The Synaptic and Circuit Mechanisms Underlying a Change in Spatial Encoding in the Retina

• Repurposing of retinal circuits provides luminance-dependent computation
• Dendro-axonal gap junctions control rectification of cone bipolar synapse
• Spatial integration by retinal ganglion cells changes with luminance
• Interactions between parallel circuits control spatial integration

SummaryComponents of neural circuits are often repurposed so that the same biological hardware can be used for distinct computations. This flexibility in circuit operation is required to account for the changes in sensory computations that accompany changes in input signals. Yet we know little about how such changes in circuit operation are implemented. Here we show that a single retinal ganglion cell performs a different computation in dim light—averaging contrast within its receptive field—than in brighter light, when the cell becomes sensitive to fine spatial detail. This computational change depends on interactions between two parallel circuits that control the ganglion cell’s excitatory synaptic inputs. Specifically, steady-state interactions through dendro-axonal gap junctions control rectification of the synapses providing excitatory input to the ganglion cell. These findings provide a clear example of how a simple synaptic mechanism can repurpose a neural circuit to perform diverse computations.