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The dynamic displacement of the semicircular canal cupula and modulation of afferent nerve discharge were measured simultaneously in response to physiological stimuli in vivo. The adaptation time constant(s) of normal cupulae in response to step stimuli averaged 36 s, corresponding to a mechanical lower corner frequency for sinusoidal stimuli of 0.0044 Hz. For stimuli equivalent to 40–200 deg/s of angular head velocity, the displacement gain of the central region of the cupula averaged 53 nm per deg/s. Afferents adapted more rapidly than the cupula, demonstrating the presence of a relaxation process that contributes significantly to the neural representation of angular head motions by the discharge patterns of canal afferent neurons. We also investigated changes in time constants of the cupula and afferents following detachment of the cupula at its apex—mechanical detachment that occurs in response to excessive transcupular endolymph pressure. Detached cupulae exhibited sharply reduced adaptation time constants (300 ms–3 s, n = 3) and can be explained by endolymph flowing rapidly over the apex of the cupula. Partially detached cupulae reattached and normal afferent discharge patterns were recovered 5–7 h following detachment. This regeneration process may have relevance to the recovery of semicircular canal function following head trauma.

Cochlear outer hair cells (OHCs) are fast biological motors that serve to enhance the vibration of the organ of Corti and increase the sensitivity of the inner ear to sound. Exactly how OHCs produce useful mechanical power at auditory frequencies, given their intrinsic biophysical properties, has been a subject of considerable debate. To address this we formulated a mathematical model of the OHC based on first principles and analyzed the power conversion efficiency in the frequency domain. The model includes a mixture-composite constitutive model of the active lateral wall and spatially distributed electro-mechanical fields. The analysis predicts that: 1) the peak power efficiency is likely to be tuned to a specific frequency, dependent upon OHC length, and this tuning may contribute to the place principle and frequency selectivity in the cochlea; 2) the OHC power output can be detuned and attenuated by increasing the basal conductance of the cell, a parameter likely controlled by the brain via the efferent system; and 3) power output efficiency is limited by mechanical properties of the load, thus suggesting that impedance of the organ of Corti may be matched regionally to the OHC. The high power efficiency, tuning, and efferent control of outer hair cells are the direct result of biophysical properties of the cells, thus providing the physical basis for the remarkable sensitivity and selectivity of hearing., Author Summary The sense of hearing is exquisitely sensitive to quiet sounds due to active mechanical amplification of sound-induced vibrations by hair cells within the inner ear. In mammals, the amplification is due to the motor action of “outer hair cells” that feed mechanical power into the cochlea. How outer hair cells are able to amplify vibrations at auditory frequencies has been somewhat of a paradox given their relatively large size and leaky electrical properties. In the present work, we examined the power conversion efficiency of outer hair cells based on first principles of physics. Results show that the motor is highly efficient over a broad range of auditory frequencies. Results also show that the motor is likely controlled by the brain in a way that allows the listener to focus attention on specific frequencies, thus improving the ability to distinguish sounds of interest in a noisy environment.

Microvilli (stereocilia) projecting from the apex of hair cells in the inner ear are actively motile structures that feed energy into the vibration of the inner ear and enhance sensitivity to sound. The biophysical mechanism underlying the hair bundle motor is unknown. In this study, we examined a membrane flexoelectric origin for active movements in stereocilia and conclude that it is likely to be an important contributor to mechanical power output by hair bundles. We formulated a realistic biophysical model of stereocilia incorporating stereocilia dimensions, the known flexoelectric coefficient of lipid membranes, mechanical compliance, and fluid drag. Electrical power enters the stereocilia through displacement sensitive ion channels and, due to the small diameter of stereocilia, is converted to useful mechanical power output by flexoelectricity. This motor augments molecular motors associated with the mechanosensitive apparatus itself that have been described previously. The model reveals stereocilia to be highly efficient and fast flexoelectric motors that capture the energy in the extracellular electro-chemical potential of the inner ear to generate mechanical power output. The power analysis provides an explanation for the correlation between stereocilia height and the tonotopic organization of hearing organs. Further, results suggest that flexoelectricity may be essential to the exquisite sensitivity and frequency selectivity of non-mammalian hearing organs at high auditory frequencies, and may contribute to the "cochlear amplifier" in mammals.

Somatic measurements of whole-cell capacitance are routinely used to understand physiologic events occurring in remote portions of cells. These studies often assume the intracellular space is voltage-clamped. We questioned this assumption in auditory and vestibular hair cells with respect to their stereocilia based on earlier studies showing that neurons, with radial dimensions similar to stereocilia, are not always isopotential under voltage-clamp. To explore this, we modeled the stereocilia as passive cables with transduction channels located at their tips. We found that the input capacitance measured at the soma changes when the transduction channels at the tips of the stereocilia are open compared to when the channels are closed. The maximum capacitance is felt with the transducer closed but will decrease as the transducer opens due to a length-dependent voltage drop along the stereocilium length. This potential drop is proportional to the intracellular resistance and stereocilium tip conductance and can produce a maximum capacitance error on the order of fF for single stereocilia and pF for the bundle.