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Hair-Cell Versus Afferent Adaptation in the Semicircular Canals

¹Department of Bioengineering, University of Utah, Salt Lake City, Utah; ²National Aeronautics and Space Administration Ames BioVIS Technology Center, Moffett Field, California; ³Department of Neurology and Center for Anatomy and Functional Morphology, Mount Sinai School of Medicine, New York, New York; ⁴Departments of Otolaryngology and Neurobiology Washington University School of Medicine St. Louis, Missouri; and ⁵Marine Biological Laboratory, Woods Hole, Massachusetts

Submitted 26 April 2004; accepted in final form 6 August 2004

The time course and extent of adaptation in semicircular canal hair cells was compared to adaptation in primary afferent neurons for physiological stimuli in vivo to study the origins of the neural code transmitted to the brain. The oyster toadfish, Opsanus tau, was used as the experimental model. Afferent firing-rate adaptation followed a double-exponential time course in response to step cupula displacements. The dominant adaptation time constant varied considerably among afferent fibers and spanned six orders of magnitude for the population (1 ms to >1,000 s). For sinusoidal stimuli (0.1–20 Hz), the rapidly adapting afferents exhibited a 90° phase lead and frequency-dependent gain, whereas slowly adapting afferents exhibited a flat gain and no phase lead. Hair-cell voltage and current modulations were similar to the slowly adapting afferents and exhibited a relatively flat gain with very little phase lead over the physiological bandwidth and dynamic range tested. Semicircular canal microphonics also showed responses consistent with the slowly adapting subset of afferents and with hair cells. The relatively broad diversity of afferent adaptation time constants and frequency-dependent discharge modulations relative to hair-cell voltage implicate a subsequent site of adaptation that plays a major role in further shaping the temporal characteristics of semicircular canal afferent neural signals.

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