Light-Induced Changes in Gap Junctional Coupling of OFF Alpha Ganglion Cell Arrays in Mouse Retina

Purpose: : To determine the effect of ambient light on the alpha ganglion-to-alpha ganglion cell (GC/GC) and alpha ganglion-to-amacrine cell (GC/AC) electrical and tracer coupling in the mouse retina.

Methods: : We obtained simultaneous extracellular recordings from neighboring OFF alpha cells under light- and dark-adapted conditions. Cross-correlation functions (CCF) for spontaneous spikes were then compared under the two light conditions. We used narrow and intermediate correlations to assess the coupling strength of GC/GC and GC/AC electrical synapses, respectively (Brivanlou et al. 1998). In a second cohort of retinas, the gap junction permeable tracer Neurobiotin was iontophoresed into targeted OFF alpha GC somata under dark- and light-adapted conditions. The number of coupled GCs and ACs labeled under the two light conditions was then compared.

Results: : As we have reported previously, OFF alpha cells in the mouse retina are coupled homologously to each other and heterologously to neighboring ACs. Consistent with this coupling pattern, we found that the spontaneous spiking of neighboring alpha GCs in dark-adapted retinas was correlated with CCFs showing both narrow and intermediate patterns of concerted activity. Light adaptation enhanced the intermediate correlated activity, but had little effect on narrow correlations. Further, we found that light adaptation increased the number of tracer-coupled GCs, but did not significantly increase the size of the GC/GC coupled field. This suggests that light adaptation did not result in recruitment of second tier GC neighbors. Interestingly, while light adaptation did not increase the number of tracer-coupled ACs found near an injected alpha GC, the field of coupled ACs was extended nearly two times that found in dark-adapted retinas.

Conclusions: : Our data indicate a light-induced modulation of coupling of OFF alpha GC arrays. Light produced an expansion of the field of tracer-coupled ACs, consistent with an increase in intermediate correlations of neighboring alpha GC activity. In contrast, light had little effect on the narrow spike correlations between alpha GC pairs and, likewise, had only a small effect on GC/GC tracer coupling. These differential effects suggest that while light modulates heterologous coupling between alpha GCs and ACs, it has only a minor effect on homologous coupling between neighboring alpha GCs in the mouse retina.