Behavior of the Position Vestibular Pause (PVP) Interneurons of the Vestibuloocular Reflex During Head-Free Gaze Shifts in the Monkey

1 Departments of Physiology and Biophysics and 2 Otolaryngology, Head, and Neck Surgery and 3 Washington Regional Primate Research Center, University of Washington, Seattle, Washington Submitted 28 January 2005; accepted in final form 18 August 2005 Most behavioral studies indicate that the efficacy (gain) of the vestibuloocular reflex (VOR) in primates is modulated during the voluntary head movements that accompany large shifts in the direction of gaze. However, the timing and degree of this modulation is the subject of some debate. The neurophysiological substrate for this apparent gain reduction has been sought in the behavior of the type I position vestibular pause (PVP) neuron, a well-known type of interneuron in the direct VOR pathway. With the head fixed, PVPs increase their firing rates with contraversive eye position and with ipsiversive passive head rotation and also cease firing (pause) for the duration of ipsiversive saccades. During head-free ipsiversive gaze shifts, the eyes and head move in the same direction. If the vestibular signal carried by PVPs provides the primary drive for the VOR, the vestibular signal should be present during ipsiversive gaze shifts to the degree that the VOR is present. Of 25 type I PVPs recorded, 21 ceased their discharge for the entire duration of the rapid, eye-saccade component of an ipsiversive gaze shift. The resumption of activity occurred, on average, 13 ms after the end of the saccade. These results suggest that the activity of the vast majority of PVP neurons do not reflect the state of the VOR, but rather PVPs are completely eliminated from participation in the reflex during head-free gaze movements. We conclude that if any modulation of the VOR does exist, it must occur through other, probably longer-latency, pathways. Address for reprint requests and other correspondence: A. F. Fuchs, 1959 NE Pacific St. HSB I421, Washington Regional Primate Research Center, Box 357330, University of Washington, Seattle, WA 98195-7330 (E-mail: fuchs{at}u.washington.edu )