Components and Properties of the G3 Ganglion Cell Circuit in the Rabbit Retina

The visual processing stream as it emanates from the vertebrate retina consists of numerous parallel pathways carried by ≈15 types of ganglion cell (Dacey, 1999; Masland, 2001; Wassle, 2004). The dendritic fields of neighboring ganglion cells of a given type are positioned in a mosaic so as to sample the visual scene completely. Each individual ganglion cell is a portion of a retinal circuit whose characteristics are differentiated from those of other ganglion cell types in large part by their synaptic contacts—which of the dozen or so bipolar cell types relays the output of the photoreceptor to them and which of the 30 or more amacrine cells synapse upon these bipolar cells, the ganglion cell itself, or other amacrine cells. Identification of these repeating cell assemblies is a major step in unraveling the function of the retina and early vision. It has recently become clear that many, perhaps most, retinal ganglion cells are coupled via gap junctions to specific types of amacrine cell which play a part in determining the function of the circuit and also serve as a diagnostic tool for establishing cell type. The role of these coupled amacrine cells is not presently known. They may contribute to synchronized firing of the ganglion cells (Mastronarde, 1983; Brivanlou et al., 1998; Ackert et al., 2006) or in long-range interactions (Olveczky et al., 2007; Bloomfield and Volgyi 2007; Davenport et al., 2007). In this study, we exploit the existence of gap junctions which occur between ganglion cells and amacrine cells to identify two components of a previously unknown retinal circuit. Iontophoresis of the tracer Neurobiotin (Vector Laboratories, Burlingame, CA) into a regularly identifiable ganglion cell type also stains a mosaic of amacrine cells to which the ganglion cell is coupled. The fluorescent tracer Popro1 (Hoshi et al., 2006) also passed the gap junctions and therefore allowed direct staining with Neurobiotin of individual coupled amacrine cells. Although neither this ganglion cell type nor the amacrine cell to which it is coupled have previously been able to be targeted for systematic study, the ganglion cell resembles an orientation-biased cell reported by Amthor et al. (1989) and is perhaps a homolog of the mouse ganglion cell recently described by Kim et al. (2008) as sensitive to upward motion. This article describes the characteristic morphologies of this ganglion and amacrine cell pair, identifies the site and connexin type of the gap junctions, demonstrates that the gap junctions are under dynamic control, and also identifies some further synaptic members of this cell assembly.