Physiology of Horizontal Cells
[History] [Archetypical circuitry] [Passive electrical models] [Rod and cone contributions] [Spatial characteristics] [Gap junctions] [Functional roles] [Color opponency] [References]
8. Color opponency.
Multiple cone types with pigments tuned to different regions of the visible spectrum provide vertebrates the opportunity to discriminate colors. Most mammals are dichromats (having 2 cone types); however, old world monkeys, humans, and many nonmammalian species are trichromats. Even tetrachromatic species are found among lower vertebrates. In addition to red-, green- and blue-sensitive types fish, birds and reptiles have a fourth photoreceptor sensitive to ultraviolet wavelengths. Since cones of different spectral types are directly connected to horizontal cells, it is of interest to explore how horizontal cells integrate and process this richness of spectral information. Two forms of processing are found: 'luminosity' and 'chromaticity'. Luminosity-type cells are hyperpolarized by all stimulus wavelengths and dominated by signals from red-sensitive cones. There are two varieties of chromaticity type horizontal cell: a common type depolarized by red stimuli and hyperpolarized by blue or green stimuli; and a rare trichromatic type depolarized by green stimuli and hyperpolarized by either blue or far red stimuli.
Chromaticity responses have been extensively studied in turtle and fish retinas (Svaetichin and MacNicol, 1958; Naka and Rushton, 1966; Spekreijse and Norton, 1970; Saito et al, 1973; Fuortes and Simon, 1974; Yazulla, 1976; Kolb and Lipetz, 1991; Kammermans and Spekreijse, 1995; Ammermuller and Kolb, 1996, for reviews). The responses of H2 and H3 type chromaticity horizontal cells in the turtle retina are shown in Fig. 14 below (Ammermuller and Kolb, 1996).
Fig. 14. C-type responses in H2 and H3 cells of the turtle retina (59 K jpeg image)
A cascade model, now called the Stell model, based on anatomical connections explained the opponent physiology in horizontal cells of the fish retina (Stell and Lightfoot, 1975; Stell et al.,1975; Stell, 1976). The important findings of the Stell model are that, 1) Horizontal cells are selective for cone input, and 2) the Horizontal cells are selective in output feeding back only to cones of the next shorter wavelength than represented by their inputs. The circuit (Fig. 15, below) has some of the red (L) cones responding to light by hyperpolarizations transmitted with the same polarity to monophasic (L/OFF) horizontal cell (H1 cells). As a result, H1 is hyperpolarized upon illumination of the retina. Similarly biphasic (M/OFF, L/ON) (H2) cells respond with hyperpolarization to illumination of green (M) cones and the triphasic (S/OFF, M/ON, L/OFF) (H3) cells to illumination of blue (S) cones. The cascade part of the circuit is that each H1 sends its voltage changes with reversed polarity to some cones (feedback) (Baylor et al., 1971), in this case to green cones, and each H2 sends its voltage changes with reversed polarity to blue cones. The incoming signal from the horizontal cell adds with the signal evoked by light to produce a modified signal in the cone that is transmitted to the horizontal cell of the next type as well as to any bipolar cells synapsing with that cone. As a result, while H1 hyperpolarizes to all wavelengths of illumination and with maximum response to red wavelengths (Fig. 15, below), H2 depolarizes to red wavelengths and hyperpolarizes to green wavelengths, and H3 hyperpolarizes to blue, depolarizes to green, and hyperpolarizes to red wavelengths. Witkovsky et al. (1995) showed that a Stell type cascade model for color processing was applicable to Xenopus horizontal cells too.
Fig. 15. Cascade model of color opponency in fish horizontal cells (98 K jpeg image)
Fig. 16. Recent model of color opponency in fish horizontal cells (98 K jpeg image)
More recently, Kamermans and Spekreijse (1995) disagree with the details of the anatomical connectivity shown by Stell but agree with the general principles. In their model the mono-, bi- and triphasic horizontal cells are connected to all cone types with both feedforward and feedback synapses (Fig. 16, above) but their major inputs are still from the one spectral type of cone as in the Stell model.The major difference between the three horizontal cell types is in the feedforward and feedback strength of the cone horizontal cell pairs. It is proposed that the cones modulate specific glutamate receptors of each horizontal cell type and that cone inputs can shunt each other so giving rise to the special wavelength responses recorded in the different horizontal cell types (see Kamermans and Spekreijse, 1995 for full details).
The consequences of the opponent color characteristics of the three horizontal cell types in the fish retina and also the turtle retina (see Ammermuller and Kolb, 1996, for review) are that spectrally opponent surrounds for the bipolar cells can be generated by horizontal cell feedback pathways. The figure below shows how spectral opponency would be generated in a single opponent red OFF, red/green ON cell and a double opponent red OFF/green ON, red ON/green OFF cell. In the double opponent bipolar cell (Fig. 17, top), the bipolar responds in its center with a hyperpolarization from red cones and a depolarization from green cones. The feedback from the mono and biphasic horizontal cells would mean in essence that the feedback through the green cones will work against the feedback through the red cones (dashed and dotted lines in Fig. 17, below ) so the surround of the double opponent bipolar would have a green hyperpolarization and a red depolarization. The opponent surround of the single opponent cell is easier to model. The hyperpolarizing red center of the bipolar cells has a red and green depolarizing surround formed by the red part of the signal of both mono- and biphasic horizontal cells working against each other in the red and collaborating in the green (dashed lines) (Kamermans and Spekreijse, 1995).
Fig. 17. Model of color opponency surround formation in fish bipolar cells (98 K jpeg image)
Given this background from lower vertebrates, it was a surprise that mammalian retinas revealed only luminosity-type horizontal cell responses, even in trichromatic primates (Steinberg, 1969; Niemeyer and Gouras, 1973; de Monesterio, 1978; Nelson, 1985; Dacheux and Raviola, 1990; Dacey et al., 1996). There are two types of horizontal cell in most mammals and possibly even a third type in primates. Similar to lower vertebrates, several of these cells are selective in cone innervation (Ahnelt and Kolb, 1994; Dacey et al., 1996).
Spectral sensitivity is the classic assay to determine the chromatic composition of visual signals. Spectral sensitivity curves typically plot the reciprocal of the minimum amount of light energy required to satisfy a detection task at a sampling of wavelengths across the visible spectrum. If less light is required to evoke a criterion response at one wavelength than another, the spectral sensitivity is said to be higher at that wavelength. When signals from several, spectrally distinct, photoreceptor types impinge on a second, or higher order visual neuron, such as a horizontal cell, the shape of spectral sensitivity curves is, in general, not unique, but depends both on stimulus conditions and the detection task chosen.
Fig. 18. Multiple cone signals in cat horizontal cells (98 K jpeg image)
Sets of spectral sensitivity curves, obtained in a cat horizontal cell, appear in Fig. 18, above. The shape of the curves depends both on the color of background illumination, and on the criterion (threshold) response level. Backgrounds are used to minimize contributions from rods through light adaptation, so that only cone signals are observed. Red curves characterize spectral sensitivities in the presence of steady red adapting backgrounds, while blue curves characterize spectral sensitivities in the presence of steady blue adapting backgrounds. Red cone sensitivity is relatively more depressed by red backgrounds, while blue cone sensitivity is relatively more depressed by blue backgrounds. The 'task' is to evoke a hyperpolarizing voltage responses of a chosen 'threshold' size at each wavelength. For a set of 'thresholds' a nested set of curves is generated. The smallest threshold voltage change studied (1 mV) on red backgrounds produces a spectral sensitivity curve peaked at 440 nm, revealing the presence of low voltage signals from blue cones. On blue backgrounds this signal is depressed, and the 1 mV threshold level reveals a spectral peak at 559 nm, the signature of the red cones. Regardless of background, raising threshold levels shifts spectral sensitivities towards that of the red-sensitive cones, reflecting the large amplitude contributions from this source. With red backgrounds, increases in threshold level also result in significant sensitivity losses in the 543 nm region. This is too long a wavelength to be much influenced by blue cones, and so may reflect a low-amplitude input from cat green (mid spectral) cones, a trichromatic input. Cat horizontal cells are all luminosity types. Although dominated by high-amplitude red-cone signals, low-level synergistic inputs from blue and green cones clearly contribute.
A further refinement on the 'indiscriminate-synergistic' pattern of cone input to mammalian horizontal cells has been proposed by Ahnelt and Kolb (1994a) and Dacey et al (1996). In primate retina, horizontal cells also occur only as luminosity types. Some of these cells receive synergistic signals only from red and green cones (Physiological responses of H1 cells, Fig. 19, below), while others receive synergistic input from red, green and blue cone types (Physiological responses in H2 types, Fig. 20, below). Anatomically H1 type horizontal cells tend to avoid blue cone pedicles innervating them only sparsely (blue outlines in Fig. 19, below). On the other hand HII type horizontal cells direct large numbers of dendrites towards these same blue cone synaptic pedicles (blue outlines, Fig. 20, below).
Fig 19. Intracellular staining and chromatic responses of H1 cells in monkey retina (89 K jpeg image)
Fig. 20. Intracellular staining and chromatic responses of H2 cells in monkey retina (89 K jpeg image)
The H1 and H2 types of horizontal cell both give the slow hyperpolarizing responses to a light flash even when using different wavelengths of light. HI cells are not sensitive to stimuli selective for S-cones (Fig. 19E). On the other hand, H2 cells are very sensitive to the S-wavelength (blue) end of the spectrum (Fig. 20E), but the response is still a hyperpolarizing S-potential as to the L- (red) and M-wavelengths (green) (Dacey et al., 1996). This contrasts greatly with the findings for fish and turtle horizontal cells. Thus there appears to be emerging evidence for subsets of mammalian luminosity type cells devoted primarily to processing either blue signals, or red and green signals, however spectral opponency does not appear to be part of the processing regime. If such is the case, we shall have to await further experimentation on this subject to confirm how non-opponent horizontal cells can form chromatic opponent bipolar and ganglion cells in primate retinas.
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[History] [Archetypical circuitry] [Passive electrical models] [Rod and cone contributions] [Spatial characteristics] [Gap junctions] [Functional roles] [Color opponency] [References]
Updated: May, 2001