Inhibition Controls Receptive Field Size, Sensitivity, and Response Polarity of Direction Selective Ganglion Cells Near the Threshold of Vision

Information about motion is encoded by direction-selective retinal ganglion cells (DSGCs). These cells reliably transmit this information across a broad range of light levels, spanning moonlight to sunlight. Previous work indicates that adaptation to low light levels causes heterogeneous changes to the direction tuning of ON-OFF (oo)DSGCs and suggests that superior-preferring ON-OFF DSGCs (s-DSGCs) are biased toward detecting stimuli rather than precisely signaling direction. Using a large-scale multi-electrode array, we measured the absolute sensitivity of ooDSGCs and found that s-DSGCs are ten-fold more sensitive to dim flashes of light than other ooDSGCs. We measured their receptive field sizes and found that s-DSGCs also have larger receptive fields than other ooDSGCs, however, the size difference does not fully explain the sensitivity difference. Using a conditional knockout of gap junctions and pharmacological manipulations, we demonstrate that GABA-mediated inhibition contributes to the difference in absolute sensitivity and receptive field size at low light levels, while the connexin36-mediated gap junction coupling plays a minor role. We further show that GABA-mediated inhibition masks the OFF response of ooDSGCs under scotopic conditions, restricting their responses to increases in light. These results reveal that GABAergic inhibition controls and differentially modulates the responses of ooDSGCs under scotopic conditions.\n\nSignificance StatementLight adaptation and parallel processing are two major functions of retina. Here we show that parallel processing is differentially regulated between photopic and scotopic conditions across DSGCs. This differential adaptation alters the absolute sensitivity and RF size of s-DSGCs relative to other ooDSGC types. These results point to novel mechanisms and possibly new circuit elements that shape retinal processing of motion under rod-mediated light levels.