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The Journal of Neurophysiology Vol. 87 No. 5 May 2002, pp. 2337-2357
Copyright ©2002 by the American Physiological Society
Aerospace Medical Research Unit, Department of Physiology, McGill University, Montreal, Quebec H3G 1Y6, Canada
Roy, Jefferson E. and
Kathleen E. Cullen.
Vestibuloocular Reflex Signal Modulation During Voluntary and
Passive Head Movements. J. Neurophysiol. 87: 2337-2357, 2002. The vestibuloocular reflex (VOR) effectively
stabilizes the visual world on the retina over the wide range of head
movements generated during daily activities by producing an eye
movement of equal and opposite amplitude to the motion of the head.
Although an intact VOR is essential for stabilizing gaze during walking and running, it can be counterproductive during certain voluntary behaviors. For example, primates use rapid coordinated movements of the
eyes and head (gaze shifts) to redirect the visual axis from one target
of interest to another. During these self-generated head movements, a
fully functional VOR would generate an eye-movement command in the
direction opposite to that of the intended shift in gaze. Here, we have
investigated how the VOR pathways process vestibular information across
a wide range of behaviors in which head movements were either
externally applied and/or self-generated and in which the gaze goal was
systematically varied (i.e., stabilize vs. redirect). VOR interneurons
[i.e., type I position-vestibular-pause (PVP) neurons] were
characterized during head-restrained passive whole-body rotation,
passive head-on-body rotation, active eye-head gaze shifts, active
eye-head gaze pursuit, self-generated whole-body motion, and active
head-on-body motion made while the monkey was passively rotated. We
found that regardless of the stimulation condition, type I PVP neuron
responses to head motion were comparable whenever the monkey stabilized
its gaze. In contrast, whenever the monkey redirected its gaze,
type I PVP neurons were significantly less responsive to head velocity.
We also performed a comparable analysis of type II PVP neurons, which
are likely to contribute indirectly to the VOR, and found that they
generally behaved in a quantitatively similar manner. Thus our findings
support the hypothesis that the activity of the VOR pathways is reduced
"on-line" whenever the current behavioral goal is to redirect gaze.
By characterizing neuronal responses during a variety of experimental
conditions, we were also able to determine which inputs contribute to
the differential processing of head-velocity information by PVP
neurons. We show that neither neck proprioceptive inputs, an efference copy of neck motor commands nor the monkey's knowledge of its self-motion influence the activity of PVP neurons per se. Rather we
propose that efference copies of oculomotor/gaze commands are responsible for the behaviorally dependent modulation of PVP neurons (and by extension for modulation of the status of the VOR) during gaze redirection.
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