Homologous amacrine to amacrine gap junction coupling serves communication between neighbour OFF alpha retinal ganglion cells.

Multiplexed visual coding by retinal ganglion cells (RGCs) has gained much support. Mouse transient OFF alpha RGCs (tOFFα RGCs) are excellent subjects to study this issue as they form direct RGC-RGC gap junctions (GJs) that serve spike synchronization, population coding and likely information multiplexing. In addition, tOFFα RGCs maintain GJs with a population of wide-field amacrine cells (ACs) that have been suspected to mediate an additional, loose medium-scale correlation of tOFFα RGC spikes. However, the spatial and temporal constraints of the GJ-mediated AC-RGC signalling have yet to be tested directly via a combination of morphological and functional approaches. Here we show that AC-mediated medium-scale spike correlations are strongly related to spike bursts. On the other hand, our data also show that coupled ACs' somata form spatially separated clusters each overlapping with only a single tOFFα RGC dendritic arbour suggesting the existence of GJ-coupled tOFFα RGC-AC functional units. This finding seemingly argues against the hypothesis that ACs distribute common noise for burst-based medium-scale RGC spike correlations. However, we also found a high incidence of AC-AC GJ connections thereby forming the morphological substrate for the interconnection of functional units to correlate spike bursts on a medium time scale. These data thus suggest that besides encoding visual information by a single cell, tOFFα RGCs utilize RGC-RGC GJs to directly connect RGCs as well as AC-AC GJs to interconnect tOFFα RGC functional units to mediate two forms of population codes via precise spike synchronization and loose burst correlations, respectively. KEY POINTS: Approach detector retinal ganglion cells (RGCs) and their electrically coupled amacrine cells (ACs) show morphological attributes of functional units. These coupled ACs and RGCs share their main excitatory drive. RGC-AC gap junctions underlie the generation of RGC action potential bursts. AC-AC gap junctions interconnect neighbouring RGC functional units to correlate spike bursts and underlie medium-scale spike correlations. These results broaden our understanding of feature detection mechanisms in the retinal circuitry, the prerequisite of next generation retina prostheses.