Burst activity and ultrafast activation kinetics of CaV1.3 Ca2+ channels support presynaptic activity in adult gerbil hair cell ribbon synapses

• Published in: The Journal of physiology Vol. 591; no. 16; pp. 3811 - 3820
• Main Authors: Zampini, Valeria, Johnson, Stuart L., Franz, Christoph, Knipper, Marlies, Holley, Matthew C., Magistretti, Jacopo, Masetto, Sergio, Marcotti, Walter
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 15-08-2013; Wiley Subscription Services, Inc; Blackwell Science Inc
• Subjects: Animals; Calcium Channels, L-Type - physiology; Gerbillinae; Hair Cells, Auditory, Inner - physiology; In Vitro Techniques; Kinetics; Neuroscience: Cellular/Molecular; Sodium - physiology; Synapses - physiology
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.2013.251272

Key points
• 
The transfer of sound information to the brain relies on the precise release of neurotransmitter from sensory inner hair cell (IHC) ribbon synapses.
• 
Neurotransmitter release from IHCs is triggered by Ca2+ entry mainly through one type of Ca2+ channel (CaV1.3).
• 
In this study we show that in near‐physiological conditions Ca2+ channels open very rapidly following a stimulus with a delay of about 50 μs.
• 
Despite the open probability of the Ca2+ channels being very low, they can switch to a burst‐like mode during a stimulus, maximizing Ca2+ influx into IHCs.
• 
These results help us to better understand how IHCs are able to accomplish high‐fidelity signal transfer at individual auditory ribbon synapses.
  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 (0.21 at −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.