Electrical Coupling of Heterotypic Ganglion Cells in the Mammalian Retina

Abstract

Electrical coupling has been reported to occur only between homotypic retinal ganglion cells, in line with the concept of parallel processing in the early visual system. Here, however, we show reciprocal correlated firing between heterotypic ganglion cells in multielectrode array recordings during light stimulation in retinas of adult guinea pigs of either sex. Heterotypic coupling was further confirmed via tracer spread after intracellular injections of single cells with neurobiotin. Both electrically coupled cell types were sustained ON center ganglion cells but showed distinct light response properties and receptive field sizes. We identified one of the involved cell types as sustained ON ␣-ganglion cells. The presence of electrical coupling between heterotypic ganglion cells introduces a network motif in which the signals of distinct ganglion cell types are partially mixed at the output stage of the retina.

Feedback from retinal ganglion cells to the inner retina

“…Taken together, consistent with our model predictions, these data provide direct evidence that ganglion cells can drive negative feedback signaling in the inner retina besides previously described excitatory interactions via gap junction networks (Brivanlou et al, 1998;Mastronarde, 1983;Meister et al, 1995;Nath and Schwartz, 2017;Puller et al, 2020;Roy et al, 2017;Trong and Rieke, 2008;Völgyi et al, 2013).…”

“…The circuit model thus predicts that faster enhancing effects between proximal ganglion cells can arise from 7 direct coupling, whereas slower suppressing effects between distal cells should be mediated by indirect coupling, presumably via inhibitory amacrine cells in the inner retina (Greschner et al, 2016;Naka, 1988, 1990). The prediction on the positive couplings is well supported by previous studies (Brivanlou et al, 1998;Cocco et al, 2009;Nath and Schwartz, 2017;Pillow et al, 2008;Puller et al, 2020), but direct experimental evidence is still lacking on the slow negative coupling between ganglion cells over a long distance.…”

“…Ganglion cells are, however, part of extensive gap junction networks in the retina (Bloomfield and Cook and Becker, 1995;Puller et al, 2020). While retinal neurons are generally coupled among those of the same type, ganglion cells also form electrical synapses with amacrine cells (Nath and Schwartz, 2017;Roy et al, 2017;Völgyi et al, 2009).…”

“…Different architectures of the gap junction networks are indeed responsible for distinct firing patterns among ganglion cells over multiple time-scales. For example, direct couplings between ganglion cells underlie their nearly synchronous activity within a few milliseconds, whereas indirect couplings via amacrine cells are suggested to mediate more broadly correlated activity of ganglion cells over tens to hundreds of milliseconds (Brivanlou et al, 1998;Mastronarde, 1983;Meister et al, 1995;Nath and Schwartz, 2017;Puller et al, 2020;Roy et al, 2017;Trong and Rieke, 2008;Völgyi et al, 2013). On the other hand, inhibitory effects will be obtained if ganglion cells send feedback signals to amacrine cells through electrical synapses, while the amacrine cells in turn inhibit the ganglion cells or presynaptic bipolar cells through chemical synapses (Greschner et al, 2016;Kenyon and Marshak, 1998;Naka, 1988, 1990).…”

An offset ON–OFF receptive field is created by gap junctions between distinct types of retinal ganglion cells

“…Heterotypic RGC coupling was also recently identified in the guinea pig using multi-electrode array recordings and morphological tracing with Neurobiotin 32 . The coupled RGCs in the guinea pig study were both ON sustained cells – one of them was the ON alpha – so heterotypic coupling in that system does not mix ON and OFF signals.…”