TY - JOUR
T1 - Vestibuloocular reflex signal modulation during voluntary and passive head movements
AU - Roy, Jefferson E.
AU - Cullen, Kathleen E.
PY - 2002
Y1 - 2002
N2 - 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.
AB - 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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U2 - 10.1152/jn.2002.87.5.2337
DO - 10.1152/jn.2002.87.5.2337
M3 - Article
C2 - 11976372
AN - SCOPUS:0036088751
SN - 0022-3077
VL - 87
SP - 2337
EP - 2357
JO - Journal of neurophysiology
JF - Journal of neurophysiology
IS - 5
ER -