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The Journal of Neuroscience, November 26, 2003, 23(34):10923-10933

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Cellular/Molecular
Sustained Ca²⁺ Entry Elicits Transient Postsynaptic Currents at a Retinal Ribbon Synapse

Joshua H. Singer and Jeffrey S. Diamond

Synaptic Physiology Unit, National Institutes of Health-National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892

Night (scotopic) vision is mediated by a distinct retinal circuit in which the light responses of rod-driven neurons are faster than those of the rods themselves. To investigate the dynamics of synaptic transmission at the second synapse in the rod pathway, we made paired voltage-clamp recordings from rod bipolar cells (RBCs) and postsynaptic AII and A17 amacrine cells in rat retinal slices. Depolarization of RBCs from -60 mV elicited sustained Ca²⁺ currents and evoked AMPA receptor (AMPAR)-mediated EPSCs in synaptically coupled amacrine cells that exhibited large, rapidly rising initial peaks that decayed rapidly to smaller, steady-state levels. The transient component persisted in the absence of feedback inhibition to the RBC terminal and when postsynaptic AMPA receptor desensitization was blocked with cyclothiazide, indicating that it reflects a time-dependent decrease in the rate of exocytosis from the presynaptic terminal. The EPSC waveform was similar when RBCs were recorded in perforated-patch or whole-cell configurations, but asynchronous release from RBCs was enhanced when the intraterminal Ca²⁺ buffer capacity was reduced. When RBCs were depolarized from -100 mV, inactivating, low voltage-activated (T-type channel-mediated) Ca²⁺ currents were evident. Although Ca²⁺ influx through T-type channels boosted vesicle release, as reflected by larger EPSCs, it did not make the EPSCs faster, indicating that activation of T-type channels is not necessary to generate a transient phase of exocytosis. We conclude that the time course of vesicle release from RBCs is inherently transient and, together with the fast kinetics of postsynaptic AMPARs, speeds transmission at this synapse.

Key words: ribbon synapse; rod bipolar cell; AII amacrine cell; retina; scotopic vision; AMPA receptor

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Received Aug 6, 2003; revised September 22, 2003; accepted September 24, 2003.

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