A hierarchical electrical synaptic circuit mechanism for integrative parallel visual processing in the retina.

Parallel visual processing begins with retinal bipolar cells, traditionally regarded as independent chemical synaptic channels. However, the circuit-level synaptic integration of chemical and electrical synapses within this network remains unclear. Using dual patch-clamp recordings and two-photon imaging in whole-mount retina, we systematically characterized synaptic transmission across 13 mouse and 2 human cone bipolar cell (CBC) types, revealing two distinct modes: a fast, direct chemical pathway and a slower, serial electrical-chemical circuit among both ON and OFF CBCs. In mice, the slow mode generates spatially dispersed glutamate "clouds" that facilitate integration across CBC types. We discovered specific "driver" CBCs that distribute robust, sustained signals through a hierarchical, functionally rectified network, enhancing sensitivity to small, low-contrast stimuli in downstream retinal cells and thalamic neurons in awake mice. Our findings challenge the classical view of independent CBC channels, revealing an integrative, hierarchical electrical-chemical synaptic architecture that enhances visual detection and coding efficiency.