Nonlinear Spatiotemporal Integration by Electrical and Chemical Synapses in the Retina

Electrical and chemical synapses coexist in circuits throughout the CNS. Yet, it is not well understood how electrical and chemical synaptic transmission interact to determine the functional output of networks endowed with both types of synapse. We found that release of glutamate from bipolar cells onto retinal ganglion cells (RGCs) was strongly shaped by gap-junction-mediated electrical coupling within the bipolar cell network of the mouse retina. Specifically, electrical synapses spread signals laterally between bipolar cells, and this lateral spread contributed to a nonlinear enhancement of bipolar cell output to visual stimuli presented closely in space and time. Our findings thus (1) highlight how electrical and chemical transmission can work in concert to influence network output and (2) reveal a previously unappreciated circuit mechanism that increases RGC sensitivity to spatiotemporally correlated input, such as that produced by motion. •Gap junctions mediate lateral interactions across parallel ON bipolar cell circuits•These lateral interactions nonlinearly shape glutamate release from bipolar cells•Bipolar cell synaptic output is preferentially enhanced for low contrast stimuli•Nonlinear lateral interactions increase retinal ganglion cell sensitivity to motion Kuo et al. find that electrical and chemical synaptic transmission work in concert to control glutamate release from retinal ON cone bipolar cells. This interaction enhances retinal ganglion cell sensitivity to visual inputs with strong spatiotemporal correlations, such as motion.