The number and distribution of bipolar to ganglion cell synapses in the inner plexiform layer of the anuran retina

Abstract

The main route of information flow through the vertebrate retina is from the photoreceptors towards the ganglion cells whose axons form the optic nerve. Bipolar cells of the frog have been so far reported to contact mostly amacrine cells and the majority of input to ganglion cells comes from the amacrines. In this study, ganglion cells of frogs from two species (Bufo marinus, Xenopus laevis) were filled retrogradely with horseradish peroxidase. After visualization of the tracer, light-microscopic cross sections showed massive labeling of the somata in the ganglion cell layer as well as their dendrites in the inner plexiform layer. In cross sections, bipolar output and ganglion cell input synapses were counted in the electron microscope. Each synapse was assigned to one of the five equal sublayers (SLs) of the inner plexiform layer. In both species, bipolar cells were most often seen to form their characteristic synaptic dyads with two amacrine cells. In some cases, however, the dyads were directed to one amacrine and one ganglion cell dendrite. This type of synapse was unevenly distributed within the inner plexiform layer with the highest occurrence in SL2 both in Bufo and Xenopus. In addition, SL4 contained also a high number of this type of synapse in Xenopus. In both species, we found no or few bipolar to ganglion cell synapses in the marginal sublayers (SLs 1 and 5). In Xenopus, 22% of the bipolar cell output synapses went onto ganglion cells, whereas in Bufo this was only 10%. We conclude that direct bipolar to ganglion cell information transfer exists also in frogs although its occurrence is not as obvious and regular as in mammals. The characteristic distribution of these synapses, however, suggests that specific type of the bipolar and ganglion cells participate in this process. These contacts may play a role in the formation of simple ganglion cell receptive fields.

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“…Stated another way, ganglion cells are more likely to be a third‐order neuron with GABAergic bipolar cells, whereas they are more likely to be a fourth‐order neuron with glutamatergic bipolar cells. Buzas et al (1996) reported that only 10–20% of the ribbon dyads in Bufo and Xenopus make direct contact with ganglion cells. This amount is a much smaller proportion compared with that reported for bipolar cells in retinas of urodele amphibians (Dowling and Werblin, 1969; Wong‐Riley, 1974; this report).…”

“…It is known that bipolar cells make ribbon synapses and amacrine cells make conventional synapses onto target cells in all vertebrate retinas so far studied (Kidd, 1962; Dowling and Boycott, 1966; Raviola and Raviola, 1967; Dowling, 1968; Dowling and Werblin, 1969; Witkovsky and Dowling, 1969; Dubin, 1970; Goldman and Fisher, 1978; Gabriel and Straznicky, 1993; Buzas et al, 1996). Despite a casual description of non‐ribbon synapses of bipolar cells in human retina by Allen (1969), the first extensive documentation of these synapses was made by Wong‐Riley in 1974 in tiger salamander retina, a finding later confirmed by Yang and Wang (1999) and Miller et al (2001).…”

“…Although non‐ribbon bipolar synapses have not been reported in any other amphibian, specifically Rana (Dowling, 1968; Dubin, 1970), Xenopus (Goldman and Fisher, 1978; Buzas et al, 1996), Bufo (Gábriel and Straznicky, 1993; Buzas et al, 1996), and Necturus (Dowling and Werblin, 1969), recently, large postsynaptic processes at non‐ribbon synapses of bipolar cells have been reported in Macaque monkey, rabbit, mouse, and marmoset (Grünert et al, 2002). The postsynaptic processes in monkey were immunoreactive for the kainate receptor GluR6/7.…”

Synaptology of the inner plexiform layer in the anuran retina

“…In frogs, the bipolar cells are mixed, receiving inputs from both rods and cones (Dowling, 1968;. In the IPL, in about 70% of the cases both of the postsynaptic profiles at a ribbon synapse derived from amacrine cells (Buzá s et al, 1996;Gá briel and Wilhelm, 1994;Goldman and Fisher, 1978;Zhu and Gibbins, 1997). This observation suggests a higher divergence of bipolar cell output to amacrine cells in frogs than in mammals.…”

Functional anatomy of the photoreceptor and second-order cell mosaics in the retina of Xenopus laevis

“…In recent years, evidence has accumulated that retinal ganglion cells in anurans receive a sizable direct input from BCs (Buzás et al 1996;Zhu and Gibbins 1997). However, we still do not know if all ganglion cell types receive equal amounts of direct BC inputs or not.…”