Circuit Functions of Gap Junctions in the Mammalian Retina

Gap junctions are abundant in the retina and examples have been reported for every major cell type. They provide an essential pathway in certain retinal circuits and form the substrate for signal averaging in others. At least four neuronal connexins are found in the mammalian retina and different cell types express specific connexins with different properties. Cone-to-cone coupling via Cx36 gap junctions improves the cone signal-to-noise ratio whereas rod/cone coupling, perhaps via heterotypic gap junctions, provides an alternative pathway for intermediate light intensities. The modulation of horizontal cell (HC) coupling changes the spatial profile of HC feedback to photoreceptors. In rabbit and cat retina, the axonless A-type HCs are extensively coupled via Cx50 gap junctions whereas the axon-bearing or B-type HCs of the mouse and rabbit retina have different coupling properties and may express Cx57. The primary output of the rod bipolar cell is to AII amacrine cells which are well-coupled, via Cx36 gap junctions, to form a signal averaging network for noisy signals in this high-gain rod pathway. In addition, the pathway from AII amacrine cells to ON cone bipolar cells passes via gap junctions, some of which may be heterotypic Cx36/Cx45 gap junctions. Many other amacrine cell types are also coupled via Cx36 or Cx45 gap junctions. Finally, as many as half of the ganglion cell types are coupled. This may occur directly to neighboring ganglion cells of the same type and/or to amacrine cells, which are often, but not exclusively, wide-field axon-bearing types. Ganglion cell coupling, via Cx36 or Cx45 gap junctions, may help to synchronize spike activity between neighboring cells of the same type. In general, the prevalence of gap junctions in the retina may occur because signal averaging and noise reduction are important strategies in the early steps of visual processing.