Quantitative analysis of cone photoreceptor–horizontal cell connectivity patterns in the retina of a cyprinid fish: Electron microscopy of functionally identified and HRP‐labelled horizontal cells

Abstract

Horizontal cells generating photopic luminosity and biphasic/chromaticity-type S-potentials were identified and intracellularly labelled with horseradish peroxidase in the retina of the roach. The synaptic connectivity patterns of the horizontal cell dendrites within pedicles of different spectral types of cone were then quantitatively studied by electron microscopy. Luminosity-type responses were generated by H1-like horizontal cells contacting similar numbers of red- and green-sensitive cones and very few blue-sensitive cones. Most dendritic contacts were lateral to synaptic ribbons. Central contacts with ribbons were made almost exclusively within red-sensitive cone pedicles. Biphasic/chromaticity-type S-potentials were generated by H2-like horizontal cells. The dendrites of the latter contacted green- and blue-sensitive cones, both at central and lateral sites at synaptic ribbons. An attempt was made to correlate cone ribbon connectivity patterns and spectral characteristics of the horizontal cells according to several hypotheses, some proposed in earlier studies.

Spectral Responses in Zebrafish Horizontal Cells Include a Tetraphasic Response and a Novel UV-Dominated Triphasic Response

“…7A). The blue cone contacts of H1 are presumptive sites of horizontal cell output through feedback, although as previously noted, some of the red and green cone contacts may also be feedback sites (Downing and Djamgoz 1989;Kamermans and Spekreijse 1995). Hyperpolarizations for blue and UV stimulation in H1 monophasic cells originate only via excitation of red and green opsins and not by excitatory contacts with blue and UV cones.…”

“…In particular cases where a dominant or nondominant cone is found to provide a depolarizing influence, its hyperpolarizing V max was set to 0. types are dominated by red cone inputs (De Aguiar et al 2006;Djamgoz 1984;Djamgoz and Ruddock 1979;Djamgoz et al 1985;Ohtsuka and Kouyama 1986;Sakai et al 1997;Ventura et al 1999Yang et al 1983;Yazulla 1976). However, monophasic cells receiving dominant or nondominant inputs from more than one photoreceptor type, such as red and green (Dacey et al 1996(Dacey et al , 2000De Aguiar et al 2006;Downing and Djamgoz 1989;Hashimoto and Inokuchi 1981;Hashimoto et al 1988;Kamermans and Spekreijse 1995;Kamermans et al 1989b;Sakai et al 1997;Twig et al 2003;Yang et al 1983;Yazulla 1976), red and blue (Nelson 1985), green and blue (Djamgoz 1984;Djamgoz and Ruddock 1979;Djamgoz et al 1985;Yazulla 1976), or red, green, and blue (Asi and Perlman 1998;Dacey et al 1996;Twig et al 2003;Yazulla 1976) also exist.…”

“…In goldfish, cone horizontal cells are classified as H1, H2, and H3 types, roughly in order of dendritic diameter. H1 cells are monophasic, H2 cells are biphasic, and H3 cells are triphasic (De Aguiar et al 2006;Downing and Djamgoz 1989;Stell et al 1975; for reviews, see Kamermans and Spekreijse 1995;Twig et al 2003). Selective cone contacts combine with feedback circuits between horizontal cells and cones (Kamermans et al 1991(Kamermans et al , 1989aStell and Lightfoot 1975) to comprise the underlying circuitry generating multiphasic horizontal cell responses to color.…”

Light adaptation affects synaptic vesicle density but not the distribution of GABA A receptors in goldfish photoreceptor terminals

“…The proposed widespread distribution of GABA sensitivity raises questions as to the role of horizontal cell spinules in GABA release. Horizontal cell spinules have been studied intensively over the last few years, yet their function remains controversial (i.e., Burkhardt, 1993;Downing and Djamgoz, 1989;Wagner and Djamgoz, 1993). Perhaps the spinules are involved in the efficacy of signal transmission from horizontal cells to cones, without being the actual site of GABA release.…”

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).…”