Retinal bipolar cells borrow excitability from electrically coupled inhibitory interneurons to amplify excitatory synaptic transmission

Bipolar cells (BCs) carry visual information from photoreceptors in the outer retina to retinal ganglion cells (RGCs) in the inner retina. Most BCs lack voltage-gated Na+ (NaV) channels and action potentials. Instead, voltage signals spread passively from input to output synapses. Despite this, we find that blocking NaV channels reduces synaptic output of On-cone bipolar cells (On-CBCs). These cells borrow NaV channel-mediated excitability from electrically coupled A2 amacrine cells to amplify excitatory output, allowing voltage changes to be transmitted more effectively to downstream RGCs in dim light. Because neighboring On-CBCs form electrical synapses onto the same A2 cell, a spatially adjacent group of On-CBCs is more effective than a dispersed set for recruiting A2 cell electrical excitability and driving post-synaptic RGCs. This mechanism filters the neural representation of an image to highlight shapes over spatially uncorrelated stimuli, a sophisticated feature detection property that is well-suited for object recognition.