Auditory information transfer to afferent neurons relies on precise triggering of neurotransmitter release at the inner hair cell (IHC) ribbon synapses by Ca2+ entry through CaV1.3 Ca2+ channels. Despite the crucial role of CaV1.3 Ca2+ channels in governing synaptic vesicle fusion, their elementary properties in adult mammals remain unknown. Using near-physiological recording conditions we investigated Ca2+ channel activity in adult gerbil IHCs. We found that Ca2+ channels are partially active at the IHC resting membrane potential (–60 mV). At –20 mV, the large majority (>70%) of Ca2+ channel first openings occurred with an estimated delay of about 50 μs in physiological conditions, with a mean open time of 0.5 ms. Similar to other ribbon synapses, Ca2+ channels in IHCs showed a low mean open probability (0.21at –20 mV), but this increased significantly (up to 0.91) when Ca2+ channel activity switched to a bursting modality. We propose that IHC Ca2+ channels are sufficiently rapid to transmit fast signals of sound onset and support phase-locking. Short-latency Ca2+ channel opening coupled to multivesicular release would ensure precise and reliable signal transmission at the IHC ribbon synapse.
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