Fine Tuning of CaV1.3 Ca2+ channel properties in adult inner hair cells positioned in the most sensitive region of the Gerbil Cochlea

• Published in: PloS one Vol. 9; no. 11; p. e113750
• Main Authors: Zampini, Valeria, Johnson, Stuart L, Franz, Christoph, Knipper, Marlies, Holley, Matthew C, Magistretti, Jacopo, Russo, Giancarlo, Marcotti, Walter, Masetto, Sergio
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 2014; Public Library of Science (PLoS)
• Subjects: Acoustics; Animals; Basal cells; Behavioral sciences; Biology and Life Sciences; Body temperature; Brain research; Calcium channels; Calcium channels (L-type); Calcium channels (voltage-gated); Calcium Channels, L-Type - metabolism; Channel gating; Channel opening; Channels; Cochlea; Cochlea - cytology; Conductance; Deactivation; Depolarization; Exocytosis; Fibers; Gerbillinae; Hair; Hair cells; Hair Cells, Auditory, Inner - cytology; Hair Cells, Auditory, Inner - metabolism; Hearing; Immunohistochemistry; Inflow; Ions - chemistry; Laboratories; Latency; Membrane potential; Membrane Potentials; Neurosciences; Otolaryngology; Patch-Clamp Techniques; Physiology; Resistance; Rodents; Signal transmission; Sodium - metabolism; Sound; Synapses; Synapses - metabolism; Synaptic ribbons; Time constant; Transmitters
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0113750

Hearing relies on faithful signal transmission by cochlear inner hair cells (IHCs) onto auditory fibres over a wide frequency and intensity range. Exocytosis at IHC ribbon synapses is triggered by Ca(2+) inflow through Ca(V)1.3 (L-type) Ca(2+) channels. We investigated the macroscopic (whole-cell) and elementary (cell-attached) properties of Ca(2+) currents in IHCs positioned at the middle turn (frequency ∼ 2 kHz) of the adult gerbil cochlea, which is their most sensitive hearing region. Using near physiological recordings conditions (body temperature and a Na(+) based extracellular solution), we found that the macroscopic Ca(2+) current activates and deactivates very rapidly (time constant below 1 ms) and inactivates slowly and only partially. Single-channel recordings showed an elementary conductance of 15 pS, a sub-ms latency to first opening, and a very low steady-state open probability (Po: 0.024 in response to 500-ms depolarizing steps at ∼-18 mV). The value of Po was significantly larger (0.06) in the first 40 ms of membrane depolarization, which corresponds to the time when most Ca(2+) channel openings occurred clustered in bursts (mean burst duration: 19 ms). Both the Po and the mean burst duration were smaller than those previously reported in high-frequency basal IHCs. Finally, we found that middle turn IHCs are likely to express about 4 times more Ca(2+) channels per ribbon than basal cells. We propose that middle-turn IHCs finely-tune Ca(V)1.3 Ca(2+) channel gating in order to provide reliable information upon timing and intensity of lower-frequency sounds.