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Tonotopic variations of calcium signalling in turtle auditory hair cells

A. J. Ricci, M. Gray-Keller and R. Fettiplace

1. Turtle cochlear hair cells are electrically tuned by a voltage-dependent Ca²⁺ current and a Ca²⁺-dependent K⁺ current (I_BK(Ca)). The effects of intracellular calcium buffering on electrical tuning were studied in hair cells at apical and basal cochlear locations tuned to 100 and 300 Hz, respectively.

2. Increasing the intracellular BAPTA concentration changed the hair cell's resonant frequency little, but optimized tuning at more depolarized membrane potentials due to a positive shift in the half-activation voltage (V_½) of the I_BK(Ca).

3. The shift in V_½ depended similarly on BAPTA concentration in basal and apical hair cells despite a 2·4-fold difference in the size of the Ca²⁺ current at the two positions. The Ca²⁺ current amplitude increased exponentially with distance along the cochlea.

4. Comparison of V_½ values and tuning properties using different BAPTA concentrations with values measured in perforated-patch recordings gave the endogenous calcium buffer as equivalent to 0·21 mM BAPTA in low-frequency cells, and 0·46 mM BAPTA in high-frequency cells.

5. High conductance Ca²⁺-activated K⁺ (BK_Ca) channels recorded in inside-out membrane patches were 2-fold less Ca²⁺ sensitive in high-frequency than in low-frequency cells.

6. Confocal Ca²⁺ imaging using the fluorescent indicator Calcium Green-1 revealed about twice as many hotspots of Ca²⁺ entry during depolarization in high-frequency compared to low-frequency hair cells.

7. We suggest that each BK_Ca channel is gated by Ca²⁺ entry through a few nearby Ca²⁺ channels, and that Ca²⁺ and BK_Ca channels occupy, at constant channel density, a greater fraction of the membrane area in high-frequency cells than in low-frequency cells.

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