Retinal Electrical Synapses Prime Neighbor Cells to Amplify Looming Related Threat Signals and Support Escape Behavior.

Rapid detection of looming objects is essential for survival, yet single retinal ganglion cells have receptive fields that are smaller than many behaviorally relevant looming stimuli. This mismatch raises the question of how the retina represents an expanding threat as it moves beyond the receptive field of a single neuron. Here, we show that gap junctions extend looming-related activity across a coupled network of transient OFF-alpha retinal ganglion cells. Using multiscale electrophysiology, genetic and pharmacological perturbations, and behavioral assays, we found that looming stimuli recruit neighboring retinal ganglion cells through electrical synapses. Targeted recordings showed that activation of one transient OFF-alpha cell can prime neighboring cells, allowing them to respond when the expanding edge reaches their receptive fields. Disrupting gap junction coupling reduced retinal population recruitment, altered looming-evoked response patterns in the superior colliculus, and impaired escape behavior, while leaving visual acuity, depth perception intact, and lateral-motion responses intact. These findings show that electrical synapses transform local looming responses in the retina into a coordinated population signal that extends beyond single receptive fields and supports escape behavior.