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Journal of Neuroscience, Vol 12, 3291-3309, Copyright © 1992 by Society for Neuroscience
An active motor model for adaptation by vertebrate hair cells
JA Assad and DP Corey
Department of Neurobiology, Harvard Medical School, Boston, Massachusetts.
Bullfrog saccular hair cells adapt to maintained displacements of their
stereociliary bundles by shifting their sensitive range, suggesting an
adjustment in the tension felt by the transduction channels. It has been
suggested that steady-state tension is regulated by the balance of two
calcium-sensitive processes: passive "slipping" and active "tensioning."
Here we propose a mathematical model for an adaptation motor that regulates
tension, and describe some quantitative tests of the model. Slipping and
tensioning rates were determined at membrane potentials of -80 and +80 mV.
With these, the model predicts that the I(X) curve (relating bundle
displacement and channel open probability) should shift negatively by 124
nm when the cell is depolarized, with an exponential time course that is
slower on depolarization from -80 to +80 mV than on repolarization. This
was observed: on depolarization, the I(X) curve shifted by an average of
139 nm, and displayed the expected difference in rates at the two
potentials. Because the negative shift of the I(X) curve on depolarization
represents an increase in the tension on transduction channels, the model
also predicts this tension should cause an unrestrained bundle to pivot
negatively by 99 nm on depolarization. Such movement was observed using
high-resolution video microscopy; its amplitude was variable but ranged up
to about 100 nm, and its time course was asymmetric in the same way as that
of the I(X) curve shift. In additional comparisons, the active bundle
movements and I(X) curve shift exhibited a similar steady-state voltage
dependence, and were both reversibly abolished by reduced bath Ca2+ or by
the transduction channel blocker streptomycin. Lastly, among different
cells, the amplitude of the movement increased with the size of the
transduction current. Thus, a quantitative mechanical model for adaptation
also accounts for the observed mechanical behavior of the bundle,
suggesting that the same mechanism is responsible for both, and that
adaptation is mediated by an active, force-producing mechanism.
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