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The Journal of Neurophysiology Vol. 81 No. 6 June 1999, pp. 2764-2786
Copyright ©1999 by the American Physiological Society
Division of Biology, California Institute of Technology, Pasadena, California 91125
Shenoy, Krishna V.,
David C. Bradley, and
Richard A. Andersen.
Influence of Gaze Rotation on the Visual Response of Primate
MSTd Neurons. J. Neurophysiol. 81: 2764-2786, 1999.
Influence of gaze rotation on the visual response of primate MSTd
neurons. When we move forward, the visual image on our retina expands. Humans rely on the focus, or center, of this expansion to
estimate their direction of heading and, as long as the eyes are still,
the retinal focus corresponds to the heading. However, smooth rotation
of the eyes adds nearly uniform visual motion to the expanding retinal
image and causes a displacement of the retinal focus. In spite of this,
humans accurately judge their heading during pursuit eye movements and
during active, smooth head rotations even though the retinal focus no
longer corresponds to the heading. Recent studies in macaque suggest
that correction for pursuit may occur in the dorsal aspect of the
medial superior temporal area (MSTd) because these neurons are tuned to
the retinal position of the focus and they modify their tuning during
pursuit to compensate partially for the focus shift. However, the
question remains whether these neurons also shift focus tuning to
compensate for smooth head rotations that commonly occur during gaze
tracking. To investigate this question, we recorded from 80 MSTd
neurons while monkeys tracked a visual target either by pursuing with their eyes or by vestibulo-ocular reflex cancellation (VORC; whole-body rotation with eyes fixed in head and head fixed on body). VORC is a
passive, smooth head rotation condition that selectively activates the
vestibular canals. We found that neurons shift their focus tuning in a
similar way whether focus displacement is caused by pursuit or by VORC.
Across the population, compensation averaged 88 and 77% during pursuit
and VORC, respectively (tuning shift divided by the retinal focus to
true heading difference). Moreover the degree of compensation during
pursuit and VORC was correlated in individual cells (P < 0.001). Finally neurons that did not compensate appreciably tended
to be gain-modulated during pursuit and VORC and may constitute an
intermediate stage in the compensation process. These results indicate
that many MSTd cells compensate for general gaze rotation,
whether produced by eye-in-head or head-in-world rotation, and further
implicate MSTd as a critical stage in the computation of heading.
Interestingly vestibular cues present during VORC allow many cells to
compensate even though humans do not accurately judge their heading in
this condition. This suggests that MSTd may use vestibular information
to create a compensated heading representation within at least a
subpopulation of cells, which is accessed perceptually only when
additional cues related to active head rotations are also present.
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