Variation of membrane properties in hair cells isolated from the turtle cochlea.

Abstract

SUMMARY1. Hair cells were enzymatically isolated from identified regions of the turtle basilar papilla and studied with the patch-electrode technique. The experimental aim was to relate the resonance properties seen during current injection to the membrane currents measured in the same cell under whole-cell voltage clamp.2. Solitary hair cells had resting potentials of about -50 mV, and produced a damped oscillation in membrane potential at the onset and termination of a small current step; the resonant frequency varied from 9 to 350 Hz between cells, and was correlated with the region of papilla from which a cell had been isolated. The inferred frequency map was consistent with the tonotopic arrangement described previously in the intact papilla. J. J. ART AND R. FETTIPLACE K+ current, the Ca2+ current was activated by small depolarizations from the resting potential, and over this voltage range it was about five to ten times smaller than the K+ current. Its activation was more rapid than the fastest outward currents in high-frequency cells.8. The inward current could also be carried by Ba2+, which when substituted for external Ca2+ blocked the K+ current. Measurements on cells with resonant frequencies of 13-240 Hz indicated that the peak Ba2+ current increased systematically with resonant frequency.9. Manipulations such as external addition of Cd2+ which would be expected to reduce or abolish the Ca2+ current also blocked the K+ current, consistent with a previous suggestion (Lewis & Hudspeth, 1983b) that the hair-cell K+ conductance is gated by changes in intracellular Ca2+.10. Small steady depolarizations caused a pronounced increase in current fluctuations. The spectral density of the fluctuations in a given cell could be well fitted by the sum of two Lorentzians with half-power frequencies differing by an order of magnitude.11. Both half-power frequencies changed with the resonant frequency of the hair cell, and the lower half-power frequency was consistent with that predicted from the time constant of the current relaxation. The variance-to-mean ratio for the fluctuations was about 1 pA in all cells. It is suggested the the fluctuations are dominated by the opening and closing of the K+ channels, and that the intrinsic kinetics of these channels differ in cells with different resonant frequencies.12. Single K+ channels recorded in the cell-attached mode could be opened by depolarizations of the membrane under the patch electrode. At the start and end of a depolarizing step, the probability of channel opening rose and fell with an exponential time course, the time constant varying from 2 to 20 ms in different cells.13. The results support the following conclusions: (i) the resonance behaviour and tuning of turtle cochlear hair cells are governed by the interplay of membrane Ca2+and K+ conductances; (ii) the resonant frequency is determined by the characteristics of the K+ conductance, an increase in frequency being achieved largely by faster kinetics, but also to some extent by an increase in the size of ...

The roles of the external, middle, and inner ears in determining the bandwidth of hearing

“…In mammals, tonotopicity originates in the spatially graded BM stiffness, which directly determines the passive frequency tuning of local BM vibrations (29) and, less directly, the active frequency tuning of the BM and auditory-nerve fibers innervating adjacent inner hair cells (31, 32, ʈ). In turtles, tonotopicity results largely from the electrical properties of hair cells, which also are spatially graded (33,34). Whatever its origin, tonotopicity confines cochlear responses to a well defined frequency range determined by the characteristic frequencies (CFs) of the auditory-nerve fibers innervating the extreme apical and basal sites of the cochlea.…”

“…51 with 52, pp. [34][35], the bandwidths of middle-ear transmission and cochlear analysis may have been subsequently optimized by iterative accommodation to each other's performance to meet behavioral requirements while avoiding extending either one unnecessarily (and perhaps wastefully). It will be of special interest to ascertain whether the relatively low high-frequency cutoff of hearing in chinchillas and humans was brought about by parallel evolutionary reductions in the bandwidths of both the cochlea and middle-ear transmission, which allowed ultrasonic hearing in their ancestors (1).…”

The Role of BKCa Channels in Electrical Signal Encoding in the Mammalian Auditory Periphery

“…In particular, BK Ca channels, which are largeconductance, voltage-and Ca 2ϩ -dependent K ϩ channels, play a prominent role in determining the AP phenotype in many neurons (Vergara et al, 1998;Shao et al, 1999;Faber and Sah, 2003). In nonmammalian auditory hair cells, BK Ca contributes to electrical frequency tuning in the absence of APs (Art and Fettiplace, 1987;Fettiplace and Fuchs, 1999). However, less is known about the impact of BK Ca on electrical signaling in other nonspiking cells, such as retinal neurons (Sakaba et al, 1997;Mitra and Slaughter, 2002) or mechanosensory hair cells of the mammalian ear, despite strong expression of BK Ca in these cells (Skinner et al, 2003;Vigh et al, 2003).…”

Exploring the Role of Mechanotransduction Activation and Adaptation Kinetics in Hair Cell Filtering Using a Hodgkin-Huxley Approach

“…The number of both calcium and potassium channels increases tonotopically [1,16]. Additionally, the kinetics of the BK channels decrease as frequency increases [1,16]. Electrical resonance does not appear to translate to mammalian hair cells where the presence of intrinsic tuning mechanisms remains to be described.…”

“…Lower frequency resonances incorporate additional conductances [8]. The number of both calcium and potassium channels increases tonotopically [1,16]. Additionally, the kinetics of the BK channels decrease as frequency increases [1,16].…”