Barry B. Lee

Horizontal cells of the primate retina : cone specificity without spectral opponency

The chromatic dimensions of human color vision have a neural basis in the retina. Ganglion cells, the output neurons of the retina, exhibit spectral opponency; they are excited by some wavelengths and inhibited by others. The hypothesis that the opponent circuitry emerges from selective connections between horizontal cell interneurons and cone photoreceptors sensitive to long, middle, and short wavelengths (L-, M-, and S-cones) was tested by physiologically and anatomically characterizing cone connections of horizontal cell mosaics in macaque monkeys. H1 horizontal cells received input only from L- and M-cones, whereas H2 horizontal cells received a strong input from S-cones and a weaker input from L- and M-cones. All cone inputs were the same sign, and both horizontal cell types lacked opponency. Despite cone type selectivity, the horizontal cell cannot be the locus of an opponent transformation in primates, including humans.

Receptive field structure in the primate retina

This review summarizes recent work relevant to receptive field structure of cells of the parvocellular (PC) and (MC) magnocellular pathways in the primate. In the PC-pathway, recent data suggest that different color- and cone-opponent ganglion cells make up specific anatomical classes with specific cone connectivities and bipolar cell input. For example, blue-on ganglion cells have been identified anatomically as the small bistratified ganglion cell class. For the midget ganglion cells, which appear to be red-green opponent, there seems to be only one mosaic for red and green on-center and one for red and green off-center cells. This mixture of cell type within a retinal cell mosaic is unusual, as is the fact that dendritic trees of neighboring midget cells do not overlap. Physiologically, all PC-cells lack a contrast gain control mechanism and show a high degree of spatial and temporal linearity of their responses. In the magnocellular pathway, on- and off-center cells, corresponding to parasol cells with dendritic trees ramifying in the inner and outer sublaminae of the inner plexiform layer, show properties familiar from studies of cat ganglion cells, e.g. a contrast gain control is present. However, a chromatic input to the receptive field surround gives their responses an additional order of complexity.

Responses to pulses and sinusoids in macaque ganglion cells.

The goal of the study was to compare pulse responses with sinusoidal temporal responsivity. The response of macaque ganglion cells was measured to brief luminance and chromatic pulses and to luminance or chromatic sinusoidal modulation. To make both positive and negative lobes of the pulse response visible, responses to pulses of opposite polarity were combined to yield a linearized pulse response. Tests of superposition were used to evaluate the linearized pulse response to different combinations of pulse duration and Weber contrast. A prediction of the pulse response was derived using sinusoidal responsivity functions and Fourier synthesis. For ganglion cells of the parvocellular (PC) pathway, shape and absolute amplitude of linearized pulse responses corresponded well to the predicted responses over a range of pulse durations at 0.5 and 1.0 Weber contrast for both luminance and chromatic modulation. For ganglion cells of the magnocellular (MC) pathway, shape and amplitude of the linearized pulse responses and the predicted responses corresponded when the contrast-duration product was low. This correspondence held for luminance modulation over a thousand-fold range of retinal illuminance. For contrast-duration combinations that produced a more vigorous response, over 100 imp/sec, the linearized pulse responses of MC-pathway cells became larger and time-advanced relative to the linear prediction until saturation became apparent. Incorporation of high Michelson contrast responses in the Fourier synthesis captured the timing but not the amplitude of the linearized pulse response. The data suggest that a mechanism similar to a contrast gain control acts upon MC- but not PC-pathway-cells. The data confirm that use of linear modelling to describe temporal behaviour of retinal ganglion cells is appropriate for small signals.

From Pigments to Perception

Peter H. Schiller Department of Brain and Cognitive Sciences Massachusetts Institute of Technology Cambridge, Massachusetts To better understand the functions of the color-opponent and broadband channels that originate in the primate retina, we examined the visual capacities of monkeys following their selective disruption. Color vision, fine but not coarse form vision and stereopsis are severely impaired in the absence of the color-opponent channel whereas motion and flicker perception are impaired at high but not low temporal frequencies in the absence of the broad-band channel. Much as the rods and cones of the retina can be thought of as extending the range of vision in the intensity domain, we propose that the color-opponent channel extends visual capacities in the spatial and wavelength domains whereas the broad-band channel extends them in the temporal domain.

Rod inputs to macaque ganglion cells

The strength of rod inputs to ganglion cells was assessed in the macaque retina at retinal positions within 3-15 deg eccentricity. The experimental paradigm used temporally modulated heterochromatic lights whose relative phase was varied. This paradigm provided a sensitive test to detect rod input. In parvocellular (PC) pathway cells, the gain of the cone-driven signal decreased with decrease in luminance. At 2 td a weak rod response, of a few impulses per second for 100% rod modulation, was revealed in about 60% of cells. For blue-on cells, the cone-driven response also decreased with retinal illuminance, but no rod response could be found. In magnocellular (MC) pathway cells, rod input was much more apparent. Responses became rod dominated at and below 20 td; we cannot exclude rod intrusion at higher retinal illuminances. Responsivity was maintained even at low retinal illuminances. Temporal-frequency dependent rod-cone interactions were observed in MC-pathway cells. Rod responses were of longer latency than cone responses, but there was no evidence of any difference in rod latency between parvocellular and magnocellular pathways.

Responses of macaque ganglion cells and human observers to compound periodic waveforms

We measured responses of macaque retinal ganglion cells to different periodic waveforms (sinusoidal, square, rapid-on and rapid-off sawtooth waveforms) for both luminance and equiluminant chromatic modulation. We analyzed the responses with a peak-to-trough detector. At low frequencies, on-center and off-center magnocellular (MC-) pathway cells showed a ten-fold higher responsivity to the rapid-on and rapid-off sawtooth respectively. Red-on (+L-M) and green-on (+M-L) parvocellular (PC-) pathway cells showed a four-fold greater responsivity to rapid red-on and rapid green-on equiluminant chromatic sawtooth waveforms respectively. At an equivalent retinal eccentricity, we measured psychophysical thresholds for luminance stimuli and chromatic stimuli. We concluded that luminance sawtooth sensitivities from psychophysics are consistent with selective detection through MC-pathway on- and off-center channels in the visual system. The differences between the compound periodic waveforms seen in the PC-pathway cell data did not occur in the psychophysics. In a second analysis, cell responses to sinusoidal modulation were used to predict the linear response to square-wave and sawtooth waveforms. PC-pathway cells showed linear temporal behavior over a wide range of contrasts, but MC-pathway cells displayed linear behavior only for low-contrast luminance modulation. Using these linear fits, we implemented a model incorporating central low-pass filtering in the MC- and PC-pathways before the peak-to-trough detector. This model captured better the time scale and relative sensitivity to periodic waveforms found in the psychophysical data.

Chromatic sensitivity of ganglion cells in the peripheral primate retina.

Visual abilities change over the visual field. For example, our ability to detect movement is better in peripheral vision than in foveal vision, but colour discrimination is markedly worse. The deterioration of colour vision has been attributed to reduced colour specificity in cells of the midget, parvocellular (PC) visual pathway in the peripheral retina. We have measured the colour specificity (red–green chromatic modulation sensitivity) of PC cells at eccentricities between 20 and 50 degrees in the macaque retina. Here we show that most peripheral PC cells have red–green modulation sensitivity close to that of foveal PC cells. This result is incompatible with the view that PC pathway cells in peripheral retina make indiscriminate connections (‘random wiring’) with retinal circuits devoted to different spectral types of cone photoreceptors. We show that selective cone connections can be maintained by dendritic field anisotropy, consistent with the morphology of PC cell dendritic fields in peripheral retina. Our results also imply that postretinal mechanisms contribute to the psychophysically demonstrated deterioration of colour discrimination in the peripheral visual field.

Receptive fields of primate retinal ganglion cells studied with a novel technique

We have reinvestigated receptive-field structure of ganglion cells of the macaque parafovea using counterphase modulation of a bipartite field. Receptive fields were mapped with luminance, chromatic, and cone-isolating stimuli. Center sizes of middle (M) and long (L) wavelength cone opponent cells of the parvocellular (PC) pathway were consistent with previous estimates (Gaussian radii of 2-4 min of arc, corresponding to center diameters of 6-12 min of arc). We calculate that a large factor of the enlargement relative to cone radius could be blur due to the eyes natural optics. Maps were consistent with cone selectivity in surround mechanisms, which had radii of 5-8 min of arc. For magnocellular (MC) cells, center size estimates were also consistent with grating measurements from the literature (also Gaussian radii of 2-4 min of arc). The surround mechanism contributing the MC-cell frequency-doubled response to chromatic modulation appears to possess a subunit structure, and we speculate it derives from nonlinear summation of signals from M,L-cone opponent subunits, such as midget bipolar cells.

Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus

We studied the anatomical substrates of spatial vision in a New World monkey, the marmoset Callithrix jacchus. This species has good visual acuity and a foveal specialization which is qualitatively similar to that of humans and other Old World primates. We measured the spatial density of retinal ganglion cells and photoreceptors, and calculated the relative numbers of these cell populations. We find that ganglion cells outnumber photoreceptors by between 2.4:1 and 4.2:1 in the fovea. The peak sampling density of ganglion cells is close to 550,000 cells/mm2. This value falls by almost 1000-fold between the fovea and peripheral retina; a value which approaches recent estimates of the centroperipheral ganglion cell gradient for human and macaque monkey retina and primary visual cortex. The marmoset shows a sex-linked polymorphism of color vision: all male and some female marmosets are dichromats. Six of the retinas used in the present study came from animals whose chromatic phenotype was identified in electrophysiological experiments and confirmed by polymerase chain reaction (PCR) amplification of cone opsin encoding genes. One animal was a trichromat and the others were dichromats. Antibodies against short wavelength-sensitive (SWS) cones labeled close to 8% of all cones near the fovea of one dichromat animal, consistent with electrophysiological evidence that the SWS system is present in all marmosets. The topography and spatial density of cone photoreceptors and ganglion cells was similar to that reported for macaque retina, and we found no obvious difference between dichromatic and trichromatic marmoset retinas. These results reinforce the view that the main determinate of primate foveal topography is the requirement for maximal spatial resolution.

Suppressive Surrounds and Contrast Gain in Magnocellular-Pathway Retinal Ganglion Cells of Macaque

The modulation sensitivity of visual neurons can be influenced by remote stimuli which, when presented alone, cause no change in the ongoing discharge rate of the neuron. We show here that the extraclassical surrounds that underlie these effects are present in magnocellular-pathway (MC) but not in parvocellular-pathway (PC) retinal ganglion cells of the macaque. The response of MC cells to drifting gratings and flashing spots was halved by drifting or contrast-reversing gratings surrounding their receptive fields, but PC cell responses were unaffected. The suppression cannot have arisen from the classical receptive field, or been caused by scattered light, because it could be evoked by annuli that themselves caused little or no response from the cell, and is consistent with the action of a divisive suppressive mechanism. Suppression in MC cells was broadly tuned for spatial and temporal frequency and greater at high contrast. If perceptual phenomena with similar stimulus contexts, such as the “shift effect” and saccadic suppression, have a retinal component, then they reflect the activity of the MC pathway.