Color opponency in cone-driven horizontal cells in carp retina. Aspecific pathways between cones and horizontal cells.

Abstract

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...

The dynamic characteristics of the feedback signal from horizontal cells to cones in the goldfish retina

“…This stimulus strongly activated the L-cones, whereas it hardly stimulated the M-cones. This depolarizing response is generated via negative feedback from the MHCs to the M-cones (see Fig Lightfoot, 1975; Kamermans et al 1991;Kamermans & Spekreijse, 1995). The mean time constant of this depolarizing response was 36 ± 8 ms (n = 6).…”

“…1A) (Piccolino et al 1981;Wu, 1994;. Note that the feedback pathway that generates the depolarizing response in the BHC is the same negative feedback pathway as that generating the rollback response in the MHCs Kamermans et al 1991;Kamermans & Spekreijse, 1995).…”

“…MHCs feed back to M-cones and induce via this pathway a depolarizing response in BHCs to red light Kamermans et al 1991;Kamermans & Spekreijse, 1995). For shorter wavelengths, the depolarizing response will become smaller and, finally, hyperpolarizing.…”

Localization of the AMPA subunit GluR2 in the outer plexiform layer of goldfish retina

“…The elegance of this model was that it not only accounted for the then present data but also had predictive value and generated numerous studies to determine its validity. There have been two substantive modifications of this model in fish based on combined electrophysiological and anatomical findings (Downing and Djamgoz, 1989;Kamermans et al, 1991;Kamermans and Spekreijse, 1995). The major modification was that the lateral horizontal cell dendrites served both pre-and postsynaptic functions, as opposed to the purely presynaptic function proposed by Stell and Lightfoot (1975).…”

Tetrachromatic input to turtle horizontal cells

“…Since they respond opponently to different spectral wavelengths (Svaetichin & MacNichol, 1958), they were implicated in color processing in early studies and formed the basis of different models of color processing (Gouras, 1972;Fuortes & Simon, 1974;Stell, 1975). More recently, they have been considered part of a feedback system to produce color constancy (Kamermans et al, 1991).…”