A B S T R A C T The spectral and dynamic properties of cone-driven horizontal cells in carp retina were evaluated with silent substitution stimuli and/or saturating background illumination. The aim of this study was to describe the wiring underlying the spectral sensitivity of these cells. We will present electrophysiological data that indicate that all cone-driven horizontal cell types receive input from all spectral cone types, and we will present evidence that all cone-driven horizontal cell types feed back to all spectral cone types. These two findings are the basis for a model for the spectral and dynamic behavior of all cone-driven horizontal cells in carp retina. The model can account for the spectral as well as the dynamic behavior of the horizontal cells. It will be shown that the strength of the feedforward and feedback pathways between a horizontal cell and a particular spectral cone type are roughly proportional. This model is in sharp contrast to the Stell model, where the spectral behavior of the three horizontal cell types is explained by a cascade of feedforward and feedback pathways between cones and horizontal cells. The Stell model accounts for the spectral but not for the dynamic behavior of the horizontal cells.
INTRODUCTIONIn carp and goldfish retina three types of cone-driven horizontal cells exist. They are called the mono-, bi-, and triphasic horizontal cells (MHC, BHC, and THC) depending on their spectral sensitivity characteristics (MacNichol and Svaetichin, 1958;Norton et al., 1968). Stell and co-workers (SteU et al., 1975(SteU et al., , 1982Stell, 1976) proposed a cascade model, which relates the spectral response properties of the horizontal cells (HC) to the structure of the ribbon synapse in the cone synaptic terminal. Stell's model is based on a morphological study of Golgi impregnated material from goldfish retina. In that study it was shown VOLUME 97" 1991 that the H 1 cells make central as well as lateral contacts with the synaptic ribbons of the long wavelength sensitive cones (R-cones) and make lateral contacts only with the middle and short wavelength sensitive cones (G-cones, B-cones). The H2 cells, however, make central as well as lateral contacts in the G-cones and make lateral contacts only with the B-cones. Finally, the H3 cells make central as well as lateral contacts only with the B-cones.Assuming that the central HC processes are the forward pathway from the cones to the HCs, that the lateral HC processes are a sign-inverting feedback pathway from HCs to the cones, and that the HI cells correspond to MHCs, H2 cells to BHCs, and H3 cells to THCs, the color coding of the HCs could be explained simply.However, three major problems exist with the Stell model: (a) The dynamics of the responses of all three cone horizontal cell types in carp retina to red light are equal except for latency differences (Spekreijse and Norton, 1970). According to the model of Stell, these responses are generated through different pathways, and hence should show latency as well as dynam...