Primate retina: cell types, circuits and color opponency
Introduction
The mammalian retina displays a diversity of cell types and functionally distinct synaptic pathways (Masland, 1996). Much of this anatomical diversity has been recently summarized (Rodieck, 1988; Sterling, 1990; Vaney, 1990): at least 2 horizontal cell and 10 bipolar cell populations transmit signals in parallel from photoreceptors to ganglion cells. In turn, the ganglion cells further subdivide into an estimated 20–25 anatomically distinct populations that project in parallel to about a dozen target structures in the midbrain and thalamus. Still more complex, the link between ganglion cells and bipolar cells is modulated by the amacrine cell types. To a first approximation there appears to be a number of distinct amacrine cell types dedicated to a given bipolar–ganglion cell pathway, with the total number of amacrine cell populations currently estimated to be at least 40 (Vaney, 1990; Wässle and Boycott, 1991). Thus the “retinal circuit” is not a single circuit but many “microcircuits”, comprising on the order of 80 neural cell types. One purpose of these multiple microcircuits is to create the characteristic physiological properties of the parallel visual pathways that link the retina to a diverse set of target structures in the brainstem. A challenge then, is to systematically characterize retinal cell types with the goal of clarifying the structure and function of the circuitry dedicated to each of the central visual pathways.
The neural code for color begins in the retina. The voltage response of a photoreceptor initiated by the absorption of a photon is independent of the wavelength of that photon. The probability that a photon is absorbed is thus a function of both wavelength and the density of photons incident on the photoreceptor. In the first step toward the generation of chromatic signals the wavelength independent responses of the long, middle and short wavelength sensitive cone types are transformed into spectrally opponent responses of certain retinal ganglion cells (see review in Kaplan et al., 1990). The diversity of cell types of the trichromatic primate retina raises a question as to which cell types display spectral opponency or other physiological properties (such as input from only a single cone type) that would suggest a critical role in an opponent transformation. My goal in this chapter is to briefly review what is currently known of the physiology of morphologically identified cell types in the macaque monkey retina with reference to the generation of color-related signals. The classical approach to this problem has been to combine intracellular recording and cell staining methods to reveal the morphology of a cell whose response to light has been observed (e.g., Dacheux and Raviola, 1990). Recently we have applied this basic technique to an in vitro preparation of the macaque retina. In a modification of this method identified cell types are targeted for intracellular recording and staining under direct microscopic control (Yang and Masland, 1994). Before reviewing the results some critical aspects of the method are outlined in the next section.
Section snippets
In vitro retina–choroid preparation of macaque retina
Intracellular techniques for directly relating morphology to physiology were first applied with limited success to the intact eye of the anesthetized macaque monkey (DeMonasterio, 1979; Zrenner et al., 1983) (see further discussion in Section 5; ganglion cells). A superfused eyecup preparation was later used to make the first intracellular recordings from the non-spiking, H1 horizontal cell type (Dacheux and Raviola, 1990). This approach was also of limited value because the in vitro eyecup was
History: a role in color coding?
Horizontal cells are the lateral interneurons of the outer retina; their dendritic processes innervate the axon terminals of the photoreceptors and form the lateral elements of the synaptic triad. Horizontal cells of a given type are electrically coupled to one another by gap junctions and form a widespreading electrical syncytium; they provide a negative feedback signal to photoreceptors and play an important role in the generation of receptive field surrounds in bipolar cells and ganglion
History: midget and diffuse bipolar classes
The retinal bipolar cells convey photoreceptor signals to the amacrine and ganglion cells, yet despite this central position in the retinal circuitry, very little is known about their responses to light. In non-mammalian retina, bipolar cells show a distinct center-surround receptive field organization (e.g. Kaneko, 1973). Some non-mammalian bipolar cells also show spectral opponency (Kaneko and Tachibana, 1983). In mammalian retina, bipolar cell physiology has been studied mainly at the
History: parasol, midget and small bistratified types
In order to understand the circuitry that gives rise to spectrally opponency it is necessary to clearly identify the ganglion cell types that transmit wavelength-selective signals. In an early attempt to directly link morphology to physiology using intracellular recording and staining methods in the intact primate eye, DeMonasterio addressed the question of which ganglion cell types transmitted spectral opponent signals (DeMonasterio, 1979). He suggested that two common types, the parasol and
History: anatomical diversity
The lack of spectral opponency in the H1 and H2 horizontal cells focuses attention on the amacrine cells, the laterally connecting interneurons of the inner retina, as a basis for cone-opponent circuitry. One possibility, for example, is that a “midget” amacrine cell exists. That is, an amacrine cell type that receives input from a single midget bipolar connected to, say, an L-cone, and directs inhibitory output exclusively to a midget ganglion cell that receives excitatory M-cone input from
Summary and future directions
One major problem for fully characterizing the retinal origins of spectral opponency is the great diversity of cell types in the primate retina whose physiology and morphology remain largely uncharacterized. A fresh approach to this problem is the use of an in vitro preparation of the macaque monkey retina that permits a systematic study of the cone inputs to morphologically identified ganglion cells and retinal interneurons. Horizontal cell types which have long been suggested as key
References (63)
Asymmetry of ON- and OFF-pathways of blue-sensitive cones of the retina of macaques
Brain Res.
(1979)- et al.
A multi-stage color model
Vision Res.
(1993) - et al.
Double color-opponent receptive fields of carp bipolar cells
Vision Res.
(1983) Receptive fields in primate retina
Vision Res.
(1996)Processing and encoding of visual information in the retina
Curr. Opin. Neurobiol.
(1996)- et al.
Losses in peripheral colour sensitivity predicted from “hit and miss” post-receptoral cone connections
Vision Res.
(1996) - et al.
Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina
Vision Res.
(1983) - et al.
Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey
Neuroscience
(1984) - et al.
Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm
Vision Res.
(1975) The mosaic of amacrine cells in the mammalian retina
Prog. Retinal Res.
(1990)
Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina
Vision Res.
Characteristics of the blue sensitive cone mechanism in primate retinal ganglion cells
Vision Res.
Intracellular recordings from a biplexiform ganglion cell in Macaque retina, stained with horseradish peroxidase
Brain Res.
Horizontal cells and cone photoreceptors in primate retina: a golgi-light microscopic study of spectral connectivity
J. Comp. Neurol.
Horizontal cells and cone photoreceptors in human retina: a golgi-electron microscopic study of spectral connectivity
J. Comp. Neurol.
Morphological classification of bipolar cells of the primate retina
Eur. J. Neurosci.
Trichromacy, opponent colours coding and optimum colour information transmission in the retina
Proc. R. Soc. Lond. (Biol.)
Synaptic feedback, depolarization, and color opponency in cone photoreceptors
Visual Neurosci.
Cone inputs to three types of non-midget ganglion cell in macaque fovea
Invest. Ophthal. Visual Sci., Suppl.
Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina
Nature
Axon-bearing amacrine cells of the macaque monkey retina
J. Comp. Neurol.
Morphology of a small-field bistratified ganglion cell type in the macaque and human retina
Visual Neurosci.
Morphology and physiology of the AII amacrine cell network in the macaque monkey retina
Soc. Neurosci. Abstr.
The “blue-on” opponent pathway in primate retina originates from a distinct bistratified ganglion cell type
Nature
Horizontal cells of the primate retina: cone specificity without spectral opponency
Science
Dendritic field size and morphology of midget and parasol ganglion cells of the human retina
Proc. Natl. Acad. Sci. USA
The rod pathway in the rabbit retina. A depolarizing bipolar and amacrine cell
J. Neurosci.
Physiology of HI horizontal cells in the primate retina
Proc. R. Soc. Lond. (Biol.)
Glutamate responses of bipolar cells in a slice preparation of the rat retina
J. Neurosci.
Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina
Visual Neurosci.
Glycine receptors in the rod pathway of the macaque monkey retina
Visual Neurosci.
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