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J Neurophysiol 93: 2777-2786, 2005. First published December 15, 2004; doi:10.1152/jn.01002.2004
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Responses of Irregularly Discharging Chinchilla Semicircular Canal Vestibular-Nerve Afferents During High-Frequency Head Rotations

Timothy E. Hullar1,2, Charles C. Della Santina1, Timo Hirvonen1, David M. Lasker1, John P. Carey1 and Lloyd B. Minor1

1Department of Otolaryngology—Head and Neck Surgery, The Johns Hopkins University School of Medicine, Baltimore, Maryland; and 2Department of Otolaryngology—Head and Neck Surgery, Washington University School of Medicine, St. Louis, Missouri

Submitted 23 September 2004; accepted in final form 7 December 2004

Mammalian vestibular-nerve afferents innervating the semicircular canals have been divided into groups according to their discharge regularity, gain at 2-Hz rotational stimulation, and morphology. Low-gain irregular afferents terminate in calyx endings in the central crista, high-gain irregular afferents synapse more peripherally in dimorphic (bouton and calyx) endings, and regular afferents terminate in the peripheral zone as bouton-only and dimorphic endings. The response dynamics of these three groups have been described only up to 4 Hz in previous studies. Reported here are responses of chinchilla semicircular canal vestibular-nerve afferents to rotational stimuli at frequencies up to 16 Hz. The sensitivity of all afferents increased with increasing frequency with the sensitivity of low-gain irregular afferents increasing the most and matching the high-gain irregular afferents at 16 Hz. All afferents increased their phase lead with respect to stimulus velocity at higher frequencies with the highest leads in low-gain irregular afferents and the lowest in regular afferents. No attenuation of sensitivity or shift in phase consistent with the presence of a high-frequency pole over the range tested was noted. Responses were best fit with a torsion-pendulum model combined with a lead operator ({tau}HF1s + 1)({tau}HF2s + 1). The discharge regularity of individual afferents was correlated to the value of each afferent's lead operator time constants. These findings suggest that low-gain irregular afferents are well suited for encoding the onset of rapid head movements, a property that would be advantageous for initiation of reflexes with short latency such as the vestibulo-ocular reflex.


Address for reprint requests and other correspondence: T. E. Hullar, Dept. of Otolaryngology—Head and Neck Surgery, Washington University School of Medicine, 660 S. Euclid Ave. #8115, Saint Louis, MO 63110 (E-mail: hullart{at}ent.wustl.edu)




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