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. 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.
Bibliographical noteFunding Information:
We thank Gautam Awatramani, Will Grimes, Gabe Murphy, and Max Turner for suggestions on an earlier version of the manuscript; Mike Ahlquist, Mark Cafaro, Shellee Cunnington, and Paul Newman for outstanding technical support; Josh Singer for providing Gjd2-EGFP mice and Rachel Wong for providing Gus8.4-EGFP mice; and members of the Rieke lab for helpful feedback throughout this project. This work was supported by NIH (EY11850 to F.R.) and the Howard Hughes Medical Institute (F.R.).