Jan Kremers

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.

L/M cone ratios in human trichromats assessed by psychophysics, electroretinography, and retinal densitometry.

Estimates of the relative numbers of long-wavelength-sensitive (L) and middle-wavelength-sensitive (M) cones vary considerably among normal trichromats and depend significantly on the nature of the experimental method employed. Here we estimate L/M cone ratios in a population of normal observers, using three psychophysical tasks-detection thresholds for cone-isolating stimuli at different temporal frequencies, heterochromatic flicker photometry, and cone contrast ratios at minimal flicker perception--as well as flicker electroretinography and retinal densitometry. The psychophysical tasks involving high temporal frequencies, specifically designed to tap into the luminance channel, provide average L/M cone ratios that significantly differ from unity with large interindividual variation. In contrast, the psychophysical tasks involving low temporal frequencies, chosen to tap into the red-green chromatic channel, provide L/M cone ratios that are always close to unity. L/M cone ratios determined from electroretinographic recordings or from retinal densitometry correlate with those determined from the high-temporal-frequency tasks. These findings suggest that the sensitivity of the luminance channel is directly related to the relative densities of the L and the M cones and that the red-green chromatic channel introduces a gain adjustment to compensate for differences in L and M cone signal strength.

Ganglion cells of a short-wavelength-sensitive cone pathway in New World monkeys: morphology and physiology.

We have studied the morphology and physiology of retinal ganglion cells of a short-wavelength-sensitive cone (SWS-cone) pathway in dichromatic and trichromatic New World anthropoids, the capuchin monkey (Cebus apella) and tufted-ear marmoset (Callithrix jacchus). In Old World anthropoids, in which males and females are both trichromats, blue-ON/yellow-OFF retinal ganglion cells have excitatory SWS-cone and inhibitory middle- and long-wavelength-sensitive (MWS- and LWS-) cone inputs, and have been anatomically identified as small-field bistratified ganglion cells (SB-cells) (Dacey & Lee, 1994). Among retinal ganglion cells of New World monkeys, we find SB-cells which have very similar morphology to such cells in macaque and human; for example, the inner dendritic tree is larger and denser than the outer dendritic tree. We also find blue-on retinal ganglion cells of the capuchin to have physiological responses strongly resembling such cells of the macaque monkey retina; for example, responses were more sustained, with a gentler low frequency roll-off than MC-cells, and no evidence of contrast gain control. There was no difference between dichromatic and trichromatic individuals. The results support the view that SWS-cone pathways are similarly organized in New and Old World primates, consistent with the hypothesis that these pathways form a phylogenetically ancient color system.

Angular Velocity, Not Temporal Frequency Determines Circular Vection

This paper shows that the experienced speed of circular vection depends on stimulus speed, not on stimulus temporal frequency. But why would anyone think the contrary? The point is that many modelers in the field of motion perception believe that perceived speed is determined by temporal frequency. Moreover, the optokinetic behaviour of the fly is said to be dependent on the temporal frequency, not the speed, of the stimulus pattern (Reichardt, 1987). It was the aim of the present experiment to test the notion that the experienced speed of circular vection is proportional to stimulus velocity information, which is carried by the temporal and the spatial characteristics of light.

Morphology and physiology of primate M- and P-cells

Catarrhines and platyrrhines, the so-called Old- and New-World anthropoids, have different cone photopigments. Postreceptoral mechanisms must have co-evolved with the receptors to provide trichromatic color vision, and so it is important to compare postreceptoral processes in these two primate groups, both from anatomical and physiological perspectives. The morphology of ganglion cells has been studied in the retina of catarrhines such as the diurnal and trichromatic Macaca, as well as platyrrhines such as the diurnal, di- or trichromatic Cebus, and the nocturnal, monochromatic Aotus. Diurnal platyrrhines, both di- and trichromats, have ganglion cell classes very similar to those found in catarrhines: M (parasol), P (midget), small-field bistratified, and several classes of wide-field ganglion cells. In the fovea of all diurnal anthropoids, P-cell dendritic trees contact single midget bipolars, which contact single cones. The Aotus retina has far fewer cones than diurnal species, but M- and P-cells are similar to those in diurnal primates although of larger size. As in diurnal anthropoids, in the Aotus, the majority of midget bipolar cells, found in the central 2 mm of eccentricity, receive input from a single cone and the sizes of their axon terminals match the sizes of P-cell dendritic fields in the same region. The visual responses of retinal ganglion cells of these species have been studied using single-unit electrophysiological recordings. Recordings from retinal ganglion cells in Cebus and Aotus showed that they have very similar properties as those in the macaque, except that P-cells of mono- and dichromatic animals lack cone opponency. Whatever the original role of the M- and P-cells was, they are likely to have evolved prior to the divergence of catarrhines and platyrrhines. M- and P-cell systems thus appear to be strongly conserved in the various primate species. The reasons for this may lie in the roles of these systems for both achromatic and chromatic vision.

Visual responses of ganglion cells of a New‐World primate, the capuchin monkey, Cebus apella

1 The genetic basis of colour vision in New‐World primates differs from that in humans and other Old‐World primates. Most New‐World primate species show a polymorphism; all males are dichromats and most females trichromats. 2 In the retina of Old‐World primates such as the macaque, the physiological correlates of trichromacy are well established. Comparison of the retinae in New‐ and Old‐World species may help constrain hypotheses as to the evolution of colour vision and the pathways associated with it. 3 Ganglion cell behaviour was recorded from trichromatic and dichromatic members of a New‐World species (the capuchin monkey, Cebus apella) and compared with macaque data. Despite some differences in quantitative detail (such as a temporal response extended to higher frequencies), results from trichromatic animals strongly resembled those from the macaque. 4 In particular, cells of the parvocellular (PC) pathway showed characteristic frequency‐dependent changes in responsivity to luminance and chromatic modulation, cells of the magnocellular (MC) pathway showed frequency‐doubled responses to chromatic modulation, and the surround of MC cells received a chromatic input revealed on changing the phase of heterochromatically modulated lights. 5 Ganglion cells of dichromats were colour‐blind versions of those of trichromats. 6 This strong physiological homology is consistent with a common origin of trichromacy in New‐ and Old‐World monkeys; in the New‐World primate the presence of two pigments in the middle‐to‐long wavelength range permits full expression of the retinal mechanisms of trichromatic vision.

Flicker cone electroretinogram in dichromats and trichromats

To measure cone signal strengths in the flicker electroretinogram (ERG) of dichromats and trichromats, we developed a set of flickering stimuli (30 Hz), which excite the middle-wavelength-sensitive (M-) and long-wavelength-sensitive (L-) cones independently. ERG responses to eight different ratios of L- to M-cone contrasts were recorded from each subject. The short-wavelength-sensitive (S-) cone contrast was 0% in all measurements. The recordings were Fourier analyzed to determine the amplitude of the fundamental component. ERG threshold values for each subject resulted in ellipses when plotted in an L-/M-cone contrast space. As expected, the orientations of the threshold ellipses of the protanopes (N = 2) were parallel to the L-cone axis, whereas those of the deuteranopes (N = 2) were parallel to the M-cone axis. For the trichromats (N = 5), there was considerable interindividual variation in ellipse orientation.

Receptive field dimensions of lateral geniculate cells in the common marmoset (Callithrix jacchus)

We measured the spatial receptive field dimensions of cells in the lateral geniculate nucleus (LGN) of the common marmoset (Callithrix jacchus) using a bipartite field stimulus in which the two halves of the field were modulated identically but in counterphase. Horizontal and vertical edges between the two fields were positioned at different locations in the receptive field. By assuming that centers and surrounds have gaussian profiles, we were able to obtain a satisfactory mathematical description of the data. Receptive field centers were about a factor 1.6 larger than those of macaque LGN cells, in accordance with the smaller marmoset eye. There was a limited correspondence with dendritic tree dimensions of marmoset retinal ganglion cells. We further found that center and surround gaussians were not always concentric, and that the centers of some cells were elongated. This might allow some direction or orientation biases in LGN cells.

The assessment of L- and M-cone specific electroretinographical signals in the normal and abnormal human retina.

Electroretinography (ERG) is a non-invasive method that can contribute to a description of the functional organization of the human retina under normal and pathological circumstances. The physiological and pathophysiological processes leading to an ERG signal can be better understood when the cellular origins of the ERG are identified. The ERG signal recorded at the cornea is initiated by light absorption in the photoreceptors which leads to activity in the photoreceptors and in their post-receptoral pathways. Light absorption in distinct photoreceptor types may lead to different ERG responses caused either by differences between the photoreceptors or between their post-receptoral pathways. The description of contributions of the different photoreceptor types to the ERG may therefore give more detailed insight in the origins of the ERG. Such a description can be obtained by isolating the responses of a single photoreceptor type. Nowadays, careful control of differently colored light sources together with the relatively well-known cone and rod fundamentals enables a precise description and control of photoreceptor excitation. Theoretically, any desired combination of photoreceptor excitation modulation can be achieved, including conditions in which the activity in only one photoreceptor type is modulated (silent substitution). In this manner the response of one photoreceptor type is isolated without changing the state of adaptation. This stimulus technique has been used to study the contribution of signals originating in the different photoreceptor types to the human ERG. Furthermore, by stimulating two or more photoreceptor types simultaneously, the interaction between the different signals can be studied. With these new techniques results of measurements in healthy subjects and patients with retinal diseases can be compared. This approach should ultimately help to develop better diagnostic tools and result in a fuller description of the changes and the pathophysiological mechanisms in retinal disorder. Finally, data obtained with cone and rod specific stimuli may lead to a reinterpretation of the standard ERG used in a clinical setting.

Cone selective adaptation influences L- and M-cone driven signals in electroretinography and psychophysics.

To assess the influence of selective adaptation of long (L) and middle (M) wavelength sensitive cones with electroretinography (ERG) and psychophysics, a novel adaptation procedure was developed, which comprises a selective and quantifiable change in the state of adaptation in the different cone types. One adaptation condition was used as a reference. In four additional conditions, the M-cones or the L-cones were selectively adapted, so that they absorbed either more or less photons. At each of these five states of adaptation, the ERG response amplitudes to 30Hz L- and to M-cone selective stimuli were measured. Furthermore, the psychophysical sensitivities to L- and M-cone selective stimuli were measured at different temporal frequencies. In subjects with normal color vision, adaptation can have a strong influence on the L- and M-cone driven response amplitudes in the ERG and on both the L- and the M-cone sensitivities in the psychophysical luminance channel. As a result, the L- to M-cone ERG and psychophysical ratios can change dramatically at the different states of adaptation. The cone sensitivity thresholds and the L- to M-cone sensitivity ratio in the psychophysical chromatic channel are about unity at all states of adaptation, suggesting the presence of a compensatory mechanism. In dichromats, the responses and sensitivities to stimulation of the absent cone type were generally small at all states of adaptation. But, with reddish backgrounds residual ERG responses and residual psychophysical sensitivities were observed, indicating the presence of either a robust rod driven signal or an additional adaptation mechanisms that are not cone driven and that have not been described before.