Nanodomain Control of Exocytosis Is Responsible for the Signaling Capability of a Retinal Ribbon Synapse

Abstract

Primary sensory circuits encode both weak and intense stimuli reliably, requiring that their synapses signal over a wide dynamic range. In the retinal circuitry subserving night vision, processes intrinsic to the rod bipolar (RB) cell presynaptic active zone (AZ) permit the RB synapse to encode signals generated by the absorption of single photons as well as by more intense stimuli. In a study using an in vitro slice preparation of the mouse retina, we provide evidence that the location of Ca channels with low open probability within nanometers of the release sites is a critical determinant of the physiological behavior of the RB synapse. This gives rise to apparent one-to-one coupling between Ca channel opening and vesicle release, allowing presynaptic potential to be encoded linearly over a wide dynamic range. Further, it permits a transition from univesicular to multivesicular release (MVR) when two Ca channels/AZ open at potentials above the threshold for exocytosis. MVR permits small presynaptic voltage changes to elicit postsynaptic responses larger than quantal synaptic noise.