The gain of signaling in primary sensory circuits is matched to the stimulus intensity by the process of adaptation. Retinal neural circuits adapttovisual scene statistics, including the mean (background adaptation) and the temporal variance (contrast adaptation)ofthe light stimulus. The intrinsic propertiesof retinal bipolar cells and synapses contribute tobackground and contrast adaptation, butit isunclear whether both forms of adaptation depend on the same cellular mechanisms. Studies of bipolar cell synapses identified synaptic mechanisms of gain control, but the relevance of these mechanisms to visual processing is uncertain because of the historical focus on fast, phasic transmission rather than the tonic transmission evoked by ambient light. Here, we studied use-dependent regulation of bipolar cell synaptic transmission evoked by small, ongoing modulations of membrane potential (VM) in the physiological range. We made paired whole-cell recordings from rod bipolar (RB) and AII amacrine cellsinamouse retinal slice preparation. Quasi-white noise voltage commands modulated RBVMand evoked EPSCsinthe AII.Wemimicked changes in background luminanceorcontrast, respectively, by depolarizing theVMor increasing its variance.Alinear systems analysisof synaptic transmission showed that increasing either the mean or the variance of the presynaptic VM reduced gain. Further electrophysiological and computational analyses demonstrated that adaptation to mean potential resulted from both Ca channel inactivation and vesicle depletion, whereas adaptationto variance resulted from vesicle depletion alone. Thus, background and contrast adaptation apparently depend in part on a common synaptic mechanism.
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