Color opponency in horizontal cells of the vertebrate retina

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Abstract

Chromaticity (C-type) horizontal cells have been studied extensively for more than 40 years since the first recording of such units in the fish retina. C-type horizontal cells are seen in almost every retina of cold-blooded species that contains at least two different spectral types of cone. These cells are characterized by photoresponses of polarity that depends upon the wavelength of the stimulating light. There are two basic varieties of chromaticity horizontal cells, biphasic or triphasic cells. Biphasic cells are characterized by one wavelength in which response polarity reverses and triphasic cells have two wavelengths where response polarity reverses. The neuronal network underlying the genesis of color opponency in C-type horizontal cells has been the subject of debate for many years. It is generally accepted now that cones feed-forward excitatory inputs to horizontal cells which in turn exert inhibitory effects on the cones by negative feedback pathways.

C-type horizontal cells belonging to the same class are interconnected via gap junctions to form a tight syncytium. However, the spatial properties of these cells depend upon the polarity of the photoresponse because the membrane resistances of the syncytium change with different inputs. Thus, color opponency in C-type horizontal cells depends on the spatial properties of the stimulating light in addition to its dependence upon wavelength, intensity and ambient illumination. The functional role of C-type horizontal cells is to influence the spatial–chromatic organization of the receptive fields of proximal neurons. Thus, the responsiveness of bipolar cells and ganglion cells to surround illumination depend to a great extent upon the horizontal cells. However, the exact mode whereby horizontal cells can affect the organization of the proximal neurons has yet to be elucidated.

Section snippets

The S-potentials

In 1953, Gunar Svaetichin first reported on light-evoked responses that were recorded intracellularly from the vertebrate retina (Svaetichin, 1953). He believed that these responses originated in single cone photoreceptors and therefore, the title of his article was “The cone action potential”. Only later studies, using dye-filled microelectrodes proved that S-potentials originated from 2nd order retinal neurons; horizontal cells (Kaneko, 1970; Werblin and Dowling, 1969).

Since first described

Chromaticity (C-type) horizontal cells in different species

The idea that color opponency can start so early in the visual system; at the first synapse in the retina, has attracted numerous researchers, all of whom have studied the spectral properties of the chromaticity units (C-types) and the neuronal circuits that underlie their genesis. The diversity of C-type horizontal cells within and between retinas depends upon the number of different cone pigments and the neural interactions between cones and horizontal cells. Furthermore, studies in the same

Physiological—anatomical correlation of C-type horizontal cells

Golgi staining, intracellular marking and immunostaining techniques have been used to characterize the various morphologies of horizontal cells in different vertebrate retinas (Boycott et al., 1978; Cajal, 1972; Gallego, 1986; Kolb, 1970; Kolb et al., 1988; Leeper 1978a, Leeper 1978b; Stell and Lightfoot, 1975; Wässle and Reiman, 1978). When these techniques were coupled to electrophysiological recordings of horizontal cell photoresponses, morpho-physiological correlation could be made (

Defining color opponency

Color opponency in vertebrate horizontal cells is expressed in depolarizing responses to wavelengths in one part of the spectrum and hyperpolarizing responses to wavelengths in another part. Therefore, the wavelength at which response polarity reverses can be used to define the spectral properties of these cells. We will call this wavelength, the null wavelength.

In order to define the spectral properties of the horizontal cells, monochromatic light stimuli of dim intensity are used to elicit

The neural network underlying color opponency in horizontal cells

The neural interactions underlying the genesis of color opponency in horizontal cells is of interest because it represents the locus where the trichromatic color channels are transformed into opponent channels. A neural network of excitatory feed-forward and inhibitory feedback pathways have been suggested, based on anatomical observations of cone-horizontal cell connections, to underlie color opponency in fish (Stell, 1967; Stell and Lightfoot, 1975). These anatomical observations were

Gap junctions

All physiological types of horizontal cell in all vertebrate species are connected to their homologous neighbors by gap junctions (Kolb, 1977; Witkovsky and Dowling, 1969; Yamada and Ishikawa, 1965). Gap junctions are formed at closely applied plasma membranes (2–4nm gap) of the two horizontal cell structures. Each half of the cell supplies connexons or hemichannels to complete the gap junction channel. In fish and turtle retinas Cx43 and Cx26 have been demonstrated to comprise the horizontal

Modulation of color opponency in C-type horizontal cells

The functional properties and even the morphological characteristics of horizontal cells can be modulated by physiological conditions and by a variety of chemicals that are released by retinal cells when the conditions of illumination are changed. These neuromodulators alter the modes of information processing in order to adjust retinal function to a new state of adaptation. The most extensively studied neuromodulator is dopamine but in recent years nitric oxide and retinoic acid have been

Color matching and the pigment theory

Color matching is one of the most fundamental psychophysical experiments in color vision. The subject is instructed to adjust the intensities of red, green and blue lights until the mixture appears indistinguishable from a given monochromatic light stimulus. According to the pigment theory, color matching is achieved only when the rate of photon absorption by each of the visual pigments participating in color vision is equal for the matched light stimuli (Alpern, 1989; Rushton, 1972). The

Functional roles of C-type horizontal cells

The phototransduction process in the outer segments of the photoreceptors transforms light energy into electrical activity that is then, transmitted via chemical and electrical synapses from the photoreceptors to the bipolar and ganglion cells. The ganglion cells serve as the output neurons of the retina transmitting their light-induced electrical activity to the brain. The light-induced ganglion cell responses differ significantly from those of the photoreceptors due to the extensive

Future perspectives

The spectral properties of chromaticity horizontal cells and the neural interactions in the distal retina between cone photoreceptors and horizontal cells have been studied extensively for over 40 years following the first report of color opponency in an S-unit (Svaetichin and MacNichol, 1958). Electrophysiological recordings of membrane potentials and membrane currents, anatomical observations of neuronal interactions and immunostaining techniques for localization of specific proteins have led

Acknowledgements

This chapter is dedicated to two scientists who have been very influential in vision research and introduced me (I.P.) to color vision and to horizontal cell physiology; Matthew Alpern and Mike Fuortes. We thank other colleagues especially Richard A. Normann and Helga Kolb for their valuable advice throughout the years. We thank the Israel Science Foundation for continued support over the years.

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