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The Journal of Neurophysiology Vol. 83 No. 1 January 2000, pp. 563-587
Copyright ©2000 by the American Physiological Society
Department of Physiology, Hokkaido University School of Medicine, Sapporo 060-8638, Japan; and Department of Physiology and Biophysics and Regional Primate Research Center, University of Washington, Seattle, Washington 98195
Fukushima, Kikuro,
Toshikazu Sato,
Junko Fukushima,
Yasuhiro Shinmei, and
Chris R. S. Kaneko.
Activity of Smooth Pursuit-Related Neurons in the Monkey
Periarcuate Cortex During Pursuit and Passive Whole-Body Rotation. J. Neurophysiol. 83: 563-587, 2000. Smooth pursuit and vestibularly induced eye movements interact to
maintain the accuracy of eye movements in space (i.e., gaze). To
understand the role played by the frontal eye fields in
pursuit-vestibular interactions, we examined activity of 110 neurons in
the periarcuate areas of head-stabilized Japanese monkeys during
pursuit eye movements and passive whole-body rotation. The majority
(92%) responded with the peak of their modulation near peak stimulus
velocity during suppression of the vestibuloocular reflex (VOR)
when the monkeys tracked a target that moved with the same amplitude
and phase and in the same plane as the chair. We classified
pursuit-related neurons (n = 100) as gaze- velocity
if their peak modulation occurred for eye (pursuit) and head (VOR
suppression) movements in the same direction; the amplitude of
modulation during one less than twice that of the other; and modulation
was lower during target-stationary-in-space condition (VOR ×1) than
during VOR suppression. In addition, we examined responses during VOR
enhancement (×2) in which the target moved with equal amplitude as,
but opposite direction to, the chair. Gaze-velocity neurons responded
maximally for opposite directions during VOR ×2 and suppression. Based
on these criteria, the majority of pursuit-related neurons (66%) were
classified as gaze-velocity with preferred directions uniformly
distributed. Because the majority of the remaining cells (32/34) also
responded during VOR suppression, they were classified as
eye/head-velocity neurons. Thirteen preferred pursuit and VOR
suppression in the same direction; 13 in the opposite direction, and 6 showed biphasic modulation during VOR suppression. Eye- and
gaze-velocity sensitivity of the two groups of cells were similar; mean
(± SD) was 0.53 ± 0.30 and 0.50 ± 0.44 spikes/s per °/s,
respectively. Gaze-velocity (but not eye/head-velocity) neurons showed
significant correlation between eye- and gaze-velocity sensitivity, and
both groups maintained their responses when the tracking target was
extinguished briefly. The majority of pursuit-related neurons
(28/43 = about 65%) responded to chair rotation in complete
darkness. When the monkeys fixated a stationary target, more than half
of cells tested (21/40) discharged in proportion to the velocity of
retinal motion of a second laser spot (mean velocity sensitivity = 0.20 ± 0.16 spikes/s per °/s). Preferred directions of
individual cells to the second spot were similar to those
during pursuit. Visual responses to the second spot
movement were maintained even when it was extinguished briefly. These
results indicate that both retinal image- and gaze-velocity signals are
carried by single periarcuate pursuit-related neurons, suggesting that
these signals can provide target-velocity-in-space and gaze-velocity
commands during pursuit-vestibular interactions.
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