Journal of Neuroscience, Vol 15, 7201-7216, Copyright © 1995 by Society for Neuroscience
Differential processing of semicircular canal signals in the vestibulo- ocular reflex
DE Angelaki, BJ Hess and J Suzuki
Department of Surgery (Otolaryngology), University of Mississippi Medical Center, Jackson 39216-4505, USA.
Selective semicircular canal inactivation and three-dimensional eye
movement recordings have been used to investigate the spatial organization
of vestibular signals in the vestibulo-ocular reflex (VOR) of rhesus
monkeys. In animals with one pair of semicircular canals inactivated,
afferent activity no longer codes all spatial components of head angular
velocity. if it were the activation pattern of semicircular canal afferents
alone that determines VOR slow phase eye velocity, the head velocity
components along the sensitivity vectors of the remaining intact
semicircular canals would determine the orientation of slow phase eye
velocity. Thus, angular head velocity and slow phase eye velocity would not
necessarily always align. Alternatively, if vestibulo-ocular signals coded
absolute angular head motion in space based on both semicircular canal and
otolith afferent information, one might expect a spatial transformation of
the encoded head angular velocity signals such that slow phase eye velocity
and angular head velocity continue to spatially align. Examination of the
VOR at different frequencies between 0.01 Hz and 1 Hz revealed a
frequency-specific spatial organization of vestibulo-ocular signals. Mid
and high frequency vestibulo-ocular responses were determined exclusively
by the orientation of the sensitivity vectors of the remaining intact
semicircular canals. In contrasts, low frequency vestibulo-ocular responses
were largely determined by the orientation of the head relative to gravity.
These low frequency responses after selective semicircular canal
inactivation could be predicted and simulated by a simple model where
semicircular canal signals are spatially transformed from a head-fixed to a
space-fixed (inertial) representation of angular head velocity. These
findings suggest that low frequency vestibulo-ocular responses are
dominated by inertial vestibular signals that detect absolute head motion
in space based on both semicircular canal and otolith afferent information.
Inertial vestibular signals are likely to contribute to head control and
motor coordination of gaze, head and body posture.
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