Theory of electrically driven shape changes of cochlear outer hair cells

P. Dallos, R. Hallworth, B. N. Evans

Research output: Contribution to journalArticle

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Abstract

1. A theory of cochlear outer hair cell electromotility is developed and specifically applied to somatic shape changes elicited in a microchamber. The microchamber permits the arbitrary electrical and mechanical partitioning of the outer hair cell along its length. This means that the two partitioned segments are stimulated with different input voltages and undergo different shape changes. Consequently, by imposing more constraints than other methods, experiments in the microchamber are particularly suitable for testing different theories of outer hair cell motility. 2. The present model is based on simple hypotheses. They include a distributed motor associated with the cell membrane or cortex and the assumption that the displacement generated by the motor is related to the transmembrane voltage across the associated membrane element. It is expected that the force generated by the motor is counterbalanced by an elastic restoring force indigenous to the cell membrane and cortex, and a tensile force due to intracellular pressure. It is assumed that all changes take place while total cell volume is conserved. The above elements of the theory taken together permit the development of qualitative and quantitative predictions about the expected motile responses of both partitioned segments of the cell. Only a DC treatment is offered here. 3. Both a linear motor and an expanded treatment that incorporates a stochastic molecular motor model are considered. The latter is represented by a two- state Boltzmann process. We show that the linear motor treatment is an appropriate extrapolation of the stochastic motor theory for the case of small voltage driving signals. Comparison of experimental results with model responses permits the estimation of model parameters. Good match of data is obtained if it is assumed that the molecular motors undergo conformational length changes of 0.7-1.0 nm, that they have an effective displacement vector at approximately -20° with the long axis of the cell, and that their linear density is ~80/μm. 4. An effort is made to parcel out motile response components that are a direct consequence of the motor action from those that are mediated by cytoplasmic pressure changes brought about by the concerted action of the motors. We show that pressure effects are of minor importance, and thus rule out models that rely on radial constriction/expansion-mediated internal pressure change as the primary cause of longitudinal motility. 5. As a consequence of the interaction between the Boltzmann process and the mechanical characteristics of the cell, the electromotile response is asymmetric. It is shown that axial displacement is always greater in the contraction direction, whereas radial displacement is always greater in the expansion direction. These results are in full accord with experimental observations. The treatment is extended to consider the effects on motility of changing membrane potential, and its significant influence on the cell's nonlinear responsiveness is demonstrated. We show that modest depolarization produces a linearization of the response, whereas severe depolarization results in a reversal of response asymmetry. 6. The relevance of the results to putative in vivo outer hair cell motility is considered.

Original languageEnglish (US)
Pages (from-to)299-323
Number of pages25
JournalJournal of Neurophysiology
Volume70
Issue number1
DOIs
StatePublished - Jan 1 1993

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

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