Journal of Neurophysiology, Vol 76, Issue 5 3249-3263, Copyright © 1996 by APS

ARTICLES

Modulation of the human vestibuloocular reflex during saccades: probing by high-frequency oscillation and torque pulses of the head

S. Tabak, J. B. Smeets and H. Collewijn
Department of Physiology, Helmholtz School, Faculty of Medicine, Erasmus University Rotterdam, The Netherlands.

1. We probed the gain and phase of the vestibuloocular reflex (VOR) during the execution of voluntary gaze saccades, with continuous oscillation or acceleration pulses, applied through a torque helmet. 2. Small-amplitude (< 1 degree), high-frequency (10-14 Hz) head oscillations in the horizontal or vertical plane were superimposed on ongoing horizontal gaze saccades (40-100 degrees). Torque pulses to the head ("with" or "against" gaze) were superimposed on 40 degrees horizontal saccades. Eye and head movements were precisely measured with sensor coils in magnetic fields. 3. Techniques were developed to separate the oscillatory (horizontal or vertical) component from the gaze shift and obtain VOR gain and phase with Fourier techniques from the relation between eye-in-head and head oscillations. These involved either subtraction of exactly matching saccades with and without oscillation (drawback: low yield) or time shifting of successive trials to synchronize the oscillations (drawback: slight time blurring of saccades). 4. The results of these matching and synchronization methods were essentially identical and consistent. Presaccadic gain values of the horizontal VOR (typically about unity) were reduced by, on average, approximately 20 and 50% during horizontal saccades of 40 and 100 degrees, respectively. These percentages may be truncated because of methodological limitations, but even after taking these into account (on the basis of simulation experiments with 2 different, theoretical profiles of suppression) our results do not support a complete saccadic VOR suppression for any substantial fraction of saccadic duration. Qualitatively similar changes were found when the vertical VOR was probed during 100 degrees horizontal saccades. 5. Concomitantly with the reductions in gain, VOR phase was advanced by approximately 20 degrees during the saccade. 6. In the wake of gaze saccades, VOR gain was consistently elevated (to approximately 1.0) above the presaccadic level (approximately 0.9). We submit that this mechanism ensures stable fixation of the newly acquired target at a time when the head is still moving substantially. 7. Although the responses to head torque pulses showed idiosyncratic asymmetries, analysis of the differences in eye and head movements for pulses with and against consistently showed a sharp fall of VOR gain at saccadic onset, following an approximately exponential course with a time constant of approximately 50 ms. This decay may be assumed to reflect VOR gain for a period of approximately 50 ms, after which secondary gaze control mechanisms become dominant. 8. The time course of the gain decay and phase shift of the VOR suggest that suppression of the "integrative (position) loop" of the VOR circuit was more complete than suppression of the direct, "velocity" pathway.

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