Retinal Cx36 gap junctions in the inner and outer plexiform layers differentially control visual thresholds.
Gap junctions are an important component of signal communication in sensory systems. In the retina, connexin 36 (Cx36) gap junctions integrate visual signals over space and time. However, we do not understand how Cx36 gap junctions in the inner- and outer-retina govern visual thresholds under dim light conditions. Here we address this question using transgenic mouse models, a state-of-the-art operant behavioral assay, and psychophysical modelling. Visual thresholds with Ganzfeld illumination decreased steeply (-2 log/dec) with flash durations < 0.5 s, reaching an asymptotic value of ~2 x 10-4 ph/m2/s with longer flashes. Temporal summation and photon noise modelled under Signal Detection Theory account for the observed thresholds. Removal of outer-retinal Cx36 lowers visual thresholds by 2.6-fold. Nested model analysis suggests that the probability of transmission of single photon signals between rods and bipolar cells increases in the absence of CX36 gap junctions between rods and cones. Removal of Cx36 in both the inner and outer retina increases visual thresholds by 16.5-fold, consistent with a loss of spatial-averaging and reduction of neural noise by Cx36 in the inner-retina. We conclude that both inner- and outer-retinal Cx36 control visual thresholds under dim light conditions, but in distinct ways. Outer-retinal Cx36 increases thresholds, perhaps in a necessary tradeoff that provides rod signals access to the alternative rod-cone pathway, whereas inner-retinal Cx36 decreases thresholds by increasing spatial-integration, more than compensating for outer retina losses.