Hierarchical retinal computations rely on hybrid chemical-electrical signaling

Bipolar cells (BCs) are integral to the retinal circuits that extract diverse features from the visual environment. They bridge photoreceptors to ganglion cells, the source of retinal output. Understanding how such circuits encode visual features requires an accounting of the mechanisms that control glutamate release from bipolar cell axons. Here, we demonstrate orientation selectivity in a specific genetically identifiable type of mouse bipolar cell-type 5A (BC5A). Their synaptic terminals respond best when stimulated with vertical bars that are far larger than their dendritic fields. We provide evidence that this selectivity involves enhanced exci-tation for vertical stimuli that requires gap junctional coupling through connexin36. We also show that this orientation selectivity is detectable postsynaptically in direction-selective ganglion cells, which were not pre-viously thought to be selective for orientation. Together, these results demonstrate how multiple features are extracted by a single hierarchical network, engaging distinct electrical and chemical synaptic pathways.

Automated summary

Bipolar cells are crucial in extracting diverse features from the visual environment and connecting photoreceptors to ganglion cells. In this study, we found that a specific type of mouse bipolar cell, BC5A, exhibits orientation selectivity. These cells' synaptic terminals respond best to vertical stimuli that are larger than their dendritic fields. This selectivity involves increased excitation for vertical stimuli, which requires gap junctional coupling through connexin36. Interestingly, we also discovered that this orientation selectivity can be detected in direction-selective ganglion cells, which were previously not thought to be selective for orientation. These findings demonstrate how a hierarchical network can extract multiple features using distinct electrical and chemical synaptic pathways.