midget pathways of the primate retina underlie resolution and red green color opponency

Midget pathways of the primate retina underlie resolution and red green color opponencyHelga Kolb, PhDProfessor Emeritus of Ophthalmolgy & Visual Sciences, The University of Utah School of Medicine.

[email protected]

Corresponding author.

Created: May 24, 2007. Last Update: April 4, 2012.

1 General characteristicsThe specialized cone pathways of the central fovea of human and monkey retinas have the least convergence and the greatest resolution capabilities of the visual system. This is accomplished by making the connections as “private” as possible and narrowing them to a one to one relationship in the so-called midget pathways. Figure 1 shows an older drawing from Polyak’s book (1) that shows the very narrowest field bipolars and ganglion cells of the fovea.

The midget pathways consist of midget bipolar cells and midget ganglion cells, the latter of which project to individual parvocellular layer cells of the lateral geniculate nucleus in the brain. Because of the need for the high acuity midget pathways also to be organized into ON- and OFF-center channels like the diffuse cone pathways for maximization of contrast, it means that every cone of the fovea will have dual midget pathways. The two midget bipolars will be an ON-center type and an OFF-center type and will connect with ON-center and OFF-center midget ganglion cells respectively. Because midget bipolar/ganglion cell circuits are devoted to a single cone, and the individual cones are of different spectral type maximally excited by short (S-cone/blue), medium (M-cone/green) or long (L-cone/red) wavelengths, they must carry sensitivity information about one wavelength. Thus the midget system concerned with the M- and L-cones in particular are considered also to carry L- or M-signals to the brain where further processing takes place to allow us the red and green discriminations of color vision.

The S-cone system is rather different from the M- and L-cone systems from the initial level of the cone itself to its circuitry though the retina and into the brain. We do not consider the S-cone pathway as a midget pathway (see later chapter on S-cone pathways). So this chapter is devoted to the M- and L-midget pathways and as we shall see, they carry both a resolution and a chromatic message through the retina to the brain.

2 Visual acuity starts with cone spacing and midget circuitryVisual acuity is a measure of our ability to discriminate the finest detail: either by discriminating two parallel lines apart (Vernier acuity) or two tiny spots or stars apart (point discrimination). The primate and human visual system is capable of acuity of 1 min of arc or 60 cycles/degree of visual angle. One degree of visual angle is thought to cover approximately 280-300 um of retinal distance (2). The area of the retina where the cone photoreceptors are most closely packed in a more or less hexagonal array, is, of course, the center of the fovea and is about one degree across (Fig. 2). So visual discrimination of 1 min of arc is about the center to center spacing (3 µm) of the cones of the central mosaic in the foveola (Fig. 3).

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If the minimum center to center spacing (a ) is 3 µm for the cones of the fovea, then the grating resolution limit, known as the Nyquist limit, is a √3, about 1 min of arc. One may ask why the grating resolution is not better than 1 min of arc and the size of, or even less than the diameter of each cone, i.e. a or < a . For these narrower gratings, the spatial interference of the packed cones would apparently cause Moire effects, or aliasing, if line separations of less than a √3 are used, as shown below (3) (Fig. 4). These interference patterns, with a repeat length that depends on the angle that the grating makes with the cone mosaic, make it impossible to determine the wavelength of the grating. It turns out that under normal conditions, the optics of the eye do not sharply image gratings of greater than 60 cycles/degree (4). The optical blur of the eye minimizes Moire effects in spatial sampling (Fig. 4).

The image is also blurred by the optics of the eye to project onto about 10 cones (Fig. 4). Lateral shifts of this image can then be compared over these 10 cones and their midget chains of neurons for later computation in the brain. This allows better discrimination (resolution) because of the possibility of imposing antagonism from neighboring cone systems, i.e. surrounds on the pathways and increasing contrast and discrimination between the several midget-single-cone originating pathways (5).

We know that three classes of cone comprise the cone foveal mosaic, but we have long been curious as to how the three different spectral types of cone are arranged in the hexagonal mosaic. The S-cones (blue cones) are fairly easily picked out from the L-cones (red cones) and M-cone (green cones) on some distinguishing morphological features (see chapter on S-cone pathways). In fact the S-cones are seen as the larger profiles disrupting the hexagonal mosaic in the wholemount view of the foveal mosaic of Figure 2 (arrows point to S-cones). In the foveal region of the cone mosaic S-cones form from 8-12% of the cones (6). The very center of the foveal pit is almost devoid of S-cones. So the remainder of the cones are somehow divided into the L- and M-cone populations. In the human fovea, psychophysical measurements have suggested that red cones outnumber green by 2:1 (7). However, direct measurements by microspectrophotometry of all cones in small patches of cones in the fovea of monkeys, has revealed that red and green cones occur in about equal proportion (Fig. 5) (8). Roorda and Williams (9) made direct measurements of spectral sensitivity of foveal cones in the living human eye by a sophisticated technique of adaptive optics to increase spatial resolution. They found that humans varied greatly in their proportions of red cones to green cones: some individuals have almost equal proportions while others have a higher proportion of red cones, to the extreme of 2 red cones to every green cone. The red and green cones lie randomly in the mosaic meaning that clusters of cones of the same spectral type will occur together as illustrated in figure 5 from Mollon and Bowmaker’s paper. An interesting point can be deduced from these findings. It does appear possible then, that a multiheaded midget or diffuse cone bipolar with a small dendritic tree, could contact all the same spectral type of cones in the primate fovea.

3 Cone to midget bipolar cell connectionsPolyak (Fig. 6) had already described two types of midget ganglion cell in the primate retina in 1941 (1). He had studied and drawn ganglion cells from vertical sections of Golgi-stained monkey retina and noticed that the midget ganglion cells in particular (although it is also true of the small and large parasol ganglion cells) had dendrites branching at one of two levels in the IPL: close to the ganglion cell bodies (the area we now know as sublamina b) or in neuropil close to the amacrine cell bodies (the area we now know as sublamina a). He had also drawn and remarked on the fact that midget bipolar cells came in long and short axon varieties to fit the two midget ganglion cell varieties (Fig. 7) (1)).

Midget pathways of the primate retina underlie resolution and red green color opponency

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The important distinction between two types of midget bipolar cell was not made until an electron microscope study was able to show differences in their synaptic contacts with the cone pedicle (10). Thus, invaginating midget bipolar cells (imb) were found to connect with cone pedicles at central elements, invaginating synapses at the cone pedicle ribbons (Fig. 8 and Fig. 9). Flat midget bipolar cells connect to cone pedicles at wide-cleft, basal junctions (fmb), most often on either side of the invaginating dendrite of the imb (Fig. 8 and Fig. 10).

4 Midget ganglion cellsViewing Golgi stained whole-mount primate retinas has been particularly helpful in revealing the differences between the three ganglion cell types that are involved with spatial and color vision: namely the midget ganglion cells, the blue/yellow ganglion cells and the parasol ganglion cells (1, 11, 12). The midget ganglion cells are thought to be high acuity cells that also carry a red or green color specific signal. They project to the parvocellular layers of the lateral geniculate nucleus and are thus called P cells (Fig. 11) (13). Midget ganglion cells come in high branching varieties that are probably OFF-center physiologically and low branching types that are ON-center physiologically. Movie 1 is a through focus series of an ON and OFF midget pair in human retina.

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Movie 1. A focus series of two Golgi-stained P or midget ganglion cells in the human retina.

Figure 11 shows two midget ganglion cells in comparison with a parasol ganglion cell (M cell) of peripheral human retina. The one midget ganglion cell has an 18 μm diameter dendritic tree and the other has a larger dendritic field at 35 μm in diameter. The movie above shows that the midget ganglion cell with the smaller dendritic field comes into focus at a different level from the larger field cell. The former midget ganglion cell branches high in the IPL and so is probably an OFF center type physiologically. The lower branching midget ganglion cell with the larger dendritic tree is probably an ON center type. Why the OFF center type has a smaller dendritic tree compared with ON center type remains a mystery at present but one implication may be that the midget OFF system acuity is higher in acuity than the ON system (14).

The connections between the midget bipolar and the midget ganglion cells have always been thought to be "private", i.e. one to one. Because of the similar size and branching level of the axon terminal of the bipolar cell and the dendritic arbor of the midget ganglion cell in the foveal area particularly, it has been assumed that axon terminal and dendritic field overlap and synapse, with no room for convergence from more than one bipolar axon per ganglion cell. However, the story may be different in the peripheral retina where the midget ganglion cells have larger dendritic fields. Obviously more than one midget bipolar axon could fit the dendritic tree of the receiving peripheral midget ganglion cell as seen in Figure 12.


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http://www.ncbi.nlm.nih.gov/books/n/webvision/ch14midget/bin/Movie1focus.mov

The one to one relationship was positively proven to be the case in the parafoveal area by an electron microscope study and reconstruction of serially sectioned midget ganglion cells and their input midget bipolar cell axons in parafovea, about 2 mm from the foveal pit (Fig 14) (15). More recently we have also performed a serial section electron microscope study of foveal midget bipolar axons and their connections with the dendrites of foveal midget ganglion cells (Fig. 13) (14).

The respective midget bipolar cells are almost solely synaptic upon single midget ganglion cells (Fig. 14), except in the very central fovea where a few midget bipolar synapses are shared with neighboring midget ganglion cells because of the crowding of neurons and neuropil (Fig. 13). Since we know (16) that ganglion cells branching in sublamina a will be OFF center and those branching in sublamina b will be ON center we can be sure that midget ganglion cells branching close to the amacrine cell layer will be OFF center and those branching close to the ganglion cell layer will be ON center. This ON and OFF midget ganglion cell organization in primate has now been shown conclusively by Chichilnisky’s group (17). So it appears that in the foveal region and out to the borders of the central retina (about 4 mm from the fovea center) the midget pathways of the human fovea are organized in the following manner: 1 cone to 2 midget bipolar cells (ON- and OFF-center bipolar types) to 2 midget ganglion cells (ON- and OFF-center ganglion cell types).

What we find more difficult to say is what spectral type of cone is connected in the midget bipolar to midget ganglion cell chain. M- and L-cones are indistinguishable anatomically. Where we can recognize S-cone (blue) pedicles on unusual morphological features (6, 18, 19) (see chapter on S-cone pathways), the M- and L-cones look the same. There is some evidence that M- and L-connected midget bipolar cells have different numbers of synaptic ribbons associated with their axons and therefore different quantities of output sites to their midget ganglion cell in the fovea (20): but which axon terminal/ganglion cell pair is associated with M- or L-cone pathways is still a moot question.

Four to five millimetres beyond the fovea, in near periphery, the midget bipolar cells become 2- and 3-headed, connecting to 2 and 3 cones respectively (1, 12, 21). Midget ganglion cells are found throughout the near and mid peripheral retina (1, 12, 22, 23) and their dendritic trees increase in size but are often composed of several domains of dendrites. The further peripheral it gets, the more domains of dendrites compose the dendritic tree of midget ganglion cells. So it seems likely, that more than one midget bipolar cell will synapse upon each midget ganglion cell, probably each bipolar occupying one of the domains of the dendritic tree.

Serial section electron microscopy and reconstruction of axons and dendrites of midget ganglion cells at the edge of the central area (i.e. 4 mm from the foveal center) and from peripheral retina (12 mm from the foveal center) indicate that the prediction of multiple input from cones to midget bipolar cells, and multiple inputs from midget bipolar cells to midget ganglion cells is correct in peripheral retina (Fig. 15 and Fig. 16). Our estimation (14) is that 3 midget bipolar cells synapse on a single ganglion cell 4 mm from the fovea (Fig. 15) (14). Even more convergence of midget bipolar cells to midget ganglion cells occurs in far peripheral retina where we estimated at least 3 multi-headed midget bipolar cells synapse on a single midget ganglion (Fig. 16).

In the fovea where a single cone connects with its midget bipolar and midget ganglion cell system, the pathway will of necessity be carrying a single color receptive field center. Beyond the fovea where the midget pathway is 2 and 3 channeled and/or many midget bipolars have input, the midget ganglion cell's center may be a mixture of cone color types. Despite the patchy and random nature of the red and green cone mosaic and multiple midget


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bipolar inputs, does the midget ganglion cell retain a dominant commitment to one spectral class of cone and a color opponent center surround organization? This is in fact is what is concluded in both physiological (24-26) and the most recent functional connectivity report from Chichilnisky's group (Fig. 17) (17). Figure 17 shows the results of midget ganglion cell measurements with multielectrode recordings and high resolution stimulation of single cone types included in these ganglion cells' receptive fields. Although both red and green cones input the cell, single spectral type of cone i.e. either red types or green types, dominate the receptive field centers (Fig. 17, white outlined, and white lines).

5 Circuits underlying red and green color opponency in the human retinaMidget ganglion cells of the monkey retina (presumably also of human retina) are known to respond to light with an opponent chromatic organization in their surround (5, 27, 28) (Fig. 18). That is, midget ganglion cells of central retina, when recorded from electrophysiologically, have the smallest receptive fields, and are organized as L-cone ON or OFF center, and M-cone ON or OFF center. Each midget ganglion cell type has a larger surround of the opposite polarity and the opponent color. The surrounds of the midget ganglion cells, as Chichilnisky's group have elegantly shown (17), That the surround is comprised of many red and green cone inputs, suggesting non-specific, but mixed spectral input to surrounds (Fig. 17e-g, black lines and circles).

The parasol varieties of ganglion cells are the non-color opponent, phasic varieties of ganglion cell recorded in the retina (28) and are also called M cells projecting to the lateral geniculate nucleus (13, 28, 29). A smaller field, tonic and not clearly color opponent ganglion cell type is also recorded in the retina and parvocellular layers of the geniculate nucleus (Fig. 18) (5). Whether these are the minority extrafoveal midget ganglion cells that are no longer color specific like some of the cells in the Field et al., study (17) remains to be seen.

The opponent color surrounds recorded in midget ganglion cells (28) provide color and spatial opponency. It appears clear now that all primate cone bipolar types have a center/surround organization (Fig. 19) (17, 30). This includes the midget bipolar cells (Fig. 19) (30). Where does this antagonistic surround organization come from?

The horizontal cells are thought to contribute to the surround response of bipolar cells in submammalian species and particularly in creatures with good color vision. Horizontal cells have been shown to be color opponent in response in fish and turtles for example (31-34). The situation is different in primate retina where color opponency has been difficult to detect in intracellular recordings of monkey horizontal cells (35) despite the anatomical findings on spectrally selective connectivity (35, 36).

However, it has recently been shown by elegant experiments in macaque monkey that red and green cones receive an antagonistic surround response from horizontal cells, presumably HI cells (37). Similarly, primate (blue) S-cones clearly have an opponent yellow surround that appears to come from horizontal cells driven by L- and M-cones according to Packer and co-authors (38). Very recent evidence from the same group (39) indicates quite definitively that horizontal cell feedback can account for surround opponency to red and green midget ganglion cells in primate retina, showing that the midget bipolar cells are already color opponent in nature. There does not appear to be any inner retina (amacrine cell) input to organize surrounds in midget bipolar cells and midget ganglion cells. The possibility exists that some large field diffuse cone bipolar types that are not spectrally opponent, and have surrounds consistently larger than midget bipolar cells, could involve an amacrine cell content (30, 40).


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We believe that L- and M-midget ganglion cell responses are organized in the manner shown in Figure 20. An L-cone would contact two L-cone midget bipolars and through them, two L-cone midget ganglion cells. For example, an L-cone ON-center midget bipolar would contact a single L-cone at invaginating synapses in the OPL, and a single L-cone ON-center midget ganglion cell in sublamina b of the IPL. The same L-cone would also be contacted by a single OFF-center midget bipolar at basal junctions, and the bipolar would, in turn, contact a single OFF-center midget ganglion cell in sublamina a of the the IPL (Fig. 20, left). Thus L-cone ON- and L-cone OFF-center receptive field ganglion cell types are generated (red + center and orange - center, Fig. 20, left). M-cones would be connected in a similar manner to two midget bipolars (ON and OFF types) and two midget ganglion cells which would also be ON and OFF-center receptive field types (dark green + center and light green - center, Fig. 20, right).

All of the three types of horizontal cell, HI, HII and HIII could make M-cone surrounds to L-cone center bipolars, and L-cone surrounds to M-cone center bipolar cells. However the HII cell may be more involved with spectrally antagonistic fields in the blue/yellow bipolar cell pathways (see Webvision: S-Potentials and Horizontal Cells).

6 Magnocellular and blue/yellow ganglion cellsThe large field parasol cells of the primate retina are thought to convey achromatic information concerning low spatial acuity, movement and luminance messages (41, 42). Parasol cells come in ON- and OFF-center varieties like the midget ganglion cells and project to the magnocellular layers of the lateral geniculate nucleus (Fig. 21): hence they are also called M cells (13, 43). Parasol ganglion cells also have a surround mechanism to their receptive field physiology, that, like the midget ganglion cells, is thought to originate mainly in the outer plexiform layer from a horizontal cell feedback mechanism (44). The blue yellow ganglion cells (Fig. 21) are a bistratified type and thought to be driven by blue-specific bipolar cells, and other midget or diffuse types to give them their yellow response (11). They project to a special layer of the geniculate nucleus called the koniocellular layer or K layer (45, 46) (Fig. 20). We shall deal with the short wavelength sensitive system in another chapter (Webvision: S-cone pathways) and so will say little more about these ganglion cells here.

About the AuthorsThe biosketch for Helga Kolb can be found in the About the Editors section of Webvision.

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Figure 1. Polyak’s drawing of bipolar and ganglion cells in the foveal slope of the monkey retina. The illustration is taken from

Polyak, 1941 (1).


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Figure 2. Tangential section through the human fovea. The larger cones (arrows) are blue cones. The illustration is taken from

Ahnelt et al., 1987 (6).


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Figure 3. Human foveal cone mosaic. Visual discrimination of 1 min of arc is about the center to center spacing (3 μm) of the

cones of the central mosaic in the foveola. The illustration is from Wässle and Boycott, 1991 (3).


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Figure 4. The minimum center to center spacing (a ) is 3 μm for the cones of the fovea. This determines the Nyquist spatial

resolution limit, a√3, approximately 1 min of arc. If the grating wavelength (λ) is less than this, Moire patterns (B and C )

result which vary depending of the angle of the mosaic to the grating. Thus the grating can’t be uniquely resolved. The

illustration is from Wässle and Boycott, 1991 (3).


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Figure 5. Absorbance spectra of three cone types as measured in foveal patches of cones in rhesus monkey. The spectral

composition of these cone patches are shown. The illustration is from Mollon and Bowmaker, 1992 (8).


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Figure 6. Stephen L. Polyak (1889-1955) is a major authority on the anatomy and neural organization of the primate eye.


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Figure 7. Drawing of Golgi-stained midget bipolar cells (h) in the monkey retina by Polyak, 1941 (1).

Figure 8. Schematic drawing of a cone pedicle ribbon triad to show the differences in synaptic contacts of invaginating midget

and flat midget bipolar cell dendrites.


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Figure 9. EM of a Golgi stained invaginating midget bipolar cell in the monkey retina. OPL, outer plexiform layer.


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Figure 10. EM of a Golgi-stained flat midget bipolar cell in the monkey retina. OPL, outer plexiform layer. The illustration is

from Kolb, 1970 (10).


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Figure 11.Golgi staining of parasol (M) and midget (P) ganglion cells in the human retina. Scale bar 10 μm for all images. The

illustration is from Kolb, Lindberg and Fisher, 1992 (12)


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Figure 12. Midget bipolar cells (imb, fmb) have larger axon terminals at greater distances from the fovea (retinal eccentricity of

4.5mm as compared to 12 mm). Midget ganglion cells (MGC) have larger dendritic fields (here seen at 8 mm) as they increase

in eccentricity..


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Figure 13. 3-D reconstruction in human fovea taken from serial electron micrographs of a group of neighboring midget bipolar

cells and their post-synaptic midget ganglion cells..


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Figure 14. 3-D reconstruction taken from serial electron micrographs of a flat and an invaginating midget bipolar cell and their

respective midget ganglion cells at 2mm from the foveal center in human retina..


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Figure 15. 3-D reconstruction taken from serial electron micrographs of a single midget ganglion cell (ON MGC) at 4 mm

eccentricity from the foveal center in macaque retina. Three midget bipolar cells (imb1, imb2, imb3) synapse upon the midget

ganglion cell, each in contact with a single cone. Thus 3 cones input to this midget ganglion cell.


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Figure 16. 3-D reconstruction taken from serial electron micrographs of a peripheral midget ganglion cell (ON MGC). Three

domains of its dendrites receive from three midget bipolar cells (imb1, imb2, imb3). As each midget bipolar cell is likely to be

three-headed at this eccentricity, it is likely that 9 cones are connected to this ganglion cell.


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Figure 17. The cone wiring pattern of peripheral midget ganglion cells in macaque monkey retina. a) to c) Functional mapping

of cones by ON and OFF midget ganglion cell centers. Spectral composition is mainly a mixture of red and green cones. The

white circles indicate central cone input. Note in b) and c) a blue cone provides input. In the surrounds of such midget ganglion

cell, e) to g) (black circles), many red and green cones have input, suggesting non-specific, but mixed spectral input to

surrounds. The illustration is from Field et al, 2010, including many contributors from the Chichilnisky group (17).


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Figure 18. Color-opponent units as recorded in monkey retina. The illustration is from Gouras, 1968 (28).


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Figure 19. Center-surround receptive field structure of monkey bipolar cells. (A) Bipolar cell hyperpolarized to a small 150 μm

diameter spot centered on the receptive field. (B) Cell depolarized to an annulus (inner diameter 150 μm; outer diameter 1200

μm), Stimulus wave-form is shown below the traces in A and B. (C) Plot of the center and surround Gaussians, giving the

center (43 μm) and surround (437 μm ) mean receptive field diameters. The illustration is from Dacey et al., 2000 (30).


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Figure 20. Summary diagram of midget pathways through the primate retina with color opponent centers and surrounds (red/

green) and ON (+) or OFF(-) centers and surrounds.


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Figure 21. Diagram of the projections of primate ganglion cells to the lateral geniculate nucleus an the superior colliculus. The

illustration B/Y above is from Dacey and Lee, 1994 (11). The LGN illustration is from Shapley and Perry, 1986 (13).


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midget pathways of the primate retina underlie resolution and red green color opponency

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