Functional architecture of the mammalian retina.

PHYSIOLOGICAL REVIEWS Vol. 71, No. 2, April 1991 Printed in U.S.A.

Functional

Architecture HEINZ

W&SLE

of the Mammalian AND

BRIAN

Retina

B. BOYCOTT

Max-Planck-Institut fiir Hirnforschung, Neuroanatomie, Frankfurt, Federal Republic of Germany; Department of Anatomy, Guy’s Hospital Medical School, London, United Kingdom

I. II. III. IV. V.

VI.

VII.

VIII.

Introduction ......................................................................................... Retinal Topography ................................................................................. Photoreceptors and Spatial Sampling .............................................................. Horizontal Cells ..................................................................................... Bipolar Cells ......................................................................................... A. Cone bipolar cells and ON- and OFF-dichotomy of the retina ................................... B. Types of cone bipolar cells ....................................................................... C. Rod bipolar circuitry ............................................................................. Amacrine Cells ...................................................................................... A. Amacrine cell diversity .......................................................................... B. Glycinergic amacrine cells ....................................................................... C. Cholinergic amacrine cells and directional selectivity .......................................... D. y-Aminobutyric acid-ergic amacrine cells ...................................................... ...................................... E. Definition of amacrine cells and their functional polarity F. Conservation of amacrine cell shape ............................................................ .......................................................................... G. Amacrine cell coverage Ganglion Cells ....................................................................................... A. Physiological classes ............................................................................. B. Morphological classes ............................................................................ C. Stratification of ganglion cell dendrites ......................................................... D. Ganglion cell coverage ........................................................................... ..................................................................... E. Ganglion cell microcircuitry Ganglion Cell Function .............................................................................. A. Spatial resolution ................................................................................ ............................................................................... B. Stimulus detection ........................................ C. Ganglion cell density and cortical magnification factor

I. INTRODUCTION

Neuroanatomic studies of the mammalian retina have the invaluable advantage that, as difficulties arise in the functional classification of a structure, auxiliary information from physiology, psychophysics, or knowledge of vision in general can help to solve the problem. When small pieces of the mammalian retina were observed by microscopy more than 150 years ago, a dispute arose as to which elements might be the “light sensors.” This was resolved by trying to explain a psychophysical experiment. By 1830, Purkinje had demonstrated that the blood vessel pattern of the inner retina became visible when an observer looks through a pinhole. Exploiting this entoptic phenomenon, Mtiller (251) established a position for the light detectors, placing them at the rod and cone layer. Ten years later, Schultze (343) published a view, still valid, of the cellular elements of the retina (Fig. 1A) without, of course, being able to resolve their connectivity pattern. Schultze also studied whole flatmounted human retinas. Thus Schultze could demonstrate that the fovea contains exclusively cones and that 0031-9333/91

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rods are mixed with cones only outside the fovea. Knowing the fovea is blind at night, Schultze concluded that cones are responsible for photopic and therefore color vision, whereas rods mediate scotopic or night vision. A third example of the fruitful interplay between knowledge of the structure of the retina and a predicted function is illustrated in Figure 1B. Cajal(49), using the then newly discovered Golgi-staining method, described in detail the cellular components of the retina. Knowing that “vision propagates from the outer towards the inner retina,” Cajal made a flow diagram of how signals might pass from the photoreceptors through the retina to the brain. Cajal regarded retinal organization as particularly strong support for his ideas about the functional polarity of neurons, i.e., that dendrites receive signals and that axons are the outputs (296). Although the idea of functional polarity and, more generally, of neurons not forming a syncyticum were first formulated by Cajal for the cerebellum, “the study of the retina shed light on the general problem and mechanism of action of nervous cells” (50). The object of this review is to survey current under447

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trates more on the functional approach to understanding the retina as a system, a system that translates images into neuronal representations. II. ONL

OPL

INL

I PL

GCL

ONF FIG. 1. Schematic diagrams of vertebrate retina. A: vertical view of neural elements of human retina. OS, outer segments; IS, inner segments; ONL, outer nuclear layer; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; GCL, ganglion cell layer; ONF, optic nerve fiber layer. [Adapted from Schultze (343).] B: signal flow through retina according to Cajal (50). a, Rod bipolar cell; b, cone bipolar cell; c, large ganglion cell; d, small ganglion cell; e, cone; f, rod; SVC, subcortical visual center.

standing of how the different neurons of the mammalian retina are arrayed and interconnected to form functional units. Since the discovery of the concentric receptive fields of mammalian retinal ganglion cells (It%), the trigger-feature units of frog retinal ganglion cells (16, 193), and the directionally selective ganglion cells of the rabbit retina (19, ZO), there has been a rapid escalation of literature on the physiological properties of individual cells, the definition of functional units, and the identification of morphological and neurotransmitter types. Intracellular recording from retinal cells has, largely for technical reasons, been carried out in nonmammalian retinas. Many of these results can be generalized to mammalian retinas; however, we also examine some instances where there are differences. The cell biology of the vertebrate retina has been summarized recently by Dowling (87), and selected topics of retinal function, such as the biophysics of phototransduction (23,24,143, 189, 431, 432), the molecular biology of photopigments (260262, 294), and neurotransmitter systems (44, 77, Zll-213,232,242,247) of the retina, have been reviewed. Several recent reviews have summarized the structural element and circuits of the mammalian retina (226,227, 314, 362, 363, 365, 392). Our review therefore concen-

RETINAL

TOPOGRAPHY

Most mammalian retinas contain a specialized region of high cell density (146). In primates this is the “fovea,” in cats it is the “central area,” and in rabbits it is the “visual streak.” These regions are specialized for high visual resolution, and by coordinated movements of head and/or eyes, an object can be fixated so that its image can be brought into register with the fovea or central area. The whole retina cannot have such a high resolution because of limits of space in the cerebral cortex. Within the fovea1 projection to primary visual cortex (Vl) of the macaque monkey, 100 mm2 of cortical surface are dedicated to 1 degree2 of visual space (382, 388). If this were extrapolated to include the whole visual field, Vl would require a cortical surface of >l X lo6 mm2. This is ~100 times more than the total cortical surface of the macaque monkey. Hence only a minute fraction of the visual field, the fovea, can be so largely represented. As reviewed by Hughes (146), different animals show varied regional specializations of their retinas, which are adapted to their habitats. The visual streak of rabbits, for instance, is a high-density area that scans the horizon. The existence of such specialized regions of high resolution raises the following question: Are the neuronal elements and their connections different in such areas, or are the functional units the same all over the retina, subject only to scaling and proportional changes? When the densities of cones, rods, and ganglion cells of cat and monkey retinas are compared, common features can be observed (Fig. 2). Ganglion cells show the steepest density gradients, with their density changing from central to peripheral retina by a factor of 50100 in cats and by more than a factor of 1,000 in monkeys, whereas cones have a shallower gradient. Rods are absent in the monkey fovea (277,343), and correspondingly, there is a local minimum in the cat central area (360). The number of cones per ganglion cell is smallest in the fovea and central area (0.3 cones/ganglion cell in the fovea, 3-4 cones/ganglion cell in the central area) and increases continuously toward the peripheral retina. At 10 mm eccentricity there are 16 cones for each ganglion cell in monkeys and 20 cones in cats. Thus the spatial grain, responsible for visual resolution, is improved by two factors: 1) the densities of cones and ganglion cells are increased toward the central retina, and 2) the ratio of cones to ganglion cells is decreased. The anatomic limit is reached by the primate fovea. Here midget ganglion cells are connected through midget bipolar cells to a single cone (36, 300). In the cat central area ,&ganglion cells are connected to about four cones (363). It is important to decide whether changing convergences, expressed by the density curves of Figure 2, reflect different functional circuits or simply represent


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of rods, cones, and ganglion

ECCENTRICITY

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lar to cat P-cells, have rather large dendritic fields in the peripheral retina, and their sizes decrease toward the central retina (413). However, at eccentricities t3 mm, PP-cell dendritic fields remain rather constant, and, as Figure 2 shows, at comparable eccentricities, ganglion cell density exceeds cone density. This seems to be the eccentricity, where PP-cells can receive input from only one cone and their dendritic field size does not therefore decrease further. Thus, given these graduated changes, midget ganglion cells are nothing special but just fovea1 PP-cells. In the preceding paragraphs we argue that there is an “uniformity” of retinal units and circuits within the retina of a given species. It is very likely that such a uniformity and conservation of circuits can also be documented when retinas from different mammalian species are compared. The rod pathway, the directional selective (DS) circuitry, and details of amacrine cell morphology and transmitters are shown in this review to be very similar in most mammals. This is the reason why a more generalized view of the mammalian retina is presented; differences between species and regional specializations are dealt with in section VII.

and III.

a scaling of the same basic wiring pattern. In the cat retina, the density changes of ganglion cells are an order of magnitude less than in the monkey retina; hence the situation is more transparent. It is illustrated for ,&ganglion cells in Figure 3. The density of ,&ganglion cells decreases from center to periphery, but the dendritic field size increases at the same rate. Consequently the product of dendritic field size and density, the coverage factor, remains constant with changing eccentricity (400). The same inverse relationship has been found for many other neuronal cell types of the retina. Physiological recordings from central and peripheral retina have not revealed a basic functional difference within a given physiological class; rather they suggest a scaling that is proportional to the dendritic field changes. Hence it is very likely that in the central area and the peripheral retina of cats there are identical functional circuits differing only in spatial scale and numbers of cells. The fovea of the primate retina at first sight seems to be an exception to this general rule, and in particular, midget ganglion cells could be considered as a distinct cell class uniquely associated with the fovea. As has been shown by Perry et al. (292), PP-ganglion cell& simi-

classes

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ARCHITECTURE

’ Three different names are used at present to identify two Pp- and Pewof ganglion cells of the macaque mo nkey retina:

PHOTORECEPTORS

AND

SPATIAL

SAMPLING

Two types of photoreceptors transduce a light stimulus on the retina into an electrical signal: rods respond to dim lights and mediate scotopic vision, whereas cones operate in bright light and are responsible for color vision. Within the last years much detail concerning the function of rods and cones has been obtained. This information includes the molecular genetics of rod and cone pigments (260-262, 294), the physiology of their spectral absorbance curves (25, 26, 341), the biophysics of the transduction process (23,24,116,131,143,165,189, 431, 432), and also the voltage- and transmitter-gated currents of their inner segments (13,15,21,157,158,334, 372,373). It is disappointing after all this progress that the cone types of mammals cannot yet be fully distinguished by morphological criteria. Blue cones can be recognized from immunocytochemical staining (249, 370, 371) and by other criteria, such as selective uptake of Procion dyes. They are also relatively different in size from red and green cones (Fig. 4A) (3,80,81). Blue cones are generally agreed to be between 10 and 18% of the cones in rhesus monkey, baboon, and human retinas. They are arrayed in a regular lattice (349) but are practically absent in the fovea. There is less agreement on the relative proportions of red to green cones. With the use of selective bleaching and activity markers the ratio was found to be I:2 in the baboon (215). However, the generality of this result has been questioned recently on the basis of psychophysical cells, midget and parasol cells, P- and M-cells. In this review, we use Pp- and Pa-cells, following the original definition of these cells (292). When for brevity we use “primate” we mean macaque monkeys unless otherwise specified.


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FIG. 3. Mosaic and dendritic field size of P-ganglion cells in cat retina. Open circles, cell bodies of OFF-@cells, which were retrogradely labeled from lateral geniculate nucleus (400). A comparable but independent mosaic was also found for ON-(?-cells. Eccentricity is -1 mm in A, 1.7 mm in B, and 5 mm in C, frames are 250 X &SO-pm wide. Dendritic fields inserted were taken from Dann et al. (76) and represent Lucifer yellow-injected ,&cells. Dendritic field size and perikaryal spacing increases in proportion from A to C; apparently dendritic field is delimited by immediate neighbors.

experiments in humans (55), which suggest a ratio of 21. Estimates of the relative encounter frequencies from microspectrophotometry claim equal numbers of red and green cones in rhesus monkeys (133). The spatial mosaic formed by primate fovea1 cones (Fig. 4B) has recently been analyzed in considerable detail, because the cone array determines the limits of spatial resolution, hyperacuity, and stereovision (140, 141). The absorption spectra of red and green cones overlap to a large extent (26, 341), and therefore their synergistic information can be used as a luminosity signal in spatial sampling (152,191,246). It is an attractive idea that during evolution of the fovea the primary selection pressure was for improved visual acuity and hence for higher cone density and lower cone-to-ganglion cell convergence. When the anatomic limit was reached, one cone was connected through a midget bipolar cell to a midget ganglion cell. Later mutations in the cone pigments superimposed on this one-to-one connection established the chromatic system (260, 262). However, the requirements of high acuity meant that the action spectra of the cones had to remain close. The lack of a morphological distinctiveness between red and green cones, the common regular mosaic (410), and the retention of the full numbers of cones in dichromats (54) give circumstantial support to this idea of their late evolution. In retinas with lower spatial resolving power, such as in goldfish or turtles, the peak sensitivities are further apart (132), and there are independent mosaics of chromatically different cones (252, 342). Within the primate fovea the cones form a regular hexagonal mosaic (67, 140, 141, 279, 329), with a minimum center-to-center spacing (a) of 2-3 pm (Fig. 4B). The resolution limit (Nyquist limit) is @a (Figs. 4B and 5A) (356). Why is a spatial interpolation procedure not used to gain higher resolution (423)? Figure 5A illustrates that such an interpolation could improve resolu-

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tion for gratings from v3a to a. However, as first observed for the insect visual system (123), spatial interferences would result in a moire effect known as aliasing. In the human fovea, such distortions would occur with gratings of period length 2 mm on the retina. However, their detailed morphology varies, and several morphological types have been described (302). Recently some of the GABAergic amacrine cells have been found to have the capacity to accumulate indoleamines (276, 405). This has been used to identify them for intracellular injection with Lucifer yellow. With this technique two wide-field amacrine cells in the rabbit retina (330,391) and three in the cat retina (412) have been described (Fig. 12, see Fig. 14). Intracellular recordings followed by HRP injection are available for the Al7 cell of the cat retina (269) and from the Sl cell in the rabbit retina (310). They give depolarizing light responses and form reciprocal synapses at rod bipolar cell dyads. The processes of Al7 cells are very thin with characteristic varicosities at the site of their synapses with rod bipolar cell axon terminals (see Fig. 13C’) (178, 332, 366). It has been proposed that these varicosities are, to a large extent, electrically isolated (227). If so, each reciprocal synapse at a dyad could be a locally operating circuit that is not influenced much by activity in other parts of the dendritic field. E. DeJinition Polarity

of Amacrine

Cells and Their

Functional

Amacrine cell processes both receive and make synaptic contacts, but the input and output synapses are

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not necessarily adjacent. Different amacrine cells have characteristic patterns of segregation of synapses. This suggests not only localized synaptic effects (see sect. VIA) but that many amacrines may have a functional polarity. Here we interpret this diversity in a way that may give logical coherence and incorporate into the amacrine cell class such cells as interplexiform cells, which are usually considered to be a separate type. Figure 13 summarizes simple, as well as some extreme, examples of functional polarity in amacrine cells. The AI1 amacrine cells (Fig. 13A) receive their major input from rod bipolar cells and distribute their outputs vertically through the ON- and OFF-layers within the constraints of a narrow dendritic field (113, 362, 366). Their functional polarity is concerned with signal transfer within a small column of the retina. Cholinergic amacrine cells (Fig. 13B) have a functional polarity along a horizontal plane. They receive inputs all over their dendritic fields, but the output synapses are confined to an annulus at the circumference of the cell (43, 107, 112). However, the Al7 amacrine cell (Fig. 13C) seems to have no functional polarity. Numerous fine dendrites radiate away from the cell body, and their varicosities are involved in reciprocal synapses with rod bipolar cell dyads (178,310,332,366). Four further, seemingly extreme, cell types of the inner retina show that “amacrine cells” can be adapted to serve very different strategies for the distribution of input and output synapses. There is no logical reason why they should not be included as amacrine cells. One type is the somatostatin-immunoreactive cell (Fig. 13D), which has its cell body exclusively in the lower retina and projects a single long process into the upper retina (313, 323). Similar cells have been described in the bird retina (49,52,X8) and were named “association” amacrine cells. The second type are the interstitial amacrine cells (Fig. 13E), which were recently injected with HRP by Dacey (69). They have a perikaryon in the IPL, a circular “dendritic field” of ~300 pm diameter, and an enormous multidirectional “axonal field” that is -10 times larger. The third type are the well-known interplexiform cells (37) (Fig. 130. They receive input into the dendritic field within the IPL and have processes leaving the IPL and ascending through the INL into the OPL. There they branch and make conventional synapses onto dendrites of bipolar cells (53,182,201). Unexpectedly there is now evidence that some amacrine cells make synapses within the optic nerve fiber layer to form a third, previously undiscovered, plexiform layer (147,184,392). Because the cells receive input in the IPL and make output synapses onto ganglion cell bodies and ganglion cell axons, they can be included in this general scheme of functional polarity of amacrine cells. However, an important caution has to be applied before the acceptance of a cell as a retinal cell type because errors in development occur. An example is misplacement of cell bodies in an inappropriate retinal layer. In general a “newly discovered” cell should be accepted as a distinct and separate type only when it is certain that such cells provide a uniform coverage of the


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FIG. 12. Drawings of putative y-aminobutyric acid (GABA)-ergic-displaced injected with Lucifer yellow in ganglion cell layer of fixed retinas after labeling mine. Cell on left is Al7 amacrine cell in classification scheme of Kolb et al. (180) Cell at middle probably corresponds to A20 cells and has very few long dendrites. part of their dendritic tree, and have few very long processes, which are probably long. [From Wassle et al. (412).]

retina. A particularly good example for this view are indoleamine-accumulating cells in the OPL of the rabbit, which were injected with Lucifer yellow by Sandell and Masland (330). Originally the authors thought them to be a special type. However, they were able later to stain the whole population (331), and it became clear that the cells were not making a uniform coverage and are therefore clearly misplaced amacrine cells. Association ganglion cells (68, 90, 122) are cells with an axon projecting into the IPL. However, these cells do not form a population with any retinal coverage and are probably also developmental errors. Biplexiform cells (219,437) may well be another example. F. Conservation

of Amacrine

It was suggested shape of an amacrine

Cell Shape

in the preceding section that the cell is to an extent adapted to its

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amacrine cells from flat-mounted cat retinas. Cells were of their cell bodies with the indoleamine 5,6-dihydroxytryptaand has characteristic varicosities all along its fine dendrites. Two cells on risht are putative A22 cells, have spines in central understained here. These processes can be several millimeters

functional role. It is not surprising that once an adaptation has evolved it stays as a constant element of mammalian retinal organization. In recent years several transmitter specific circuits have been sufficiently well studied in different mammalian species for the conservation of shape and transmitter across species to become apparent. Modern transmitter studies in different retinas were initiated with the Falck-Hillarp (105) method of formaldehyde-induced fluorescence (86, 94-96, 271). A narrow stratum of the IPL, close to the amacrine cell layer, became brightly fluorescent and a few, rather large, cell bodies were revealed in the amacrine cell layer. This result has been elaborated in succeeding years, and the dopaminergic amacrine cells have been immunocytochemically stained with antibodies against tyrosine hydroxylase (TH) (45, 46, 224, 271, 278). In whole mounts, TH-immunoreactive fibers form a dense


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FIG. 13. Functional polarity of different amacrine cells of mammalian retinas. A: vertical view of AI1 amacrine cell, which was injected with Lucifer yellow in rat retina. Such a cell receives synapses from rod bipolar cells in lower part of dendritic tree (shown in black) and makes chemical output synapses at lobular appendages in top one-half of dendritic tree (stippled). [From Voigt and Wassle (398).] B: flat view of Lucifer yellow-injected cholinergic amacrine cell in whole mount of rat retina. Cholinergic amacrine cells receive input all over their dendritic field, but output is restricted to annular zone at circumference, where many varicosities are found. Whole mount was also immunostained with antibodies against choline acetyltransferase to reveal all cholinergic amacrine cells (open circles). [From Voigt (39’7).] C: flat view of Lucifer yellow-injected Al7 cell from cat retina (part of Al7 cell in Fig. 12). At varicosities such cells both receive and make synapses. D: whole mount of rabbit retina. Dots indicate cell bodies of somatostatin-immunoreactive amacrine cells, which are restricted to lower retina. Fine processes leaving cell bodies make dense network in upper retina. [From Sagar (323).] E: flat view of horseradish peroxidase-injected interstitial amacrine cell of monkey retina. Cell has a proximal “dendritic field” (dashed processes) and a distal “axonal field” (solid processes). [From Dacey (69).] F: vertical view of Golgi-stained interplexiform cell of cat retina. [From Boycott et al. (37).] See Fig. 1 for definitions of abbreviations. Bar: 20 pm (A), 50 pm (B), 45 pm (0 3 mm (0,100 pm (E), 25 pm FL


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plexus at the INL-IPL border, which contains characteristic “rings” (381) encircling the AI1 amacrine cell bodies. The AI1 amacrine cells receive synapses within these rings (223,301,398), and thus dopamine is thought to play an important role in modulating this crucial interneuron of the rod pathway. Cholinergic amacrine cells are perhaps the best documented example of the conservation of cell shape and transmitter. Their occurrence as matching populations of INL and displaced amacrine cells and the stratification of their dendrites in two narrow bands within the IPL seems to be a consistent feature of all mammalian retinas (107, 293,306, 315,340,375,389,397) and maybe also of nonmammalian retinas (22, 386). As shown in Figure 11, their “starburst” morphology makes them unmistakable across different species. The apparent covariation of shape and transmitter in the mammalian retina has predictive power. As illustrated in Figure 14 for cats, rabbits, and monkeys, all three retinas contain a cell type comparable to the Al7 amacrine cells of cats (178,269,310,332). Although the Golgi-stained examples in Figure 14 are likely to be only partially stained, the common shape of a cell body from which radiate many small straight dendrites bearing tiny varicosities at regular intervals is apparent. In the cat retina, A17 cells have been shown to be GABAergic (302), and both in cats and in rabbits they are engaged with the rod bipolar cell dyad (178,269,310,332). In both species they can accumulate indoleamines (330, 391, 412), which made it possible to inject and stain them intracellularly with Lucifer yellow (see Fig. 12). In the monkey retina only the shape of this amacrine cell is known; however, from the details of the cells in the cat and the rabbit retina, it is reasonable to suppose that this amacrine type in the primate retina is also a GABAergic neuron involved with rod bipolar cells. Many of the modern experimental anatomic techniques cannot be applied in the human retina. However, classic staining of cells is possible and, for the reasons given, we believe predictions with respect to their transmitters and possible functional roles can be made. Differences exist when mammalian amacrine cells are compared with those of nonmammalian retinas. In the tiger salamander retina, GABAergic amacrine cells have small dendritic fields, whereas glycinergic amacrine cells seem to have large dendritic fields (207). The same holds for the fish retina (Zll-213,253,433). In the mudpuppy retina, GABAergic inhibition is tonic, whereas glycinergic inhibition seems to be more phasic (27). This is in contrast to the mammalian retina, where glycinergic amacrine cells exhibit tonic light responses and have small dendritic fields (303).

G. Amacrine

cells trem

Cell Coverage

There are striking differences in the way amacrine CO ver the retina with their processes; the two exes are discussed firs t. The AI1 cells are locally

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operating interneurons, with their cell bodies arrayed in a regular mosaic (390). Their densely branched processes tile the retina with a minimum overlap such that a light spot projected onto the retina is represented in not more than three to four AI1 cells. The coverage of the array is comparable to that of ,&ganglion cells (see Fig. 3). The putative GABAergic A20 (180) amacrine cell is different (412). Figure 12 shows it has only few processes, which run for several millimeters without any side branches. It is meaningless to define a dendritic field and thus a coverage factor for such a cell type. However, as pointed out by Masland (226, 227), the “physiological impact” of a sparsely branched widefield amacrine cell can be assessed by taking the average dendritic length it provides for every square millimeter of the retina. The summated length of the dendrites of one A20 cell (see Fig. 12) is 6 mm. The density of these cells (412) was estimated to be 500/mm2. Therefore in each square millimeter of retina, A20 cells would possess a cumulative dendritic length of 3 m. Were these fine processes woven as a cloth, the spacing between the warp and woof would be only 0.7 pm. Hence the sparsely branched A20 system can make an efficient contribution to signal transfer through the retina. Questions now arise whether, and over how great an area, such a cell might integrate the light stimulus and whether these long fine processes conduct signals. It could be that the dendrites work only as a very local synaptic circuit, such as a GABAergic reciprocal synapse at a bipolar cell dyad. Cholinergic amacrine cells operate somewhere in between the two extremes exemplified by the AI1 and the A20 cell. They have a well-defined dendritic tree, which is small in the central retina and increases toward the peripheral retina, suggesting that the area of this dendritic tree is of functional importance (109,375, 389). However, when their coverage factor is calculated (see Fig. 13B), between 30 and 60 cholinergic cells overlap every point of the retina, suggesting that this cell type is optimized for high synaptic density. Keeping in mind the functional role cholinergic cells might play in directional selectivity, another interpretation of their high coverage factor becomes possible. Although cholinergic cells are morphologically a homogeneous population, physiologically they might comprise different classes depending on the direction of movement to which they are tuned. Thus several different physiological classes could be hidden within the 30-60 cholinergic cells overlapping any retinal point. Although the general shape of cholinergic amacrine cells is comparable between different mammalian retinas, their coverage and the density of dendritic branches per unit area varies. In the rabbit retina, coverage and dendritic branching density are high by comparison with the cat retina. Hence the synaptic density provided by cholinergic cells and their impact should be higher in the rabbit retina. Perhaps this is reflected in the rather high percentage of directionally selective ganglion cells found in the rabbit retina (394).


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FIG. 14. Drawings of putative GABAergic amacrine cells from flat-mounted retinas of different mammalian species. Top left: cell is from Golgi-Cox-stained cat retina. [From Boycott and Wassle (42).] Bottom Zeft: cell is Sl cell and was injected intracellularly with Lucifer yellow after 5,6-dihydroxytryptamine uptake in rabbit retina. [From Sandell and Masland (330).] Top right: cell was injected with Lucifer yellow-filled microelectrode in cat retina and represents Al7 amacrine cell (see also Fig. 12). Bottom right: cell is from Golgi-stained whole-mount preparation of rhesus monkey retina.

VII.

GANGLION

CELLS

A. Physiological Classes

In 1938 Hartline (134) recorded from individual fibers of the frog optic nerve and introduced the term “receptive field”; this is “the region of the retina which must be illuminated in order to obtain a response in any given fiber.” He found ON-cells, ON/OFF-Cells, and OFFcells. Kuffler (188) discovered the concentric, centersurround organization of ganglion cells in the mammalian retina. Barlow (16), Lettvin et al. (193), and later Barlow and co-workers (19, 20) recorded ganglion cells with more complex receptive fields, such as neurons that selectively responded to moving stimuli. A further functional dichotomy of both the ON- and the OFF-center

ganglion cells of the cat retina was found in 1966 by Enroth-Cugell and Robson (102): X-cells had small receptive fields and linear summation, and Y-cells had large receptive fields and nonlinear summation. From studies of the central projections of retinal ganglion cells (54,198,368) came evidence for a further functional segregation of retinal ganglion cells (60, 61, 367). Thus cat retinal ganglion cells can now be subdivided into at least 13 different functional classes (197, 199). In the primate retina, tonic ganglion cells with color-specific and small concentric receptive fields (78, 79,144) project to the parvocellular layers of the lateral geniculate nucleus (LGN) (160-162), and phasic ganglion cells with non-color-specific large concentric receptive fields (78,79) project to the magnocellular LGN layers (159,339). It is to be expected that further physiological classes will be found in the primate retina, of


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which some will project to the LGN and others to the pulvinar, the pretectum, the superior colliculus, and the accessory optic system (194, 317). B. Morphological

Classes

The morphological correlates of X- and Y-cells in the cat retina were found by Boycott and Wassle (42), and the identity of their a- with Y-cells and their ,& with X-cells has been proven by intracellular recordings and dye injections (120,324,357-359) (Fig. 15). The morphological identity of most other physiological classes [sluggish concentric cells and rarely encountered cells (60, 61), W-cells (367, 368)] has still to be found (197). Boycott and Wassle (42) described two further ganglion cell types from their Golgi-stained whole mounts, y-cells and &cells. Kolb et al. (180) described 21 different ganglion cells in the cat retina. A more quantitative approach to define further morphological classes of retinal ganglion cells has become possible recently. Cell bodies of ganglion cells can be marked by uptake of fluorescent dyes (280,281) or by retrograde transport (76,308), and it is possible to inject such prelabeled cells intracellularly under visual control on the microscope. This approach has established &cells as a separate class (70, 412), specified t-cells projecting to the pulvinar (166,

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195), and shown those ganglion cells projecting to the C-laminas of the LGN, the superior colliculus (47), and the accessory optic nucleus (48, 75) to comprise several morphological classes (318). In the primate retina a comparable correlation of form and function is lacking. However, a similar morphological diversity is expected (317). The small, colorantagonistic, tonic ganglion cells probably have their morphological correlate in PP-cells (292), the midget ganglion cells (300). The concentric, non-color-coded phasic cells very likely correspond to Pa-cells (292), the parasol ganglion cells (300, 314, 413). a-Type ganglion cells have been found in cats, rabbits, mice, rats, oxen, sheep, and several other mammals. Hence they are probably a constant feature of mammalian retinal organization (90, 92, 121, 280, 281, 286, 287). In the rabbit retina, several morphological classes have been described (5-8, 111, 281), and of particular interest here are the DS ganglion cells (6,8) and the fact that no equivalent of the ,& -or PP-system has been found (281). C. StratQication

of Ganglion

Cell Dendrites

It was suggested by Lettvin et al. (193) and later by Famiglietti and Kolb (114) that the level of stratifica-

CELL DELTA

CELL

FIG. 15. Drawings of ganglion cells from flat-mounted cat retinas after physiological recordings and intracellular stainings. Arrows point to axons. &-Cell was recorded as ON-center Y-cell, eccentricity 2.2 mm. P-Cell was recorded as ON-center X-cell, eccentricity 1.8 mm. &Cell was recorded as OFF-center sustained W-cell, eccentricity 2.5 mm. [From Saito (324).] y-Cell was recorded as transient W-cell. [From Stanford (35’7).]


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Sl

a (OFF)

s2

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FIG. 16. Stratification of ganglion cell dendrites in inner plexiform layer of cat retina. ON- and OFF-p-cells occupy 2 diffuse bands. ON- and OFF-a-CdS stratify in 2 narrow bands, G-10 pm apart. ONand OFF-&cells have 2 narrow level s of stratification: 1 is outer and 1 is m ore inner when compared with a-cells (70, 284, 412).

tion of ganglion cell dendrites within the IPL could be correlated with their physiological type. Nelson et al. (267) showed, by intracellular recordings and dye injections, that OFF-Center ganglion cells branch closer to the INL, whereas ON-Center cells keep a stratification level closer to the ganglion cell layer. This result was confirmed, and it became possible to analyze the separate mosaics of ON- and OFF-ganglion cells (284, 400). Figure 16 summarizes what is known from Golgi staining (180, 400), from intracellular recordings (120, 267, 324, 357, 358), and from intracellular staining (70, 76,412) concerning the stratification level of a-, ,&, and a-ganglion cells in the cat retina. The IPL can be subdivided into three sublayers of approximately equal width: lamina a, where OFF-ganglion cells stratify; lamina b, where ON-ganglion cell dendrites branch; and lamina c, which is mainly occupied by rod bipolar cell terminals. The scheme holds at all eccentricities and for all mammalian retinas. However, the relative proportions of the different subdivisions may change. The thickness of lamina c critically depends on whether a retina is rod dominated, similar to that of the cat, or cone dominated, similar to that of the tree shrew (Tupaia) (149). Bistratified ganglion cells seem to be present in all mammalian retinas and probably receive direct input from both the ON- and the OFF-sublaminas. An example of such cells are the ON/OFF-DS ganglion cells of the rabbit retina (6, 8). If amacrine cells were represented in the scheme of Figure 16, then they would also occupy characteristic strata. Dopaminergic amacrine cells in all mammalian retinas have their major stratification level close to the INL in stratum 1 (Sl) (94-96). The two subclasses of cholinergic amacrine cells have stratification levels near those of ON- and OFF-a-Ceh. Their dendrites are found in proximity to a-cell dendrites and are thought to synapse on them (396). Dendrites of the sparsely branched A-20 amacrine cell of Figure 12 would stratify just in between the ON- and OFF-sublaminas (S2 and S3) (412). In the m.onkey retina an uneven distribution of synles across the IPL has been repor ted (183). The num-

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ber of bipolar cell dyads is higher in two bands corresponding to the stratification level of ON- and OFFganglion cells, and a higher density of amacrine synapses was observed in the center of the IPL between the ON- and the OFF-sublaminas. Interestingly, staining for glycine receptors in the cat retina has revealed two bands of high receptor density, which coincide with the level of the ON- and OFF-sublaminas, laminas a and b (154). In contrast, GABA, receptors were found to be concentrated in lamina c where rod bipolar axons terminate; th .e labeling in laminas a and b (149,312) was more diffuse.

D. Ganglion Cell Coverage

Given the diversity of ganglion cell types, it is important to know whether each type completely tiles the retina or, stated physiologically, does a light spot projected at an arbitrary point on the retina always hit all physiological classes of ganglion cell? The answer is important to the concept of parallel information processing in the retina and visual system. If each physiological class provides an homogeneous coverage of the retina, then every spot is analyzed simultaneously with respect to its contrast (ON- and OFF-center cells), color, direction of movement, and other features. Because different ganglion cell classes also project into different visual centers of the brain (195, 399), retinal ganglion cells very specifically act as parallel operating filters that select and distribute visual information (192, 204, 350, 351). Whether a given ganglion cell type covers the retina cannot be determined by physiological recording, because microelectrodes inevitably select for larger cell bodies and axons. Such data are only obtainable when physiological units are anatomically defined and quantitatively stained. @-Cells of many mammalian retinas can be stained with reduced silver methods (282) and, more recently, with different immunocytochemical markers: neurofilaments (go), calcium-binding proteins (319), microtubule-associated proteins (233), acetylcholine receptors (167), and AbEi-antibodies (119). Their dendrites form a network that uniformly covers the retina (Fig. 17A). When the total o-cell population in Figure 17A is subdivided into ON- and OFF-Cells (Fig. 17, B and C), each population has a regular mosaic of cell bodies and uniformly tiles the area with dendritic fields. Closer examination suggests (Fig. 17, D-F) that the dendrites of neighboring cells show territorial behavior when filling the available space (409). This has been indicated by several studies where lesions, made during developmen t, have prod uced cell-free areas, which then became preferential ly in .nervated by the dendrites of the surrounding ganglion cells (103, 196, 290). The dendritic interaction during development must be rather specific, because, as can be seen in Figure 17, ON- or OFF-CdS relate only to their physiologically homologous neighbors. The dendrites of each subclass


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FIG. 17. Analysis of dendritic fields of a-ganglion cells of cat retina. A: drawing of all a-cells in area 1.7 X 1.2 mm of Bodian-stained cat retinal whole mount (eccentricity 4 mm). B: same field as in A, but only ON-a-cells are shown. C: same field as in A, but only OFF-ar-cells are shown. D: solid curves are contours of ON-a-cell dendritic fields shown in B, and dots indicate cell body locations. Dotted lines subdivide area into small territories surrounding every cell body with property that every point in particular territory has shorter distance to its own cell body than to any other. E: coverage of retina with hypothetical circular dendritic fields based on mosaic of ON-a-cells; black areas are not covered if average dendritic field is represented by circles. F: every ON-a-cell dendritic field is substituted by its mirror image with cell body unchanged. Only actual dendritic trees (D) provide effective tiling without leaving holes. [From Wassle et al. (409).]


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18. Dendritic plexus of &ganglion cells in cat retina. Six cells were intracellularly injected with horseradish peroxidase after of their cell bodies by uptake of indoleamines. They represent, at least in center, all ganglion cells of this particular type. Density of appears to remain constant across core of patch where processes of 4 cells intermingle and overlap extensively. Individual dendritic appear to show high degree of local order by interdigitating to fill available space within network. [Adapted from Dacey (70).]

do not react with the other nor with the other ganglion cell classes, the dendrites of which they must grow through during development. It is likely all ganglion cell classes produce an efficient and economical tiling of the retina with their dendritic fields. A class of ganglion cell of the cat retina has recently been identified by the capacity of the cell bodies to accumulate indoleamines (70,412). After prelabeling their cell bodies with a fluorescent indoleamine, they could be injected with Lucifer yellow or HRP, and their dendritic branching pattern was similar to that of 6cells previously described in Golgi-stained retinas by Boycott and Wassle (42). Because most of the cells in small patches were injected, their dendritic overlap could be studied (Fig. 18). Neighboring cells provide a uniform coverage of the retina, and on the average 2.2 dendritic fields overlap at any given point. In the zone of overlap the dendrites of the different cells interdigitate in a regular way such that a uniform interdendritic spacing and density of dendritic processes occurs (70). This, like the a-cell analysis (Fig. 17), indicates specific interactions of homologous dendrites during development. The requirements of a uniform coverage can be used to estimate the possible number of different ganglion cell types within a particular retina. The ON-a-Cells, the OFF-a-cells, and the indoleamine-accumulating ganglion cells are each only Z-4% of the total ganglion cell population; nonetheless, they provide a complete coverage of the retina. Given the densities and dendritic field

sizes of these cells, up to 30 different ganglion cell classes, each comprising -2-4 % of the ganglion cell population, might be present. However, such an estimate critically depends on the dendritic field size. This is exemplified by ,&ganglion cells. The ,&cell population was stained quantitatively by retrograde axonal transport of HRP from the LGN (151). Approximately 50% of all ganglion cells were found to be P-cells, and they compensate for their small dendritic fields by a high retinal density. Hence taking into account the large proportion of ,&cells reduces the number of possible ganglion cell classes in the cat retina to an estimated 15-20 classes. As mentioned, Rodieck and colleagues (47,185) have recently backfilled ganglion cells from various brain nuclei and injected them intracellularly with HRP. They described several morphological types, mostly widefield cells, all of which can be expected to give an independent coverage of the cat retina. Ganglion cells projecting to the accessory optic system [such cells were recently backfilled and injected in the rabbit and rat retina (48,75)] are probably also present in the cat retina and represent a further type of ganglion cell. All this makes it likely that the cat retina and probably any other mammalian retina is covered by up to 20 different classes of ganglion cell. At first sight the primate retina seems to be less complicated than the cat and the rabbit retina, because 80% of all ganglion cells are members of the PP-class (292). Because another 10% were classified as Pa-cells, this leaves “only” 10% for all other ganglion cells. How- ~


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ever, bearing in mind that primates have 4.5 X lo6 ganglion cells (288), that represents 150,000 ganglion cells. This is approximately the total number of ganglion cells in a cat retina (148). Because monkey and cat eyes are of similar dimensions, the remaining 10% of monkey retinal ganglion cells could comprise as many ganglion cell types as are found in the total cat retina. Indeed, there is growing modern evidence for monkey ganglion cell types other than Pcx- and PP-cells (288, 292, 314). The P@-cells at 5 mm eccentricity in temporal retina have dendritic fields of -40 pm diameter (413). Their density is 2,300/mm2 (406,407), and the resulting coverage factor is 2.9. Given that ON- and OFF-Cells as well as red and green tonic cells are the physiological correlates of PP-cells, this coverage of 2.9 appears low. It seems as if ON- and OFF-tonic cells provide an uniform coverage without allowing for the different chromatic signals of the individual cells. This agrees with what we said at the beginning of this review, that the chromatic signal probably came into the primate visual system late in evolution and the coverage of PP-cells was not affected. However, it is notable that PP-cells have rather irregular dendritic fields (36,292,300,413). This may reflect aspects of their chromatic connections. At 5 mm eccentricity, midget bipolar cells still provide contacts with individual cone pedicles and hence transfer a chromatic signal into the IPL. A PP-cell, with only red cone input to the receptive field center, has to select red midget bipolar cells for contact. Hence it is very likely that the detail of its dendritic tree reflects the requirement to come into register with specific midget bipolar axon terminals. The irregular shape of PP-cell dendritic fields at eccentricities where the cone density is low may thus represent, at least to some extent, the array of red or green cones. Such a selectivity for particular bipolar cells might also explain the low coverage of PP-cells. As illustrated in Figure 170 by the Dirichlet domains, they might precisely subdivide the terminal plane of midget bipolar cells without superfluous overlap. E. Ganglion

Cell Microcircuitry

It is still not understood what determines that a ganglion cell shall respond to a light stimulus in a brisk or sluggish manner, with transient or sustained characteristics, or with linearity or nonlinearity. One possibility is that the geometry of the dendritic tree defines the physiological behavior (168-170). Application of cable theory to different ganglion cell morphologies showed, for instance, that the nonlinearity of Y-cells can be explained by isolated compartments within their dendritic field. However, recent measurements of the membrane resistance of ganglion cell dendrites in the mudpuppy retina (239) have shown that resistance to be much higher than so far assumed. It is possible, therefore, that dendritic fields may be practically isopotential. The physiological diversity of ganglion cells might not be due to the properties of the dendrites but might

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result from differing synaptic inputs. ,&Cells receive 70% of their input synapses from bipolar cells and 30% of their input from amacrine cells, whereas a-cells receive 30% of the synaptic input from bipolar and 70% from amacrine cells (118). Because, in general, amacrine cells have more phasic responses than bipolar cells (99, 240, 241, 416), this might explain why Y-cells respond transiently to light stimulation. It has been argued that ON- and OFF- or X- and Y-cells have a transmitter selectivity (150): X-cells should get their excitatory light-driven input through excitatory amino acids only and Y-cells should get it only by the action of acetylcholine. y-Aminobutyric acid was supposed to act as the inhibitory transmitter in the ON-pathway and glycine only in the OFF-pathway. However, these claims have not been confirmed by others recording either from the intact retina (31, 33, 340) or from dissociated retinal ganglion cells (202, 203, 377). All ganglion cells dissociated from the rat retina, which almost certainly can be generalized to other mammalian ganglion cells, have receptors in their membranes for EAAs (4, 163), acetylcholine (202), GABA, and glytine (377). Recently two other possibilities have been considered to generate sustained or transient behavior. In recordings from ganglion cells in retinal slices of tiger salamanders, sustained components of the light response were caused by N-methyl-D-aspartate-type receptors, whereas transient responses were mediated through a kainate-type receptor (245). Recordings from isolated ganglion cells of the cat retina suggest that voltage-dependent channels in a- and ,&cell membranes might be different, with the gating mechanism of a-cells being faster (A. Kaneko, personal communication). This shows that discussions of the structure-function relationships of retinal ganglion cells is rapidly approaching the molecular level. Further progress can be expected when specific antibodies against these channel proteins become available to study their distribution. It is increasingly certain that all these factors, the dendritic branching pattern, the synaptic input, the ligandgated channels, and also the voltage-gated channels, are the basis of functional diversity of ganglion cells. Probably no one factor determines the nature of the responsiveness of a ganglion cell.

VIII.

GANGLION

CELL

FUNCTION

A. Spatial Resolution With the exception of midget bipolar cells in the primate retina, cone bipolar cells are connected to several cones and occur in lower density than the receptors. This integration of cone information causes a loss of spatial resolution. The same holds for ganglion cells; they integrate the light signal over the whole extent of their dendritic field. The dendritic tree defines the receptive fiel d ten .ter and as “the sampli ng aperture,” sets the limits of r es0 lving power. The spacing between


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l monkey: CROOK et al., 1988 : PEICHL ii WiiSSLE, 0 cat

;.z 0

F 3z FIG. 1% Limits of Spatial resolution set by retinal ganglion cells. A: spatial resolution of ganglion cells to gratings moving slowly across their receptive fields. Abscissa, diameters of receptive field centers (RFC). Ordinate, limits of spatial resolution of cells, which is smallest spatial wavelength (X) that could be resolved. [Data for monkeys from Crook et al. (66); data for cats from Peichl and Wassle (283).] B: Nyquist limit of P-cell mosaic in cat retina. ,&Cell in center is surrounded by 6 neighbors, of which only cell bodies are indicated by black circles. Given an intercell spacing of a, such a mosaic could resolve a grating of spatial wavelength X = fia = 1.73a. When such a grating is inserted, stripes coincide with rows of ,&cell bodies. Receptive field center of ,&cell has diameter of 3a and, according to results shown in A, can resolve gratings of X = 0.56 X 3a = 1.6%

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neighboring ganglion cells defines, as “the sampling distance,” which spatial frequency is unambiguously available within the visual system, i.e., the Nyquist limit (17, 348, 356). The spatial resolution of individual ganglion cells, measured by moving gratings of varied spatial frequency over the receptive field, is shown in Figure 19A. Both in the monkey and in the cat retina a simple correlation between receptive field center diameter (D) and the resolution limit (A) holds, X = 0.560 (58, 66,283). The Nyquist limit, assuming hexagonal packing of ganglion cells with intercell spacing (a), is defined by X = @a = 1.73a. Figure 19B summarizes the results for oN+ganglion cells of the cat retina. The ,&cell in the center is

II 140

LIMIT: = 1.73 -a

surrounded by six neighboring cells in a hexagonal mosaic with intercell spacing (a). The dendritic field of ,8cells is delimited by the immediate neighbors, hence the diameter is Za, twice the intercell spacing. The receptive field center diameters of ,&ganglion cells are ml.5 times the dendritic field diameters. This was calculated by comparing receptive field center dimensions, given in Peichl and Wassle (283), with dendritic field dimensions of Lucifer yellow-injected ,&cells taken from Dann et al. (76). The circle in Figure 19B indicates the receptive field center diameter of the P-cell, which is 3a. Consequently the ,&cell has a resolution limit of X = 0.56 X 3a = 1.68a. The grating projected onto Figure 19B is just resolved. The Nyquist limit of the ,&-cell array, X =


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HEINZ WASSLE AND BRIAN B. BOYCOTT

@a = 1.73a, is in close agreement; hence sampling aperture and sampling distance are matched. The ,&cell in the center of Figure 19B together with its immediate neighbors represents the “resolution module” of retinal ganglion cells. Because the resolution limit depends both on the spacing and the dendritic field size, only cells with high density and small dendritic fields are able to provide high visual acuity. It can now be asked which type of ganglion cell defines the visual acuity of primates. This is ~1 min of arc, corresponding to 3.3 pm on the retina. The sampling density of all ganglion cells in the macaque monkey foveal center is 668,25O/mm’, of these 10% are Pa-cells, which have to be separated into ON- and OFF-center cells, resulting in a density of 33,41Z/mm? From this a Nyquist limit of 10 ,rcrncan be calculated. This is a factor of 3 above the visual acuity measurements. It follows that midget ganglion cells (PO-cells of fovea) provide the limits of spatial resolution (237,238,338), which, in this case, is set by the cone mosaic (see sect. III).

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way and the Pa-cell pathway as an unique contrast detection system (204). In the cat retina another aspect of stimulus detection, which depends on nonlinear summation within the receptive field of Y-cells, has to be considered. When a stimulus with a fine texture is moved over the receptive field of a Y-cell, the cell will respond with a raised firing rate, because the pixels of the pattern are summated in a nonlinear manner (57, 100, 101, 142). The nonlinear subunits within the Y-cell receptive field resolve the pattern and cause the cell to fire (60). In X-cells such a textured pattern, where the individual pixels are beyond the cells’ resolution, will not raise the discharge rate. Hence Y-cells are superior to X-cells in stimulus detection. Because Y-cells have, in addition, shorter response latencies (32) and faster conducting axons (56) than all other ganglion cells, the first signal arriving in the brain from the retina is through the Y-cell channel. This signal could trigger eye movements and direct attention to the stimulus to analyze further detail through the X-cell system.

B. Stimulus Detection

In the preceding section, ganglion cells were evaluated for their capacity to resolve fine detail; small dendritic and receptive fields were found to be a necessary requirement. However, other visual tasks will be performed more efficiently if ganglion cells have large receptive fields (18). Large receptive fields permit higher sensitivity. Fluctuations in the photon distribution as well as spontaneous photoisomerisations and vesicle release at synapses produce noise that reduces the sensitivity of a cell. This noise is Poisson distributed about a mean (n) and with a standard deviation fi, which sets the limits for the detectability of a light signal. Other parameters being equal, the sensitivity of a cell that integrates signals from all photoreceptors in its field depends on the area A of the receptive field. Noise is proportional to 0, and the signal-to-noise ratio therefore improves with fl. Sterling (363) and Sterling et al. (364) have recently applied signal-to-noise considerations to the circuitry of the dark-adapted cat retina and have made predictions from the anatomy as to the efficiency of scotopic vision. In the primate retina phasic non-color-coded cells (Pcy) have large receptive fields and high-contrast sensitivity. Tonic color-coded cells (Pp) have small receptive fields and low-contrast sensitivity (162). The behavioral contrast sensitivity of monkeys and humans is several times higher than that of PP-cells (82, 237, 238, 347), which suggests it might be based on perception mediated by Pa-cells. Their high-contrast sensitivity is probably important for pattern perception at low contrasts and at low spatial frequencies. Signals from Ppcells, however, might be necessary to account for the dynamic range of the contrast sensitivity; they are crucial to explain the high-frequency cutoff and the visual acuity (238,399). It is therefore an oversimplification to consider the PP-cell pathway as only a chromatic path-

C. Ganglion Cell Density and Cortical MagniJication Factor

In the primate, the mapping of the visual field onto the striate cortex (VI) is nonuniform: the representation of the fovea occupies a large area, whereas the peripheral visual field claims only a small portion of the visual cortex (65, 74, 85,145,288,321,337,374,382,388). The cortical magnification factor (M) quantifies this distorted projection (344,345) and indicates the amount of cortex associated with each degree of visual field. The area1 magnification (M2 = mm2 cortex/degree2 visual field) of the fovea is greater by a factor of >l,OOO when compared with that of the peripheral visual field. It has been controversial until recently (for reviews see Refs. 299,380) as to whether the cortical magnification factor simply represents the variation of retinal ganglion cell density (D), with M2 being proportional to D (65a, 91,322,336,337), or whether an enhanced representation of the central visual field occurs in the geniculate and/or the visual cortex (209, 257,288, 388). There were two major problems in quantifying the ganglion cell density gradient of the primate retina. First, the population of displaced amacrine cells had to be estimated (406). Second, in the fovea, the spatial offset between ganglion cells and cone outer segments due to the cone fibers (Henle fibers) had to be allowed for to estimate the sampling density of ganglion cells (244, 289, 336, 406, 407). Ganglion cell axons innervate relay cells in the LGN where they remain separated in different layers corresponding to the eye of origin (209). In the visual cortex (VI), information from the nasal retina of one eye and the temporal retina of the other eye are combined. If it is assumed that there is equal cortical space per ganglion cell, then the cortical representation should follow the retinal ganglion cell density. This has been shown to be the case, and both the magnification


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factor and the ganglion cell density change by a factor of l,OOO-4,000 between fovea1 and peripheral visual fields (406, 407). In the cat visual system there is also a close correspondence between retinal ganglion cell density and the decrease of cortical magnification with eccentricity. In the central area of the cat retina the sampling density of ON-@-Cells is 2,000-3,000 cells/mm2 (400), and the cortical magnification factor is l-4 mm2/degree2 (333, 387). In the monkey fovea the sampling density of ON-Pp-Cells is 267,000 cells/mm2 (406,407), and the cortical magnification factor is 100-300 mm2/degree2 (382). Both the ganglion cell density and the area1 magnification factor are 100 times those of the cat. It seems that the rules of mapping the retina onto the visual cortex are similar in both cats and monkeys and that the ganglion cell density defines the visual map in the cortex. Distorted representations in the cortex are also found for other sensory modalities; the “homunculus” of the somatotopic map on the human cortex is a wellknown example (285). The simple rule, that the central representation follows the peripheral receptor or neural density, may be applicable not only to the visual system but to other sensory modalities as well (205, 206). We are grateful to I. Odenthal for typing this manuscript and to F. Boij for making the drawings. We thank P. Martin, L. Peichl, and J. Riihrenbeck for many discussions and helpful comments.

REFERENCES 1. ADAMS, C. K., J. M. PEREZ, AND M. N. HAWTHORNE. Rod and cone densities in the rhesus monkey. Invest. Ophthalmol. VisuaZ Sci. 13: 885-888, 1974. 2. AGARDH, E., B. EHINGER, AND J.-Y. WU. GABA and GADlike immunoreactivity in the primate retina. Histochemistry 66: 485490,198’7. 3. AHNELT, P. K., H. KOLB, AND R. PFLUG. Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina. J. Comp. NeuroZ. 255: 18-34,1987. 4. AIZENMAN, E., M. P. FROSCH, AND S. A. LIPTON. Responses mediated by excitatory amino acid receptors in solitary retinal ganglion cells from rat. J. Physiol. Lond. 396: 75-91, 1988. 5. AMTHOR, F. R., C. W. OYSTER, AND E. S. TAKAHASHI. Quantitative morphology of rabbit retinal ganglion cells. Proc. R. Sot. Lond. B BioZ. Sci. 217: 341-355, 1983. 6. AMTHOR, F. R., C. W. OYSTER, AND E. S. TAKAHASHI. Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Res. 198: 187-190, 1984. 7. AMTHOR, F. R., E. S. TAKAHASHI, AND C. W. OYSTER. Morphologies of rabbit retinal ganglion cells with concentric receptive fields. J. Comp. Neural. 280: 72-96, 1989. 8. AMTHOR, F. R., E. S. TAKAHASHI, AND C. W. OYSTER. Morphologies of rabbit retinal ganglion cells with complex receptive fields. J. Comp. Neural. 280: 97-121, 1989. 9. ARIEL, M., AND A. R. ADOLPH. Neurotransmitter inputs to directionally sensitive turtle retinal ganglion cells. J. Neurophysiol. 54: 1123-1143, 1985. 10. ARIEL, M., AND N. W. DAW. Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. J. Physiol. Lond.

324:161-185,1982. 11. ARKIN, M. S., AND R. F. MILLER. Bipolar origin of synaptic inputs to sustained OFF-ganglion cells in the mudpuppy retina. J. Neurophysiol. 60: 1122-1142,1988. 12. ARKIN, M. S., AND R. F. MILLER. Synaptic inputs and morphol-

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13. 14.

15.

ogy of sustained ON-ganglion cells in the mudpuppy retina. J. Neurophysiol. 60: 1143-1159,1988. ATTWELL, D. Ion channels and signal processing in the outer retina. Q. J. Exp. Physiol. 71: 497-536, 1986. ATTWELL, D., P. MOBBS, M. TESSIER LAVIGNE, AND M. WILSON. Neurotransmitter induced currents in retinal bipolar cells of the axolotl, Ambystoma mexicanum. J PhysioZ. Lond. 387: 125-161,1987. BADER, C. R., D. BERTRAND, AND E. A. SCHWARTZ. Voltageactivated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J. Physiol. Lond.

331:253-284,1982. 16. BARLOW, H. B. Summation

and inhibition in the frog’s retina. J. Lond. 119: 69-88, 1953. 17. BARLOW, H. B. The physical limits of visual discrimination. In: PhotophysioLogy, edited by A. C. Giese. New York: Academic, 1964, vol. 2, p. 163-202. 18. BARLOW, H. B. Retinal and central factors in human vision limited by noise. In: Vertebrate Photoreception, edited by H. B. Barlow and P. Fatt. London: Academic, 1977, p. 337-358. 19. BARLOW, H. B., R. M. HILL, AND W. R. LEVICK. Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J. Physiol Lond. 173: 377-407, 1964. 20. BARLOW, H. B., AND W. R. LEVICK. The mechanism of directionally selective units in rabbit’s retina. J. Physiob Land. 178: Physiol.

477-504,1965. 21. BARNES, S., of tiger

AND

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Functional architecture of the retina: development and disease.

Mammalian cadherins DCHS1-FAT4 affect functional cerebral architecture.

Sox2-Deficient Müller Glia Disrupt the Structural and Functional Maturation of the Mammalian Retina.

Determinants of mammalian nucleolar architecture.

Glia-neuron interactions in the mammalian retina.

3D genome architecture in the mammalian nucleus.

The mosaic of nerve cells in the mammalian retina.

Molecular architecture of mammalian nitric oxide synthases.

Architecture of the large subunit of the mammalian mitochondrial ribosome.

Functional architecture of the CFTR chloride channel.

Characterizing spatial distributions of astrocytes in the mammalian retina.

Species-specific wiring for direction selectivity in the mammalian retina.

Visualizing the functional architecture of the endocytic machinery.

Heritability of the network architecture of intrinsic brain functional connectivity.

Functional architecture of MFS D-glucose transporters.

Functional properties of ganglion cells of the rhesus monkey retina.

A unifying theory for the functional architecture of endothermic thermoregulation.

Functional architecture of the Reb1-Ter complex of Schizosaccharomyces pombe.

Three distinct blue-green color pathways in a mammalian retina.

Modular extracellular sensor architecture for engineering mammalian cell-based devices.

Global chromatin architecture defines functional cancer hierarchies.

The RNA binding protein RBPMS is a selective marker of ganglion cells in the mammalian retina.

Review: Zinc's functional significance in the vertebrate retina.

Synaptic Vesicle Exocytosis at the Dendritic Lobules of an Inhibitory Interneuron in the Mammalian Retina.