The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

Figure 35. Yellow baboon. Medial surface of the right hemisphere. H, H0 , hippocampal convolution and uncus; T, tip of the temporal lobe; L, vestige of the inferior arc of the limbic fissure (limbic sulcus); O, medial occipital fissure; K, calcarine fissure; SF, subfrontal fissure; a, origin of the subfrontal fissure; b, end of the subfrontal fissure; e, frontolimbic groove that marks the location of the frontolimbic annectant convolution, which is deep; i, subfrontal groove. C0 , C, C00 , convolution or lobe of the corpus callosum; F, F, F, medial surface of the first frontal convolution, the superior level being separated from the inferior or orbital level by the frontolimbic groove, e; F0 , oval lobule, or medial surface of the ascending frontal convolution; P, P, quadrilateral lobule, or medial surface of the first parietal convolution; g, h, the two parietolimbic annectant convolutions; Cu, cuneus, or triangular lobule of the occipital lobe; l, superior cuneolimbic or retrolimbic annectant convolution; m inferior retrolimbic annectant convolution; i, suborbital groove.

extent is formed by the Sylvian convolution of the parietal lobe, P1, P1, P1. This convolution is composed of two parts that formed the two edges of the fissure of Sylvius prior to dilation. The inferior or limbic edge of the Sylvian fossa is formed by the hippocampal lobe in back and the lateral olfactory root in front. The Sylvian fossa is deep in primates, as it is in carnivores, and the fissure of Sylvius must again be dilated to reveal it (see p. 481 [p. 2546 in the English translation], Fig. 34). The hippocampal lobe, which is atrophied and pushed toward the base of the hemisphere by the other temporal convolutions that extend above it, is no longer connected to the Sylvian fossa. The lateral olfactory root, which is even further atrophied, is reduced to a small white tract that burrows into the lateral part of the valley of Sylvius, crosses it, and continues on to plunge deeply into the anterolateral extremity of the hippocampal convolution. The Sylvian fossa is thus no longer separated from the valley of Sylvius except by a very short and very deep fold, f, that connects the anterolateral end of the hippocampal convolution to the outermost convolution of the frontal lobe. The rudimentary lateral olfactory root progresses along this fold. This deep fold, which I call the falciform edge, is all

that remains in primates of the limbic edge of the Sylvian fossa. It corresponds to the entrance of the Sylvian fossa, i.e., the point where the fossa merges with the valley of Sylvius. After the limbic edge disappears, the Sylvian fossa is no longer encircled in primates except by the arc of Sylvius. This arc forms an almost complete enclosure that is interrupted, below and in front, only by the valley of Sylvius. The enclosure is very elongated in an almost longitudinal direction and is consequently made up of two margins, one superior and the other inferior. The superior margin (Fig. 34) is formed in front by the inferior edge of the frontal lobe, F, and in back by the inferior edge of the parietal lobe, P2. The entire length of the inferior margin is formed by the first convolution of the temporal lobe, T1. The two margins are continuous with one another in back, s, over the terminal end of the fissure of Sylvius. We clearly see that this formation of the arc of Sylvius in primates is completely analogous with its formation in osmatic mammals. The enlarged frontal lobe makes up a larger portion of the superior margin; however, this is only a difference of degree. Aside from that, the Sylvian convolution, called parietal along the superior margin, is termed temporal along the inferior margin; however, this is only a difference in terms. Finally, the anterior extremities of the two margins are brought closer together and are no longer separated except by the width of the entrance to the Sylvian fossa, f; however, this is only a difference in form. All in all, the enclosure that surrounds the Sylvian fossa in primates does not differ in any fundamental way from what was described for osmatic mammals. The bottom of the Sylvian fossa is filled by a portion of the mantle that is well-developed enough in primates, especially in the superior primates, to merit being called a lobe. It is called the insular lobe, but it corresponds exactly in position and in constitution to the subsylvian lobule previously described for osmatic mammals (see above, p. 430-440 [p. 2522–2526 in the English translation]). As with the subsylvian lobule, the insular lobe rests upon the lentiform nucleus or extraventricular nucleus of the corpus striatum; also, like its counterpart, it is composed of two parts, one temporofrontal and the other temporoparietal. We have seen that the subsylvian lobule in osmatic mammals is formed by two folds that we have called the temporofrontal fold and the temporoparietal fold. They both originate from the temporal lobule, i.e., the portion of the parietal lobe located behind the fissure of Sylvius, and both continue up to the superior margin of the Sylvian fossa, the first to the frontal section of the margin and the second to the parietal section. Because the temporal lobule forms the posterior

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Figure 36. Chimpanzee. Medial surface of the right hemisphere. Letters as in Figure 35, except that the frontolimbic fold e is superficial and interrupts the subfrontal fissure.

boundary of the Sylvian fossa, the two folds travel from back to front, and the temporofrontal fold is located below the temporoparietal fold (see Fig. 13 and 14, p. 431 [p. 2523 in the English translation] and p. 433 [p. 2524 in the English translation]). In primates, the temporal lobule becomes the temporal lobe and extends downward and forward to below the frontal lobe; the direction of the subsylvian folds is therefore forced to change. The temporofrontal fold travels upward to reach the frontal section of the superior Sylvian margin; it changes from a horizontal to an ascending path. The temporoparietal fold deviates even more: it travels not only from below to above but also from front to back. This is due in part to its temporal insertion being moved downward and forward and in part to its parietal insertion being pushed back significantly, a result of the growth of the frontal lobe and the shifting back of the fissure of Rolando. Now the temporofrontal fold is no longer located below the temporoparietal fold; it is now located in front of it. Besides this, the change in direction does not change any of the connections of the two subsylvian folds at all. To locate the two subsylvian folds in primates, the fissure of Sylvius must be dilated to lower the inferior margin, which is formed by the first temporal convolution, and to raise the superior margin, which is formed in back by the second parietal convolution and in front by the lateral or Sylvian edge of the frontal lobe (see p. 481 [p. 2546 in the English translation], Fig. 34). We then can see the full extent of the bottom of the Sylvian fossa, i.e., the insular lobe. We can immediately distinguish two parts, one posterior and superior, n, and the other anterior and inferior, i. The posterior part, n, is formed by a fold that breaks away from the superior edge of the first temporal con-

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volution at a deep level. The fold reaches the superior furrow of the Sylvian fossa and then climbs and plunges into the deep surface of the second parietal convolution. This fold unites two convolutions that belong to different lobes and thus is among the folds termed annectant convolutions. I therefore call it the deep temporoparietal annectant convolution. I add “deep” because it is always deep in primates, but this is not always the case in other animals. We recall that the subsylvian temporoparietal fold that is its counterpart is superficial in ruminants and in the tapir, that its front portion is superficial in the horse, and that it is sometimes superficial in the pig (see above, p. 431-436 [p. 2523–2526 in the English translation], Fig. 13–17). The temporoparietal annectant convolution is simple and has no curves in most primates. It is slightly more complex in the superior primates and especially in humans, in whom it forms a convolution that is rather sinuous and rather large and yet is always very deep. In front of this annectant convolution, the rest of the insular lobe is made up of a convex protrusion, i, almost always smooth, which extends to the entrance to the Sylvian fossa, where the falciform fold, f, provides a boundary. This protrusion constitutes the insula proper. This is what is meant when someone refers simply to the insula. In other words, the insular lobe has two parts: the insula and the temporoparietal annectant convolution. The insula is separated from the lateral and inferior edge of the frontal lobe by a superior furrow and from the anterior section of the superior edge of the temporal lobe by an inferior furrow. Moreover, it is separated from the anterosuperior edge of the temporoparietal annectant convolution by a sulcus that extends obliquely from the superior furrow to the inferior furrow. This sulcus is normally not very sunken, but the two furrows are very deep; this is the origin of the name insula, coined by Reil to describe the part that they circumscribe almost entirely. The layer of gray matter that covers the insula extends without interruption below the two furrows and along the edges of the frontal and temporal lobes. Aside from this very deep and purely cortical continuity, however, the anterior and inferior extremity of the insula is more directly connected with the two neighboring lobes, with connections immediately outside the falciform fold at the entrance to the Sylvian fossa. From the insula’s anterior and inferior extremity, which we will call the pole of the insula, a short, thick fold breaks away and immediately merges with the terminal extremity of the most lateral frontal convolution. A large, short tract also breaks away from the pole, merges with the falciform fold, and plunges deeply into the superior surface of the temporal lobe. The insula thus establishes

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

connections between the temporal lobe and the frontal lobe at the bottom of and especially at the entrance to the Sylvian fossa. Given these connections, we should consider it to be analogous to the temporofrontal fold in osmatic mammals. The insula is always simple in New World monkeys and Old World monkeys as well as in gibbons. In the great apes and in humans, it is divided into a number of folds that converge on the pole and successively reach the various points of the superior furrow, which they cross to plunge deeply into the frontal lobe. In animals other than primates, the subsylvian lobule is sometimes superficial and sometimes deep, and its position depends mainly on its size. It is very small in carnivores and is completely hidden beneath the Sylvian convolution; in ruminants and the majority of pachyderms, it is larger and appears in whole or in part on the surface of the brain. The insular lobe in primates is always much larger than the subsylvian lobule in carnivores; in superior primates, it attains a size not just equal to but even larger (proportionally) than the size of the subsylvian lobule in ruminants and pachyderms. Nevertheless, it remains deep, and even all the more so when it is larger. This seemingly contradictory result is the consequence of the vast development of the convolutions that form the superior margin of the Sylvian fossa. In front, the enlarged frontal lobe lowers its lateral edge over the insula, like a kind of roof. This is the natural consequence of the overall growth of this lobe. In back, the superior margin of the Sylvian fossa is formed by the parietal lobe, which, far from having grown larger, has in contrast become smaller. However, remembering that the superior and posterior extremity of the frontal lobe exerts a force on the parietal lobe that pushes it not only backward but also outward and downward, it is understandable that the inferolateral edge of the second parietal convolution must be lower to cover the temporoparietal annectant convolution in back, as the frontal lobe covers the insula proper in front. The superior margin of the Sylvian fossa thus descends in full over the insular lobe, where it constitutes the cap, and then comes to press against the nearly straight superior edge of the first temporal convolution. This line of contact is the fissure of Sylvius. The Sylvian fossa is thereby closed over. To reveal it, we must spread apart the edges of the fissure and lift the cap. The formation of the frontal portion of the cap is the result of the frontal lobe’s development in width. In apes, the lateral edge of the lobe also increases in length; the excess length of the most lateral frontal convolution (which in apes is the third) gives rise to folding that occurs in front of the insula and forms the anterior ramus of the fissure of Sylvius. A second area of folding located above the first produces the ascend-

ing ramus of the fissure of Sylvius38 in humans and sometimes in chimpanzees and orangutans as well. The third frontal convolution, thus folded, no longer runs along only the superior edge of the insula; it curves around its anterior edge as well, from which it is separated by a third furrow, the anterior furrow of the insula. At the same time, the insula, which has become larger, is covered in several radiating folds. The Sylvian fossa, the fissure of Sylvius, and the insular lobe have now reached their peak in complexity and development. Nevertheless, the constitution of these parts and their connections has remained exactly the same as in inferior primates and furthermore has remained the same in its fundamental character as in other mammals. 7. Development of the subfrontal fissure and disappearance of the subparietal fissure. We have just examined the changes that the components of the lateral surface and inferior surface of the hemisphere undergo in primates. Changes that are no less remarkable appear on the medial surface of the hemisphere in the parts related to the superior arc of the great limbic lobe, i.e., to the lobe of the corpus callosum. Although the lobe of the corpus callosum remains relatively simpler than the rest of the mantle, it nevertheless is affected by the general complication of the hemisphere, at least in the superior primates. Its convex edge becomes more or less wavy or sinuous to the point that it starts to resemble actual convolutions; it is thus called the convolution of the corpus callosum. Its constitution remains the same, however, and the term convolution is not suitable for it because the property of a convolution is to be one of the parts of a lobe. The convolution of the corpus callosum cannot be associated with the frontal lobe, the parietal lobe, the occipital lobe, nor the temporal lobe, because it passes successively beneath the first three lobes and merges into the fourth. It thus constitutes unto itself a lobe that is separate from all the others. Clearly, it is analogous to the lobe of the corpus callosum in osmatic mammals. Our name for it, the lobe of the corpus callosum, denotes this analogy. The lobe of the corpus callosum passes in front of the frontal lobe and behind the parietal lobe. The layout of its connections with these two lobes is one of the most noteworthy distinctive characteristics of the primate brain. In osmatic brains, the superior arc of the limbic fissure, which circumscribes the lobe of the corpus callosum to a varying extent, is made up of two parts, one

38

For more detail on the anterior rami of the fissure of Sylvius, consult my Memoire sur le cerveau du gorille [Thesis on the Gorilla Brain], p. 18–22 (Revue d’Anthropologie [Journal of Anthropology], 1878).

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subfrontal, and the other subparietal (see above, p. 445-450 [p. 2529–2531 in the English translation]). These two sections of the limbic fissure are sometimes continuous with each other but are most often separated by the frontolimbic annectant convolution (Fig. 24, b, p. 450 [p. 2547 in the English translation]). Then there is a subfrontal fissure that is completely distinct from the subparietal fissure. In the carnivore order, which is the closest neighbor to the primate order and thus convenient to use for comparison, the frontal fissure exists only in a vestigial state (see Fig. 24, SF); the frontal lobe, F, is very small and is almost entirely merged with the lobe of the corpus callosum, C, C0 . Comparative anatomy shows us that the small rudimentary crevice SF is analogous to the subfrontal fissure. However, although this crevice marks the boundary of the two lobes for the attentive observer, we cannot say that it separates them; it is reduced to a short depression that is barely more noticeable than vascular impressions and is so unapparent that Leuret did not see it in the fox brain despite having been especially partial to studying this brain.39 I therefore have called it the frontal fissure in the previous description only by analogy; in reality, it is not a fissure in carnivores, because the property of a fissure is that it separates two lobes. It is only a slight sulcus in carnivores, so we will call it the subfrontal sulcus. By contrast, the subparietal fissure in carnivores is a true fissure (Fig. 24, SP), a large deep fissure that begins at the retrolimbic annectant convolution, a, describes a large curve below the parietal lobe, P, climbs up to the sagittal edge of the hemisphere, and goes on to form Leuret’s cruciate sulcus on the convex surface. Recall that this fissure separates the lobe of the corpus callosum from the sagittal parietal convolution very deeply, but, nevertheless, two annectant convolutions that are normally deep, the anterior one located at d, Figure 25, and the posterior one located at c, work together to connect these two lobes (see above, Fig. 25 and p. 450 [p. 2532 in the English translation]). In summary, the lobe of the corpus callosum in carnivores is connected with a very small frontal lobe and a very large parietal lobe. It is merged with the frontal lobe and completely distinct from the parietal lobe. The subfrontal fissure exists only in a vestigial state and

39 See Leuret’s atlas (Anatomie comparee du syste`me nerveux [Comparative Anatomy of the Nervous System]. Folio atlas, pl. IV, Fig. 3). The lobe of the corpus callosum, the surface of which is completely flat, continues without any dividing line up to the sagittal edge of the frontal lobe in this diagram. The vestige of the subfrontal fissure, which escaped the notice of such an astute observer as Leuret, is always found in the carnivore brain, even in the simplest and smallest ones, such as the weasel brain.

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only a slight sulcus remains; the subparietal fissure, on the other hand, is extremely large. In primates, the situation changes suddenly. The frontal lobe becomes very large and the parietal lobe very small; the subfrontal sulcus becomes a large and deep fissure, and the subparietal fissure disappears almost entirely; only a rudimentary version remains that can at most be called the subparietal sulcus. In primates as in carnivores, the connections between the lobe of the corpus callosum and its two neighboring lobes are determined by the degree of importance of each lobe; the smallest lobe merges with the lobe of the corpus callosum, whereas the largest lobe remains completely separate. The subfrontal fissure in primates (Fig. 35, SF) begins at a, close to the origin of the lobe of the corpus callosum, C; it curves around the anterior portion of the lobe and runs along a large part of the medial surface of the hemisphere from front to back as it gradually approaches the sagittal edge. Its posterior extremity b often reaches and sometimes passes this edge. The entire section of the medial surface that is included between this fissure and the circumference of the hemisphere is formed by the frontal lobe, F, F, F, F0 , in back by F0 by the ample extremity of the ascending (or preRolandic) frontal convolution, and in front and below by the medial surface of the first frontal convolution. A groove that is nearly constant (subfrontal groove), d, indicates the anterior border of the area F0 , which is Pozzi’s oval lobule (Meynert’s paracentral lobule). Sometimes the subfrontal groove is reduced to a simple stitch, but sometimes it is deeper; most often it emanates directly from the fissure, but sometimes it is isolated; it always travels toward the sagittal edge. The groove is absent only in the most inferior primate brains. It is still visible in the woolly monkey (see above, Fig. 30 and 31, p. 471 [p. 2541 in the English translation]), but it has disappeared in capuchins. The anterior and inferior extremity of the subfrontal fissure always stops a certain distance from the inferior edge of the hemisphere; below the fissure, the first frontal convolution always inserts into the origin of the lobe of the corpus callosum via a bent section belonging to the orbital lobule. This is the only superficial communication that consistently exists between the frontal lobe and the lobe of the corpus callosum. There is another connection, though, provided by the frontolimbic annectant convolution; it is sometimes superficial and sometimes deep. The annectant convolution crosses the subfrontal fissure near the genu of the corpus callosum. In the yellow baboon, shown in Figure 35, it is deep, and its location is indicated on the exterior only by a groove, e. When it is superficial, which is the most common

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

occurrence, it divides the subfrontal fissure into two sections that correspond to the superior level and the inferior or orbital level of the first frontal convolution. It is sometimes very thin and very short, as can be seen in our woolly monkey (p. 471 [p. 2541 in the English translation], Fig. 31, e). Other times, it is wider and longer, as in the chimpanzee, whose brain is pictured below (p. 493 [p. 2548 in the English translation], Fig. 36, e). The rest of the time, the volume of the frontolimbic annectant convolution can vary greatly within the same species. Thus, in humans and in orangutans, it is sometimes superficial and sometimes deep; however, when it is deep, its location is always indicated by a groove marking the separation of the superior level and the inferior or orbital level of the first frontal convolution. It is worthwhile adding that this frontolimbic annectant convolution in primates is not analogous to the one in carnivores (which is essentially located at the extremity of the subfrontal fissure, which it separates from the subparietal fissure). The posterior extremity of the subfrontal fissure is raised upward, and it reaches and surpasses the sagittal edge of the hemisphere in humans and apes; in other primates it does not pass this edge and does not even always reach it, but it always at least comes very close. What is absolutely constant is that this posterior extremity is always slightly in back of the posterior and superior extremity of the fissure of Rolando. These two fissures draw the borders of the frontal lobe, one on the medial surface and the other on the lateral surface of the hemisphere. They do not join up on the sagittal edge, where they both end, because their extremities are separated by a fold that connects the ascending frontal convolution and oval lobule (Fig. 35, F0 ) to the ascending parietal. Incidentally, it is easy to confirm that the oval lobule belongs to the frontal lobe and not to the parietal lobe; if we draw a line on the sagittal edge and the medial surface of the hemisphere that extends the trajectory of the posterior extremity of the fissure of Rolando, we see that the entire oval lobule remains below this line. As the subfrontal fissure grew and developed in primates, along with the frontal lobe with which it is united, an inverse change was occurring in the subparietal fissure. Recall that the parietal lobe in these animals is reduced considerably in all areas, but much more in its sagittal region than in its Sylvian region. We have already confirmed this atrophy on the convex surface of the first parietal convolution. Now we will encounter it again, much more pronounced this time, on the medial surface of the same convolution. Just as the frontal lobe is at its maximum length on the medial surface of the hemisphere, the parietal lobe is at its

minimum length there. The first parietal convolution takes up only the short space P, P (Fig. 33 and 34), included between the posterior extremity, b, of the subfrontal fissure, and the medial occipital fissure, O. This space is rarely as large as it is in the baboon, and sometimes it is much smaller (see p. 471 [p. 2541 in the English translation], Fig. 30 and 31, P, medial surface of the hemisphere of a woolly monkey brain). Foville called this space the quadrilateral lobule. The base of the quadrilateral lobule is almost entirely merged with the lobe of the corpus callosum. It has even been considered a part of this lobe, which was therefore called the crested convolution by Rolando; the convolution of the corpus callosum topped with the quadrilateral lobule does in fact somewhat resemble the crest of some fowl, narrow in front and wide in back, like the crest of a helmet. The quadrilateral lobule is not a part of the lobe of the corpus callosum, however; it belongs only to the parietal lobe. Although its base is in great part merged with the lobe of the corpus callosum, we still always find the vestige of the large subparietal fissure of other mammals in all gyrencephalic primates from the capuchin to the human. This vestige is no longer a fissure; it is no more than a short sulcus, sometimes very superficial, that is more or less parallel to the convexity of the corpus callosum. This is the sulcus SP in Figure 35 (baboon); it is much shorter in the woolly monkey (Fig. 30 and 31, p. 471 [p. 2541 in the English translation]) and in the chimpanzee (Fig. 36, below). In humans, it is sometimes more curvy and complicated by one or two grooves, but it always is in the same location, and the analogy cannot be overlooked. Through its two extremities, the subparietal sulcus comes within a varying distance of the subfrontal fissure in front and the occipital fissure in back, but it does not connect with them. It is separated from them by two folds, an anterior fold, g, and a posterior fold, h (Fig. 35), which establish a wide double connection between the parietal lobe and the lobe of the corpus callosum; they therefore can be called the parietolimbic annectant convolutions. These two annectant convolutions are in no way exclusive to primates; they are analogous to the annectant convolutions that we have already identified in carnivores. The parietolimbic annectant convolutions in carnivores are usually deep (see above, p. 451 [p. 2532 in the English translation] and p. 489 [p. 2547 in the English translation], and Fig. 25, c and d); it cannot be reiterated enough, however, that the superficial or deep location of annectant convolutions does not constitute an anatomical difference even though it can lead to great morphological differences. Recall that the anterior parietolimbic annectant convolution is large and

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superficial in cats and that the posterior parietolimbic annectant convolution is superficial in some dogs. Both are large and superficial in primates. That is the full extent of the difference. The constitution of the medial surface of the hemisphere remains the same throughout the entire series of gyrencephalic primates. We can reaffirm this by comparing diagrams described previously, of the woolly monkey, which is a New World monkey (p. 471 [p. 2541 in the English translation], Fig. 30 and 31), and the yellow baboon, which is an Old World monkey (p. 490 [p. 2547 in the English translation], Fig. 35), with the diagram included here, of the chimpanzee, which is an ape (Fig. 36). The human brain is so well known that it is not necessary to show it here; everyone will recognize in it the following components, which make up the medial surface of the hemisphere of other primates. 1. Around the threshold of the hemisphere, the first region is formed by the lobe of the corpus callosum, C, C0 , C00 (Fig. 35); the boundaries are established in back by the subparietal sulcus, SP, and in front by the subfrontal fissure, SF. The subfrontal fissure is often divided by the frontolimbic annectant convolution, e, into a superior section and an inferior (or bent, or orbital) section. The frontolimbic annectant convolution, e, is sometimes deep, in which case the two sections of the subfrontal fissure are continuous with each other. 2. Around this first region, there is an outlying region that extends to the boundary of the lateral surface and is formed 1) behind the medial occipital fissure by the cuneus (Cu) or triangular lobule of the occipital lobe; 2) between this fissure and the subfrontal fissure by the quadrilateral lobule, P, of the parietal lobe; and 3) in front of and above the subfrontal fissure by the medial surface of the frontal lobe, which in turn is broken down into three parts: a) in back, the oval lobule, which is the culmination of the pre-Rolandic or ascending frontal convolution and which has its anterior boundary set by the subfrontal groove (d); b) in front and above, by the superior level of the first frontal convolution; and c) in front and below, by the inferior or orbital level of the first frontal convolution. The frontolimbic annectant convolution, e, which is sometimes deep, marks the border of these two levels in superior primates, and the supraorbital groove, i, divides the medial surface of the orbital lobule into two folds. The continuity of the lobe of the corpus callosum with the surrounding lobes is established 1) by the insertion of the frontal lobe at the origin of the lobe of the corpus callosum, C; 2) by the frontolimbic annectant convolution, e, which is usually superficial; 3) by the anterior parietolimbic annectant convolution, g; 4) by the posterior parietolimbic annectant convolution, h;

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and 5) by the cuneolimbic annectant convolution, l, which passes between the occipital fissure, O, and the calcarine fissure, K. This fold is deep in humans and gibbons and superficial in all other primates; it represents the superior half of the retrolimbic annectant convolution in other mammals. The inferior half of this annectant convolution is represented by the fold m, which extends from the suboccipital lobule to the posterior extremity of the hippocampal convolution.

8. CONCLUSIONS We have now reviewed the characteristics that distinguish the primate brain model from the brain models of other mammals and of carnivores in particular. These characteristics are numerous and very striking, but when we study how they evolved we see that they are all directly or indirectly related to a fundamental fact that is perhaps even the starting point, the predominance of the frontal lobe. These characteristics are essentially divided into two groups, those that occur in the region of the great limbic lobe and those that occur in the extralimbic mass or mass of convolutions. Changes involving the mass of convolutions are the result of the enlargement of the frontal lobe, the increase in length of which pushes back the parietal convolutions and brings about the formation of the occipital and temporal lobes; its increase in width traps the insular lobe inside the Sylvian fossa. Changes involving the great limbic lobe are the result of the atrophy of the olfactory system and are analogous to those observed in cetaceans and especially in amphibious mammals. However, although the atrophy of the olfactory system in the latter is due to a way of life that leads to the diminishment or complete suppression of olfactory function, in primates it is due to a wholly different cause. The olfactory system in primates has lost its autonomy and has fallen to the same level as the other sense organs; like the other organs, it serves by receiving and transmitting impressions without processing them further. It is no more than a servant of the intellectual brain, and the humblest of the servants at that, because the information it provides is not as valuable as the information that increased intelligence can conclude from the other senses. The abilities to observe, analyze, and interpret have developed along with the frontal lobe and have rendered useless the entire portion of the olfactory system that exceeded the requirements for simple sensorial transmission. The system therefore atrophied. I have already explained these concepts in an earlier paragraph (see above, p. 393 [p. 2532 in the English translation]); I repeat them here to demonstrate that it is not simply a

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The Great Limbic Lobe and the Limbic Fissure in the Mammalian Series

coincidence but rather a true correlation that exists between the enlargement of the frontal lobe in primates and the inverse evolution of the great limbic lobe.40 All of the distinctive features of the primate brain model are thus subordinate to a fundamental characteristic that in a way sums them all up; it can be expressed in two words: frontal dominance. The simultaneous appearance of these numerous characteristics leads to major external changes and throws the entire cerebral morphology into such upheaval that one might believe oneself to be seeing a brand new order of things, as if the chain had been broken, nature had smashed its old molds, and the project had been started up again using a completely different set of plans. Given these appearances, most authors have avoided substantiating the similar parts of the mantle of the hemisphere in primates and in other mammals. Some, however, more convinced of the continuity of the mammalian series, have attempted to discover at least some analogies between the convolutions and fissures in primates and those in carnivores.41 Their efforts have been unsuccessful because they were based on external morphology, which shows only differences. The study of anatomical connections, however, produces entirely different results. It allows the formation, evolution, and modifications of the various parts of the mantle to be followed throughout the entire mammalian series; all of these parts can then be tracked down in the primate brain, the reasons for the existence of distinguishing characteristics can be identified, and the derivation can be determined to some extent. Leuret was an eminent author who is famous for being the first to confirm the stability of the convolutions in each species and was, posthumously, the inspiration for Gratiolet’s works. After having studied the

40

The evolution of the optic lobes in the vertebrate series offers another example in the same vein. The optic lobes are highly developed in lower classes, from fish to birds, and are sometimes so large as to have been mistaken for the cerebral lobes, which they can exceed in size. In mammals, the optic lobes are represented by no more than the corpora quadrigemina. Their atrophy coincides with the development of the cerebral lobes proper, i.e., with the constitution of the hemispheres. They are still large in monotremes, marsupials, and lissencephalic placental mammals, but they decrease in size and significance as the hemisphere grows and evolves. Just as the degradation of the optic lobes and the end of their autonomy in ordinary mammals are the consequence of the supremacy of the hemispheres where cerebral centralization takes place, so is it that in primates another evolution of the hemisphere, as evidenced by the enormous enlargement of the frontal lobe, leads to the degradation of the olfactory lobes. 41 Benedikt (Moriz). Der Raubtiertypus am menschlichen Gehirne (The Carnivore Model in the Human Brain) in Centralblatt f€ur die med. Wissenschaften [Medical Sciences Review], 1876, p. 930. Idem. Der HinterhauptsLappen der S€augethiere. (The Occipital Lobe in Mammals) in the same digest, 1877, p. 161. Meynert (Theod.) Die Windungen der convexen Oberfl€ache des Vorder-Hirnes bei Menschen, Affen, und Raubthieren. (The Convolutions of the Convex Surface of the Brain in Humans, Monkeys, and Carnivores) in Archiv f€ur Psychiatrie [Psychiatry Archives]. Berlin, 1877, in8, Vol. I, p. 257–286.

convolutions in a great number of mammals, Leuret was struck by the great diversity in the numbers, shapes, and arrangements of the convolutions. He first proceeded with analysis, which led him to create 14 groups of mammals according to as many different brain models; he even wondered if there were not additional models among animals he had not examined. After further reflection and after seeing that the groups based on convolutions were often very different from the natural groups in zoology, Leuret wondered if the numerous brain models were separated from one another by absolute boundaries or if there were similarities and transitions between them despite their lack of resemblance. He therefore posed the following two questions. “Are there intermediate stages between all brains? Are there different brain forms than the ones I have described? Only a more comprehensive observation could resolve these issues, which are of the greatest interest to anatomy and physiology.”42 These two questions are in fact a single question, since the second is but a paraphrase of the first. Leuret wrote in 1839, during an era when people were no longer concerned by Lamarck’s doctrine and had not yet been stirred by Darwin’s. It is thus highly probable that the issue of transformism did not trouble him when he posed the question of finding out whether different models of mammal brains could derive from others. This question, the great anatomical and physiological significance of which he acknowledged, remained dubious for Leuret. Today we can answer it in the affirmative, I believe. In the mantle of the hemisphere, there is a part that is common to all the mammalian brain models, the great limbic lobe, which, sometimes large and developed and distinct throughout all its parts and sometimes changed to a varying degree by atrophy and fusion, nevertheless always retains its anatomical identity. The great limbic lobe varies little in osmatic animals, and it is nearly immune to the changes that take place around it; its appearance always remains true enough for the identification of its different components and the demonstration of how they are analogous to serve as the final proof. It thus provides a solid foundation for the comparison and classification of the folds that form in the rest of the mantle and that maintain their habitual connections with the limbic lobe even as they adopt diversified structures. When atrophy in

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Leuret. Anatomie comparee du syste`me nerveux consideree dans ses rapports avec l’intelligence [Comparative Anatomy of the Nervous System, Considered in Relation to Intelligence], Vol. I, p. 400. Paris, 1839, in-8.

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anosmatic mammals significantly modifies some of the characteristics of the great limbic lobe, these connections permit all the essential components of the great lobe to be located, and they also allow the analogous relationships to be determined for the convolutions that surround the great lobe and the fissures that end there. We can thereby confirm that all of the types of brains, up to and including primate brains, differ from one another only in evolutionary features, i.e., in shape and relative size, and not in the nature of their component parts.

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This conclusion provides enough content to justify the significance that I attach to the study of the great limbic lobe and its connections in the mammalian series. It is not as it seems, and to establish its importance I was obliged to describe it in what may have seemed to be very minute detail. Those of my readers who have had the patience to stay with me until the end, however, will perhaps acknowledge that these details were not without merit, and I hope they will pardon me for the dryness and the length of this thesis.

The Journal of Comparative Neurology | Research in Systems Neuroscience

Comparative anatomy of the cerebral convolutions: The great limbic lobe and the limbic fissure in the mammalian series.

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