Burst activity and ultrafast activation kinetics of CaV1.3 Ca2+ channels support presynaptic activity in adult gerbil hair cell ribbon synapses. (21st June 2013)

• Record Type: Journal Article
• Authors: Zampini, Valeria; Johnson, Stuart L.; Franz, Christoph; Knipper, Marlies; Holley, Matthew C.; Magistretti, Jacopo; Masetto, Sergio; Marcotti, Walter
• Is Part Of: Journal of physiology. Volume 591:Number 16(2013:Aug.)
• Page Start: 3811
• Page End: 3820
• Publication Date: 2013-06-21
• Subjects: Physiology -- Periodicals; 612.005
• DOI: 10.1113/jphysiol.2013.251272
• Languages: English
• ISSNs: 0022-3751

Abstract

<abstract abstract-type="main" xml:lang="en"> <title>Key points</title> <p> <list id="l1" list-type="simple"> <list-item> <label> </label> <p>The transfer of sound information to the brain relies on the precise release of neurotransmitter from sensory inner hair cell (IHC) ribbon synapses.</p> </list-item> <list-item> <label> </label> <p>Neurotransmitter release from IHCs is triggered by Ca<sup>2+</sup> entry mainly through one type of Ca<sup>2+</sup> channel (Ca<sub>V</sub>1.3).</p> </list-item> <list-item> <label> </label> <p>In this study we show that in near‐physiological conditions Ca<sup>2+</sup> channels open very rapidly following a stimulus with a delay of about 50 μs.</p> </list-item> <list-item> <label> </label> <p>Despite the open probability of the Ca<sup>2+</sup> channels being very low, they can switch to a burst‐like mode during a stimulus, maximizing Ca<sup>2+</sup> influx into IHCs.</p> </list-item> <list-item> <label> </label> <p>These results help us to better understand how IHCs are able to accomplish high‐fidelity signal transfer at individual auditory ribbon synapses.</p> </list-item> </list> </p> <p> <bold>Abstract </bold> Auditory information transfer to afferent neurons relies on precise triggering of neurotransmitter release at the inner hair cell (IHC) ribbon synapses by Ca<sup>2+</sup> entry through Ca<sub>V</sub>1.3 Ca<sup>2+</sup> channels. Despite the crucial role of Ca<sub>V</sub>1.3 Ca<sup>2+</sup> channels in governing synaptic vesicle fusion, their elementary properties in adult mammals remain unknown. Using near‐physiological recording conditions we investigated Ca<sup>2+</sup> channel activity in adult gerbil IHCs. We found that Ca<sup>2+</sup> channels are partially active at the IHC resting membrane potential (−60 mV). At −20 mV, the large majority (>70%) of Ca<sup>2+</sup> 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, Ca<sup>2+</sup> channels in IHCs showed a low mean open probability (0.21 at −20 mV), but this increased significantly (up to 0.91) when Ca<sup>2+</sup> channel activity switched to a bursting modality. We propose that IHC Ca<sup>2+</sup> channels are sufficiently rapid to transmit fast signals of sound onset and support phase‐locking. Short‐latency Ca<sup>2+</sup> channel opening coupled to multivesicular release would ensure precise and reliable signal transmission at the IHC ribbon synapse.</p> </abstract>