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The Journal of Neuroscience, October 31, 2007, 27(44):11978-11985; doi:10.1523/JNEUROSCI.3679-07.2007

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Cellular/Molecular
The Structural and Functional Differentiation of Hair Cells in a Lizard's Basilar Papilla Suggests an Operational Principle of Amniote Cochleas

M. Eugenia Chiappe, Andrei S. Kozlov, and A. J. Hudspeth

Howard Hughes Medical Institute and Laboratory of Sensory Neuroscience, The Rockefeller University, New York, New York 10065-6399

Correspondence should be addressed to Dr. A. J. Hudspeth, Howard Hughes Medical Institute and Laboratory of Sensory Neuroscience, The Rockefeller University, 1230 York Avenue, Box 314, New York, NY 10065-6399. Email: hudspaj{at}rockefeller.edu

The hair cells in the mammalian cochlea are of two distinct types. Inner hair cells are responsible for transducing mechanical stimuli into electrical responses, which they forward to the brain through a copious afferent innervation. Outer hair cells, which are thought to mediate the active process that sensitizes and tunes the cochlea, possess a negligible afferent innervation. For every inner hair cell, there are approximately three outer hair cells, so only one-quarter of the hair cells directly deliver information to the CNS. Although this is a surprising feature for a sensory system, the occurrence of a similar innervation pattern in birds and crocodilians suggests that the arrangement has an adaptive value. Using a lizard with highly developed hearing, the tokay gecko, we demonstrate in the present study that the same principle operates in a third major group of terrestrial animals. We propose that the differentiation of hair cells into signaling and amplifying classes reflects incompatible strategies for the optimization of mechanoelectrical transduction and of an active process based on active hair-bundle motility.

Key words: active process; auditory system; gecko; hair bundle; hearing; reptile

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Received April 24, 2007; revised Sept. 10, 2007; accepted Sept. 16, 2007.

Correspondence should be addressed to Dr. A. J. Hudspeth, Howard Hughes Medical Institute and Laboratory of Sensory Neuroscience, The Rockefeller University, 1230 York Avenue, Box 314, New York, NY 10065-6399. Email: hudspaj{at}rockefeller.edu

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