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Journal of Neuroscience, Vol 11, 3096-3110, Copyright © 1991 by Society for Neuroscience
Reversible inhibition of voltage-dependent outer hair cell motility and capacitance
J Santos-Sacchi
Laboratory of Otolaryngology, UMDNJ-New Jersey Medical School, Newark 07103.
Outer hair cells (OHC) from the organ of Corti are capable of fast
voltage-induced length changes (Santos-Sacchi and Dilger, 1988), suggesting
that an associated voltage sensor should reside in the OHC plasma membrane.
Voltage-dependent mechanical responses and nonlinear charge movement of
isolated OHCs from the guinea pig were analyzed using the whole-cell
voltage-clamp technique. Ionic currents in the cells were blocked.
Nonlinear voltage-dependent charge movement or, correspondingly,
voltage-dependent capacitance was measured with step or AC analysis. OHC
movements were measured either from video or using a differential
photodiode technique. Maximum charge movements up to 2.5 pC were measured
in OHCs from the low-frequency region of the cochlea. Both AC and step
analyses indicated a peak nonlinear capacitance of 16- 17 pF. The voltage
dependence was fit to a Boltzmann relation with the step analysis
indicating a maximum nonlinear capacitance at -23 mV step potential from a
holding potential of about -120 mV, and AC analysis indicating a maximum at
a holding potential near -40 mV. AC analysis probably provides a more
accurate evaluation of voltage dependence. Measures of OHC motility
magnitude versus voltage follow the nonlinear capacitance-voltage function
obtained from AC measures. Treatment of the cells with gadolinium ions
(0.5-1 mM) blocked OHC motility. This treatment also produced a shift of
the nonlinear capacitance function along the voltage axis in the
depolarizing direction, which can be explained by membrane surface charge
screening. However, maximum capacitance was reduced as well and may
correspond to the reduction or abolition of OHC motility in response to
gadolinium treatment. Gadolinium effects were reversible. Nonlinear
capacitance is not a function of membrane deformation due to length
changes, since removal of OHC cytosol via the patch pipette abolished
longitudinal movement but did not reduce nonlinear charge movement. It is
interesting to note that the nonlinear capacitance will dynamically
influence the time constant of the OHC during acoustically evoked receptor
potential generation.
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