Response of Vestibular-Nerve Afferents to Active and Passive Rotations Under Normal Conditions and After Unilateral Labyrinthectomy (original) (raw)

2006, Journal of Neurophysiology

Sadeghi SG, Minor LB, Cullen KE. Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy. . We investigated the possible contribution of signals carried by vestibular-nerve afferents to long-term processes of vestibular compensation after unilateral labyrinthectomy. Semicircular canal afferents were recorded from the contralesional nerve in three macaque monkeys before [horizontal (HC) ϭ 67, anterior (AC) ϭ 66, posterior (PC) ϭ 50] and 1-12 mo after (HC ϭ 192, AC ϭ 86, PC ϭ 57) lesion. Vestibular responses were evaluated using passive sinusoidal rotations with frequencies of 0.5-15 Hz (20 -80°/s) and fast whole-body rotations reaching velocities of 500°/s. Sensitivities to nonvestibular inputs were tested by: 1) comparing responses during active and passive head movements, 2) rotating the body with the head held stationary to activate neck proprioceptors, and 3) encouraging head-restrained animals to attempt to make head movements that resulted in the production of neck torques of Յ2 Nm. Mean resting discharge rate before and after the lesion did not differ for the regular, D (dimorphic)-irregular, or C (calyx)-irregular afferents. In response to passive rotations, afferents showed no change in sensitivity and phase, inhibitory cutoff, and excitatory saturation after unilateral labyrinthectomy. Moreover, head sensitivities were similar during voluntary and passive head rotations and responses were not altered by neck proprioceptive or efference copy signals before or after the lesion. The only significant change was an increase in the proportion of C-irregular units postlesion, accompanied by a decrease in the proportion of regular afferents. Taken together, our findings show that changes in response properties of the vestibular afferent population are not likely to play a major role in the long-term changes associated with compensation after unilateral labyrinthectomy. Allum JH, Yamane M, Pfaltz CR. Long-term modifications of vertical and horizontal vestibulo-ocular reflex dynamics in man. I. After acute unilateral peripheral vestibular paralysis. Acta Otolaryngol 105: 328 -337, 1988. Andre-Deshays C, Revel M, Berthoz A. Eye-head coupling in humans. II. Phasic components. Exp Brain Res 84: 359 -366, 1991. Armand M, Minor LB. Relationship between time-and frequency-domain analyses of angular head movements in the squirrel monkey. J Comput Neurosci 11: 217-239, 2001. Baird RA, Desmadryl G, Fernandez C, Goldberg JM. The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60: 182-203, 1988. Beraneck M, Idoux E, Uno A, Vidal PP, Moore LE, Vibert N. Unilateral labyrinthectomy modifies the membrane properties of contralesional vestibular neurons. J Neurophysiol 92: 1668 -1684, 2004. Bizzi E, Kalil RE, Tagliasco V. Eye-head coordination in monkeys: evidence for centrally patterned organization. Science 173: 452-454, 1971. Boyle R, Highstein SM. Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents. J Neurosci 10: 1570 -1582, 1990. Bricout-Berthout A, Caston J, Reber A. Influence of stimulation of auditory and somatosensory systems on the activity of vestibular nuclear neurons in the frog. Brain Behav Evol 24: 21-34, 1984. Bronte-Stewart HM, Lisberger SG. Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys. J Neurosci 14: 1290 -1308, 1994. Caston J, Bricout-Berthout A. Responses to somatosensory input by afferent and efferent neurons in the vestibular nerve of the frog. Brain Behav Evol 24: 135-143, 1984. Cullen KE, Minor LB. Semicircular canal afferents similarly encode active and passive head-on-body rotations: implications for the role of vestibular efference. J Neurosci 22: RC226, 2002. Cullen KE, Rey CG, Guitton D, Galiana HL. The use of system identification techniques in the analysis of oculomotor burst neuron spike train dynamics. J Comput Neurosci 3: 347-368, 1996. Curthoys IS, Halmagyi GM. Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss.