Abstract
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 Ca2+ inflow through CaV1.3 (L-type) Ca2+ channels. We investigated the macroscopic (whole-cell) and elementary (cell-attached) properties of Ca2+ 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 Ca2+ 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 (P o: 0.024 in response to 500-ms depolarizing steps at ∼−18 mV). The value of P o was significantly larger (0.06) in the first 40 ms of membrane depolarization, which corresponds to the time when most Ca2+ channel openings occurred clustered in bursts (mean burst duration: 19 ms). Both the P o 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 Ca2+ channels per ribbon than basal cells. We propose that middle-turn IHCs finely-tune CaV1.3 Ca2+ channel gating in order to provide reliable information upon timing and intensity of lower-frequency sounds.
Highlights
In mammals, inner hair cells (IHCs) are responsible for the transduction of sound stimuli into an electrical signal, which is sent to the brain by afferent fibres
IHCs were held at their resting membrane potential, which was stepped to different test potentials
The sub-ms activation time constant of ICa in wholecell was comparable to the sub-ms activation of the ensemble average. These results indicate that the macroscopic ICa recorded from IHCs of the middle cochlear region can be sufficiently well described by the summed behavior of the single Ca2+ channel
Summary
Inner hair cells (IHCs) are responsible for the transduction of sound stimuli into an electrical signal, which is sent to the brain by afferent fibres. IHCs and afferent nerve fibres in the lower-frequency regions (apical and middle cochlear turns in gerbils: , a few kHz) show tuning and phase-locking to sound stimulation [11], enabling a time code of frequency to allow frequency discrimination and sound localization based on the detection of interaural time differences [13,14]. This requires the IHC receptor potentials to be graded to sound intensity, similar to basal cells, and have a phasic (a.c.) component representing the sound frequency [15]. This cochlear region represents a close match with the frequency range present in the apical coil of the more commonly used mouse (,3 kHz [17])
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