THE LIMBIC SYSTEM AND CULTURE: An Allometric Analysis of the Neocortex and Limbic Nuclei*

Este

Armstrong

Armed Forces Institute of Pathology and Department of Anatomy Uniformed Services University of the Health Sciences

The human ability to live according to learned, shared rules of behavior requires cortical functions. Is the limbic system also necessary for culture or are its functions opposed to it, requiring cortical inhibition? The sizes of monkey and ape neocortical and major limbic structures scale with brain weight, but the neocortex expands more (has a steeper exponent) than limbic structures. As the human brain evolved it did not deviate from the scaling relationships found in nonhuman anthropoids. This evidence for conservation in scaling supports the idea that limbic functions are necessary for human symbolism and culture. KEY WORDS:

Limbic system; Amygdala; Hippocampus; Septum; Memory; Emotions; Allometry; Brain

*The opznzons or assertzons contained herezn are the przvate vzews of the author and are not to be construed as officzal or as reflecting the vzews of the Department of the Army or the Department of Defense.

Received May 9, 1990; accepted October 25, 1990. Address all correspondence to Este Armstrong, Yakovlev Collectzon GO51, American Registry of Pathology, Armed Forces Instztute of Pathology, Washzngton DC 20306-6000.

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The limbic system of the brain is composed of interconnected populations of neurons that are functionally involved with emotions, memory, and olfaction. The collective name for these cortical and subcortical structures, the limbic system, originated in studies by Broca (Broca 1878), the famous nineteenth-century French neurologist and one of the founders of French physical anthropology. Broca had been impressed by the architectural contrast between the structures close to the corpus callosum and inferior horn of the lateral ventricle on the medial wall of the cerebral hemispheres and those of the rest of the cortex. Although both cortical groups are structurally heterogeneous, larger differences exist between them than within them. Broca viewed the differently structured medial cortex as a lip around the centrally placed brainstem and consequently he chose the term limbus to describe it (Broca 1878). The classical works of Papez (1937), MacLean (1952), and others (Isaacson 1974; Nauta 1979; Livingston and Escobar 1971) have carried the term forward to modern times, changing it from a description of a location to one of an integrated circuit. The exact anatomical limits of the limbic system continue to be debated, but the telencephalic regions of the septum, amygdala, and hippocampus and the subcortical structures of the mamillary bodies and anterior thalamus are included in most definitions and will be used in this discussion (Figure 1). Because the olfactory tract terminates in the amygdala and in the surrounding perirhinal cortex, the first studies of limbic structures concluded that they were sensory regions involved solely with olfaction. By the 1940s, however, it was established that olfaction was only one of several limbic functions. Emotions and memory have not only been added as functions of the limbic system but are now considered the predominant functions of the limbic system in human and n o n h u m a n primate brains (Isaacson 1974; Livingston and Escobar 1971; Papez 1937). Some limbic structures, like the amygdala and surrounding cortex, are associated with anxiety, aggression, and negative feelings (Mark and Ervin 1970; Reiman et al. 1989). Appropriate electrical stimulation in this region causes an individual (human or nonhuman) to stop on-going activity and scan the environment. If stimulation is continued a person can exhibit uncontrollable rage, like smashing a guitar against a wall, beating a wall with their hands, or in the case of monkeys, attacking others (Mark and Ervin 1970; Robinson et al. 1969). Stimulation of other areas, especially the septal area, produces more positive feelings and sexual responses in human patients (Heath 1963). The hippocampus plays a critical role in changing short-term memory into long-term storage. The latter is done not in the hippocampus but throughout the neocortex. Interruption of the integrity of the hippocampus produces

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Figure 1. Diagram of the medial surface of the h u m a n brain indicating the location of major limbic regions. CC = corpus callosum, AT = anterior thalamus and M = mamillary body, CG = cingulate cortex, S = septal region, A = amygdala, H = hippocampal region. The dotted lines indicate that the structure is well below the medial surface.

anterograde amnesia in which the patient cannot form new memories. These patients, for example, cannot commit an on-going conversation to memory. Once a disruption occurs, they are unaware that the topic has been discussed. On the other hand, new motor skills can be retained even though the patient is unaware of those abilities. Intelligence, creativity, and other aspects of their personalities are not impaired (Squire 1986). Research on the h u m a n limbic system and emotional behavior has frequently been carried out within the framework that these behaviors, as contrasted with those of cognition, are shared with other mammals, and thus are primitive (Geschwind 1965). In this paradigm, h u m a n emotions and their neurological bases are thought to have remained static during h u m a n evolution. In contrast, cognitive structures are considered to be advanced, having changed substantially during h u m a n evolution, particularly through the enhancement of crossmodal transfer of information and the attainment of language (Geschwind 1965; MacPhail 1982). Concomitant to the view of limbic behaviors as primitive is the idea that structures and circuits of the limbic system are less evolved and play a less important role in the h u m a n brain than they do in other primate brains. Support for this idea comes in part from the fact that the ratio

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between neocortical volume and those of structures in the limbic system is bigger in human brains than in the brains of other primates (Andy and Stephan 1976; Clark 1959; Smith 1895). This model also suggests that human cortical functions like symbolism and rationality evolved by becoming free from limbic influences (Geschwind 1965; Jurgens 1982; Livingston and Escobar 1971; Yakovlev 1971). A corollary thesis is that human emotions evolved only indirectly w h e n the cortex began to inhibit and otherwise control the primitive limbic output. Another point of view is that the limbic system plays an important role in h u m a n behavior. In this paradigm the tremendous differences between human and n o n h u m a n primate behaviors, including the development of language, did not arise w h e n limbic circuits were separated from those of the neocortex (Laughlin and d'Aquili 1974; Pribham 1967; Reynolds 1981; Steklis and Raleigh 1979). Rather, the h u m a n brain and behavior evolved along qualitative forms established in anthropoid primates. The differences between the two paradigms can be tested in part by analyzing neurobiological data. Although during primate evolution the neocortex expanded in size more than structures in the limbic system did, it does not follow that limbic regions have not evolved (stabilized in size) or that they were selected against (diminished in size). A n d y and Stephan (1976) point out that in ranking the importance of neural populations according to their sizes, it is necessary to use an independent standard for the overall size of the organism. In their analyses of the septal region they chose body weight as that standard. Allometric analyses clearly demonstrate that the primate septum has increased in size and is relatively bigger w h e n compared to that of insectivores. The human septum is both the largest, in absolute terms, and given our body weight, it is also the largest primate septum in relative terms (Andy and Stephan 1976; Steklis and Raleigh 1979). Another standard useful in analyses of the size of limbic structures is brain weight. The relative rankings among primate septums mentioned above reflect the fact that the brains of primates are bigger than those of insectivores, and that the h u m a n brain is the largest of all. To determine whether evolution has preferentially changed the relationship between limbic structures and the rest of the brain, it is necessary to study the size of limbic regions standardized by brain weight. The size of a particular neural structure may or may not retain a stable relationship with that of the total organ. Increases in size suggest that the neural structures continue to play a dynamic role in the functioning of the brain. If the relationship between the size of a nucleus and brain weight is not stable, then selection pressures can be hypothesized to have acted specifically on a restricted region or circuit. If, on the other hand, the

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size of a nucleus retains the same relationship with the brain, then selection pressures may have worked to preserve a form of interaction. In the latter case, however, a complication can arise if the scaling between the size of the nucleus and brain weight is not 1. Scalings that are larger or smaller than 1 (positive or negative allometry, respectively) change the proportions among various neural structures. In turn, by shifting relative numbers of input and output fibers, differing proportions have the potential to alter how a nucleus or circuit functions. Determining the specific role that the changed proportions play requires knowledge of structure-function relationships. The wealth of new information on how limbic structures are interconnected with the cortex, combined with allometric analyses of the sizes of structures, promises to bring a new appreciation of the role of limbic structures in the h u m a n brain and h u m a n evolution.

SCALING STUDIES Scaling studies require quantitative data that are both difficult and laborious to collect. Because limbic structures tend to be more anatomically distinctive than other neural regions, however, several have been measured. Allometric studies can then determine whether the sizes of the regions are a function of brain size, and if so whether they change at a similar pace with each other and with the brain or whether certain parts deviate from the trends set by overall brain growth. In the latter case, structures that become relatively bigger or smaller than expected suggest that selection pressures have increased or decreased a particular pool of neurons. It is generally assumed that more neurons translate into increased integrative potential, so the size of a neural population provides a rough estimate of capacity (Williams and Herrup 1988). The more neurons in any given neural circuit, the more permutations of integrative patterns are possible. In addition, with an increased number of neurons, signals can be strengthened (or weakened) by increasingly refined gradations, thus providing more subtle processing and functions (Bonner 1988). Size is therefore one indication of potential capacity. The first step in allometric studies is to determine whether the size of a neural structure is the one expected given the size of the rest of the brain. This step is particularly important w h e n the h u m a n brain is included since it is much larger than any other primate brain. Although the central paradigm of the evolution of h u m a n emotional structures in anthropology suggests that limbic structures should be relatively, if not absolutely, smaller in the h u m a n brain, a review of the sizes of limbic structures reveals that they are not regressive. Limbic structures in the

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human brain, such as the septum, amygdala, hippocampus, mamillary bodies, and anterior thalamic nuclei, are the sizes that would be expected in any anthropoid (monkey or ape) whose brain is scaled up to human dimensions (Figure 2; Armstrong 1982, 1986). The major regions are composite structures. For example, the septum, a region involved with the sensation of pleasure and learning (Isaacson 1974), and the amygdala, which is concerned with fear, aggression, and memory systems (Isaacson 1974; Mark and Ervin 1970), are composed of separate nuclei or neural populations whose morphometric characteristics change independently (Steklis and Raleigh 1979; Stephan et al. 1987). Future studies will help to determine whether, given particular shifts in brain weights, all parts of the regions have altered along similar paths. Data standardized according to body weight suggest that different scalings are to be expected (Andy and Stephan 1976; Steklis and Raleigh 1979; Stephan et al. 1981). The next step of analysis should be to look at the relative sizes of the major nuclei in relationship to brain size. The scaling studies suggest two things about the size of the h u m a n limbic system. First, the sizes of most limbic structures are correlated with that of the whole brain. H u m a n limbic nuclei are usually both

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Figure 2. Scattergram showing the size of the septal region (in m m 3) as a function of brain weight (in g). N o n h u m a n anthropoid values are crosses; the human point is a star. The observed h u m a n value is equivalent to that expected by scaling a n o n h u m a n monkey or ape brain up to human dimensions. The equation describing the n o n h u m a n regression is log10 septum = 0.99 + 0.75 log10 brain weight, showing that the two features scale in a negatively allometric fashion. Data from Stephan et al. 198I.

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bigger than those of other primates and attain the sizes expected for an ape or monkey whose brains were enlarged to human dimensions. In allometric terms, humans, apes, and monkeys have the same relativesized limbic structures. This finding suggests that limbic structures play approximately the same role in the human brain as they do in the other primates. Second, the neocortex (both white and gray matter) has been measured in a large number of primates (Stephan et al. 1981). Neocortical size also scales with brain weight, and as with limbic structures, the size of the human neocortex is that expected for a monkey or ape whose brain was expanded to human size. One important difference is that the neocortex scales with a slightly steeper slope than limbic structures do, meaning that for every increase in brain weight, cortical volume expands more than limbic structures do. Limbic structures scale with neocortical volume (Figure 3), but because the slope is less than 1, larger-brained monkeys have bigger neocortex-limbic system ratios than smaller-brained monkeys. Humans, as a simple consequence of in10000

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LOG NEOCORTEX Figure 3. Scattergram of the size of the amygdala (in mm 3) as a function of neocortical size (in mm3). The observed human value is expected on the basis of scaling among n o n h u m a n anthropoids. In the h u m a n brain both the amygdala and septum have the expected size whether the neocortex or brain weight is used as the standard (compare with Figure 2) because the neocortex and brain weight scale isometrically. The equation determined by regressing the amygdala on to neocortical volumes among nonhuman anthropoid genera is log]0 amygdala = 1.70 + 0.63 lOgl0 brain weight. Data from Stephan et al. 1987.

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creased brain size, have bigger neocortical-limbic structure ratios than any other primate. The scaling differential is also found when the analysis is restricted to gray matter (data from Hofman 1988). Given an increase in brain size, both cortical grey matter (composed of neurons and glia cells as well as space for interconnections) and white matter (axons and glia) have bigger correlated size increases than do limbic structures. Thus limbic structures are scaled similarly among human and nonhuman anthropoid primates, but through negative allometry they become disproportionately smaller in relationship to the size of the cortex. Examination of the role of the limbic system in h u m a n behavior must take into account the above two seemingly contradictory aspects of relative size. Because many people have addressed the importance of symbolism and neocortical functions for human behavior, I will not address the importance of the relative increase in the neocortex in this essay. Rather I will present analyses of limbic data showing which portions of the limbic system have increased in size and which have regressed. Using data from these studies and from research looking at the interconnections between the neocortex and limbic system I will discuss the importance of limbic behaviors for human culture.

H U M A N LIMBIC STRUCTURES THAT D O N O T SCALE A C C O R D I N G TO BRAIN SIZE Olfactory Structures Relatively small olfactory centers but enlarged visual structures represent one characteristic of the primate neural pattern (Allman 1982; Clark 1959). H u m a n brains are part of this general primate pattern, but they have deviated in the decrease in size of olfactory structures both absolutely and relative to brain size (Sacher 1970). The absolute and relative decreases in the olfactory receptive and integrative centers suggest that smell plays a tess important role in our behavior than it does in other primates, including those of the apes (Allman 1982; Andy and Stephan 1967; Smith 1910; Steklis and Raleigh 1979). Any interpretation of these decreases must take into consideration the fact tha~ all sensory structures are relatively small in the h u m a n brain when they are compared to homologous structures in nonhuman primate brains. In human and ape brains many visual and auditory structures have similar absolute sizes (Armstrong 1979, 1982; Passingham 1973; Shariff 1953). Somatosensory nuclei are enlarged in the human brain, but they have not expanded as much as the amount predicted by

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scaling studies that use brain weights as the standard (Armstrong 1979). During human evolution, as the brain expanded, the scaling for all sensory receptive zones lagged behind that of the rest of the brain. Sensory association regions are more difficult to measure and thus less sampled than primary sensory regions, but they seem to have maintained their scaling with brain size (Passingham 1973; Shariff 1953). An exception is the pars triangularis of the septum, which is both absolutely and relatively small in the human brain compared to the sizes in ape brains (Figure 4; data from A n d y and Stephan 1976). The pars triangularis is an olfactory association area in the posterior region of the septum (Andy and Stephan 1976). The stabilization in the absolute sizes of visual and auditory centers between apes and humans is generally not thought to mean that these structures and their constituent functions are less important for h u m a n behavior; rather, it indicates that the amount of information provided by them is adequate for their further elaboration by various association cortices. The same reasoning may be extended to olfactory regions.

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LOG BRAIN WEIGHT Scattergram of the size of the pars triangularis, a posterior nucleus within the septum. In this case the human value deviates from the scaling seen in the other anthropoids and is both absolutely and relatively smaller. Symbols and units are the same as those in Figure 2. The equation describing the size of the septum pars triangularis as a function of brain weight among nonhuman anthropoid genera is log10 pars triangularis = - 0 . 6 6 + 0.48 log10 brain weight. Data from Andy and Stephan 1976. Figure 4.

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Olfactory structures differ from those of the other sensory structures, however. The absolute sizes of both the receptive and the integrative centers in the h u m a n brain have not stabilized; they are smaller than those of many other primates (Andy and Stephan 1967). Absolutely smaller sizes of a neural population in a bigger brain are rare and suggest that active selection for a reduced size, rather than neutral selection, has occurred. A decrease in the sizes of olfactory structures could have arisen from many causes, not all of them attributable to selection pressures acting on olfaction. A changed developmental strategy, for example, could have affected the rate or duration of time that these neurons were being generated or being exposed to the actions of spontaneous cell death. Thus selection favoring a particular developmental strategy could alter the number of neurons in the olfactory system (Finlay and Slatterly 1983; Finlay et al. 1987). The small sizes of olfactory structures in the h u m a n brain do show that limbic structures can be reduced in size. In this manner they deviate from the remainder of the limbic system. The fact that the other structures have not been similarly reduced in the h u m a n brain indicates that they continue to modulate h u m a n behavior in important ways. If the major h u m a n adaptation were one of freeing rational thinking and cognitive processing from limbic influences, why have the limbic structures not decreased in size the way the components involved with olfaction have? The known functions of the limbic structures suggest that they meet three important necessities for a cultural and symbolic way of life: memory, social organization, and emotions. Before these roles are discussed, a limbic nucleus that is bigger in the h u m a n brain than expected on the basis of its scaling with brain weight among n o n h u m a n anthropoids needs to be noted. The Anterior Thalamus

The principal nucleus of the anterior thalamus is an integral part of Papez circuit, a neural pathway thought to bring emotional information to the cortex where it is further elaborated upon and brought into consciousness (Papez 1937; Ploog 1989). Compared to the relationship between the number of anterior thalamic neurons and brain weights in monkeys and apes, h u m a n brains have more anterior thalamic neurons than do those of the n o n h u m a n anthropoids even if their brains were enlarged to h u m a n dimensions (Armstrong 1980, 1986). The cause for this shift is not yet known, but a parallel alteration is found in the brains of n o n h u m a n anthropoids living in social organizations typified as containing one adult male (Armstrong et al. 1987). The parallelism exhibited

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by these anthropoids may help to clarify the role of these limbic structures and is discussed more fully below. The main nucleus of the h u m a n anterior thalamus contains more neurons than expected by allometrically enlarging a n o n h u m a n anthropoid brain. Thus selection pressures can and have specifically increased some limbic populations in the human brain. Both the allometrically expected and unexpected increases in the limbic system could be independent of or a part of our major h u m a n adaption, culture. The rest of this article argues that the h u m a n limbic system, rather than being a neural center that needs to be "escaped from" in order to have a cultural way of life, plays a critical role in supporting it.

LIMBIC FUNCTIONS IMPORTANT FOR CULTURE

Memo~ If learned, shared rules of behavior are to guide our lives, then our brains must be capable of readily making new information into accessible memories. A cultural way of life would be impossible without the ready formation of new memories that can become part of the background with which new information can be compared. Although the storage of memories is probably a function of the neocortex, the ability to form and retrieve them is a function of the limbic system (Mishkin and Appenzeller 1986; Squire 1986). The content of the memory traces is obviously dependent on what is brought to the limbic system, which is a function of the pattern of connections between the cortex and the limbic system. An important characteristic of the anthropoid brain is that the limbic system receives its information from the association areas of the cortex, both polymodal and unimodal (Mesulam 1981; Pandya et al. 1988), rather than directly from primary sensory regions. Information about the outside environment flows in a serial fashion from the primary sensory receptive regions into unimodal and then into polymodal association areas. At each stage the information is further processed. The limbic system receives its information at the end of the serial processing and is thus provided with elaborate sensory information. Since the neural integration within the polymodal association cortex is thought to underlie symbolism (Geschwind 1965; Penfield and Roberts 1959), limbic structures, including those portions involved with memory functions, are as prepared to

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process cognitive thoughts (symbols) as they are to process information about the external environment. The limbic structures, the amygdala and hippocampus, are particularly important in the establishment of memories. People and monkeys with damaged hippocampi and amygdalas live in a continuous present and are unable to remember items, persons, or instructions for more than a few seconds or once their attention has been distracted (Squire 1986). Their ability to survive d e p e n d s on the continuous presence of caretakers. A behavioral system based totally on the present would be intolerable for a cultural adaptation. Enlargement of the limbic system is critical for the creation of a brain that is capable of remembering cultural rules and events. An analysis of the management of spatial information and the coding of language has led to the suggestion that functional limits of the human hippocampus structure human language and, by extension, human cognitive maps (Wallace 1989). Involvement of the hippocampus in coding and decoding culturally determined rules of language would also require more neurons for the processing of additional information. Thus the human limbic system would be expected to be bigger than that of nonhuman primates. If an enlarged limbic system is important for human behavior for mnemonic purposes, parallels should exist in other animals for w h o m memory has become important for survival. The hippocampus, thought to play an especially strong role in the creation and maintenance of spatial maps of the environment (O'Keefe and Nadel 1978), has been hypothesized to be relatively large in the brains of animals that need precise yet flexible spatial maps of the environment. Food-storing birds, for example, need to remember the location of their food caches. Morphometric studies of their brains have shown that food-storing birds have relatively larger hippocampal structures than other birds that have fewer requirements for detailed spatial maps (Sherry et al. 1989). An elaboration of the hippocampal circuitry needed to produce these maps could have been critical for early hominids fanning out from sheltered areas to gather, scavenge, or hunt. The increase in hippocampal size for spatial maps could have been a preadaptation for the development of limbic structures enlarged sufficiently to manage the flow of memories that are critical for a cultural way of life.

Social Organization A cultural way of life requires sharing information. Limbic functions are concerned, among other behaviors, with labeling stimuli as positive

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or negative. Although lesions and stimuli to limbic structures provide examples of dramatic changes in emotional behavior, the limbic system does not function in an all-or-none manner. The valences produced by the activation of limbic structures can vary from fleeting feelings to sustained and intense forms of aggression and sexual behavior. H o w these emotions are integrated among themselves and with cortical functions can impact social organization directly. The cingulate cortex, for example, has been implicated in the organization of maternal behavior (Murphy et al. 1981). In h u m a n evolution the limbic system may have evolved in size to sustain forms of social organization that permit or maximize certain types of cooperation. If true, one would expect that other limbic structures would also have evolved differential sizes in other taxonomic groups. A morphometric study of limbic structures among apes and monkeys provides an example (Armstrong et al. 1987). The study indicates an association between the relative size of the anterior thalamus, a limbic population interconnected with the hippocampus and cingulate gyrus, and social organization. Although the cause of the association is not yet known, the correlation suggests that the integration of learning and memory states with those of emotions may be slightly different in anthropoids with different forms of social organization. The facts that nonhuman anthropoids have protean forms of social organizations, which can alter under changed ecological pressures (Wrangham 1987), and that human culture determines major aspects of human social organization do not mean that the relative sizes of neural populations cannot be significantly associated with social organization. Rather, the relative sizes may set particular thresholds or establish a particular configuration of interactive sites that may make certain stimuli more effective than others. The limbic system is set to receive multimodal and unimodal information from the association cortex. This type of pathway means that the limbic system is not solely reacting to particular stimuli (e.g., faces, or profiles of hawks) but to the context in which they appear. The ability to cooperate may depend in part on the ability to approach other individuals without engendering hostile or sexual behaviors. This situation may depend not only on the association cortex sending a myriad of stimuli to the limbic system but also on the ability of the latter to integrate information in a flexible manner, adjusting it according to the context. This ability in turn suggests that the limbic system must be of sufficient size compared to that of the cortex to enable the necessary integration of cortical information with the reward or punishment of limbic labeling. Cooperation requires that the limbic sytem be large enough not just to react to, but to modulate and integrate, cortical information.

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Emotions

The human capacity for culture and symbolization is sometimes contrasted with our ability to feel emotions. Although the creation of symbols and the emergence of emotions involve different circuits, interactions between the association cortex and the limbic system enable arbitrary symbols to capture our attention, satisfy our desires, and sustain our actions. If symbols were devoid of limbic processing, they would not interest us. Our brains are continually being bombarded with sensory information, and it is the job of the limbic system to help to select (focus attention on) a few of the on-going events or objects (Isaacson 1974). Stimulation of limbic structures causes an animal to stop what it is doing and scan the environment. Discharges in the limbic system signal the fact that attention priorities may need changing. Several nonlimbic parts of the brain are also involved with attention. The parietal association cortex contains command neurons for the motor system and has been the focus of research concerning attention (Mountcastle 1978). Destruction of the human parietal cortex produces a n~glect of stimuli that are in the side opposite from the lesion. Patients with large lesions do not see objects or the parts of objects that lie in the contralateral visual field. In extreme cases they may refuse to shave or dress that side of the body (Denny-Brown and Chambers 1958). Destruction of the polymodal parietal cortex most commonly produces this type of deficit (Mesulam 1981). Other cortices, including the frontal and temporal lobes, are also concerned with directing attention to stimuli (Posner and Peterson 1990). Analyses of these types of lesions show that the parietal cortex, and to a lesser extent the frontal and temporal lobes, are necessary for the organization of the sensory information that enables perception or the focusing of attention on particular events. Without these association cortices, stimuli cannot be properly sensed. Cortical neurons can maintain the focus of attention on selected items, but when several competing stimuli are present, each of which is adequately focused by the relevant association cortex, another system is required to decide which stimulus should be given priority. The limbic system with its labeling of stimuli with positive or negative valence and its capacity to access past events plays a critical role here. Experiments looking at conflict between frontal and parietal attentional systems have found that it is the activity of a timbic structure, the cingulate gyrus, that is most directly affected (Mesulam 1981; Mirsky 1987). For the limbic system to direct attention toward a symbol, it must receive information from the polymodal association cortex. The primate limbic system both receives and sends information to polymodal cortical

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areas. The parietal cortex, for example is interconnected with the cingulate gyrus (Mesulam et al. 1977; Pandya et al. 1981), a part of the limbic system that interacts with the hippocampus and anterior thalamus (Papez 1937). In the parietal region the lirnbic input is denser to the polymodal cortex than it is to unimodal areas, which means that the limbic system is more involved with the most extensively processed information (Pandya et al. 1981; Mesulam et al. 1981). Likewise the amygdala is interconnected with both the polymodal and the unimodal temporal lobe association cortex, and the most highly processed information shows the most connections with limbic structures (Pandya et al. 1988). If the human limbic system, like the cingulate cortex, had evolved a different form of connections and was not interconnected with the association cortex, one would expect the cellular architecture to differ between humans and other primates. No differences of this type have been observed (Armstrong et al. 1986; Zilles et al. 1986). Organizational differences in this part of the brain have been observed to separate N e w World from Old World monkeys, showing that shifts in organization are detectable, but the human organization is the same as that found in Old World monkeys and apes. Because the polymodal cortex, a neurological substrate for symbolization, has direct connections with limbic structures, the activities of the latter cannot be restricted to the modulation of drives and simple stimuli; rather, these structures are accessing the most complex neural patterns. In human behavior, symbols compete with other extrapersonal events for our attention. Without the ability to label them along a positivenegative emotional continuum, external symbols would not hold our attention and would become part of the background noise. Following this labeling, choices about particular actions can be made. In addition to the selection of items for our attention, the limbic system also invests symbols and events with a sense of satisfaction, a sense of completeness. Without these feelings or labelings, a cultural way of life would not be possible. Structures in Papez circuit (the hippocampus and cingulate gyrus) are particularly well placed for being activated by symbolic thought processes. The hippocampus in the temporal lobe receives highly processed visual and auditory information. The cingulate cortex with its reciprocal connections to the parietal and prefrontal cortices can focus attention on items in the extrapersonal space (parietal lobe) or items in the internal environment (prefrontal cortex; e.g., goals). An enlarged limbic system strategically placed to receive a maximal amount of information from the association cortex enables a cultural adaptation by giving symbols access to the limbic system that is equal to that of information derived from sensory systems. This ability in turn

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permits the individual to focus attention o n arbitrary symbols, to h a v e those symbols satisfy basic desires, a n d to sustain c o n t i n u i n g symbolic/ cultural behaviors.

SYNTHESIS Structures in the limbic system have e n l a r g e d d u r i n g h u m a n evolution. A l t h o u g h the functions of these structures are frequently o v e r l o o k e d in studies of the neurological basis for cultural adaptation, t h e y play a critical role. T h r o u g h their rich i n t e r c o n n e c t i o n s with association cortices, limbic structures m o d u l a t e r e s p o n s e s to a n d m e m o r i e s of symbols. The processing of association cortex i n f o r m a t i o n by the limbic s y s t e m e n d o w s s y m b o l s with m e a n i n g a n d i m p o r t a n c e . W i t h o u t this limbic processing, s y m b o l s w o u l d neither hold o u r attention nor b e c o m e part of our individual or collective memories. The work was supported in part by grants from the National Science Foundation (BNS-8204480 and -8820485) and the American Registry of Pathology.

Dr. Armstrong is currently the Distinguished Saentlst of the Yakovlev Collection, one of the world's largest human brain collections. She also teaches neuroanatomy at the Uniformed Services University of the Health Sciences m Bethesda, Maryland. Her primary research interests center around the evolution of the human brain and questions concernmg the role of the hmbic system and the causes of differences m relative brain size. She is currently investigating parallels in the development and maturation of three regions of human and rhesus monkey brains in order to test hypotheses concerning the role of delayed maturation in human brain evolution. She is also using some of the techniques developed to answer evolutionary questions to determine how brains from schizophrenic patients differ from those of normals. Other publications by Armstrong include "An Evolutionary Perspective" in The Human Nervous System, G. Paxinos, ed. (Academic Press, 1990) and "'Relative Size of the Anterior Thalamic Nuclei Differentiates Anthropoids by Social System" with M. R. Clarke and E. M. Hill m Brain, Behavtorand Evolution 30:263-271 (1987).

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