Electrical resonance of isolated hair cells does not account for acoustic tuning in the free-standing region of the alligator lizard's cochlea

Abstract

The cochlea of the alligator lizard is divided into two morphologically and physiologically distinct regions. In the "tectorial region," hair bundles of hair cells are draped by a tectorial membrane, whereas in the "free-standing region," hair bundles are said to be free-standing because there are no overlying tectorial structures. The acoustic tuning of the free-standing region depends at least in part on mechanical resonances of the hair bundles. In the turtle cochlea, in contrast, acoustic tuning depends in large part upon the electrical properties of the hair cells. We have investigated the electrical properties of hair cells isolated from the free-standing region of the alligator lizard's cochlea. When injected with steps of depolarizing current, these "free-standing hair cells" exhibited electrical resonances that were comparable in frequency and quality to electrical resonances in cochlear hair cells from turtles, chicks, and alligators, and in saccular hair cells from frogs and fish. In the lizard's free-standing hair cells, however, the electrical resonance frequencies (< 300 Hz) were a decade below the cells' acoustic characteristic frequencies (between 1 and 4 kHz), showing that the electrical resonance is not likely to contribute to acoustic tuning. The electrical resonances were not apparent at rest. The cells' resting potentials were significantly more negative than the activation voltage (approximately -40 mV) of the Ca(2+)-dependent K+ current upon which the electrical resonance has been shown to depend in other hair cells. At potentials more negative than -50 mV, an inwardly rectifying K+ conductance dominated. Because we observed no electrical tuning above 300 Hz, our results indirectly support a mechanical origin for acoustic tuning in the free-standing region of the alligator lizard cochlea. These results further show that acoustic tuning cannot be inferred solely from the electrical resonances of isolated hair cells.