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J Neurophysiol (December 1, 2002). 10.1152/jn.00518.2002
Submitted on 18 July 2002
Accepted on 14 August 2002
Department of Research, Central Institute for the Deaf; and Department of Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110
Dickman, J. David and
Dora E. Angelaki.
Vestibular Convergence Patterns in Vestibular Nuclei Neurons of
Alert Primates. J. Neurophysiol. 88: 3518-3533, 2002. Sensory signal convergence is a fundamental and
important aspect of brain function. Such convergence may often
involve complex multidimensional interactions as those proposed for the
processing of otolith and semicircular canal (SCC) information for the
detection of translational head movements and the effective
discrimination from physically congruent gravity signals. In the
present study, we have examined the responses of primate rostral
vestibular nuclei (VN) neurons that do not exhibit any eye
movement-related activity using 0.5-Hz translational and
three-dimensional (3D) rotational motion. Three distinct neural
populations were identified. Approximately one-fourth of the cells
exclusively encoded rotational movements (canal-only neurons) and were
unresponsive to translation. The canal-only central neurons encoded
head rotation in SCC coordinates, exhibited little orthogonal canal
convergence, and were characterized with significantly higher
sensitivities to rotation as compared to primary SCC afferents. Another
fourth of the neurons modulated their firing rates during translation
(otolith-only cells). During rotations, these neurons only responded
when the axis of rotation was earth-horizontal and the head was
changing orientation relative to gravity. The remaining one-half of VN
neurons were sensitive to both rotations and translations (otolith + canal neurons). Unlike primary otolith afferents, however, central
neurons often exhibited significant spatiotemporal (noncosine) tuning
properties and a wide variety of response dynamics to translation. To
characterize the pattern of SCC inputs to otolith + canal neurons,
their rotational maximum sensitivity vectors were computed using
exclusively responses during earth-vertical axis rotations (EVA).
Maximum sensitivity vectors were distributed throughout the 3D space,
suggesting strong convergence from multiple SCCs. These neurons were
also tested with earth-horizontal axis rotations (EHA), which would
activate both vertical canals and otolith organs. However, the recorded responses could not be predicted from a linear combination of EVA
rotational and translational responses. In contrast, one-third of the
neurons responded similarly during EVA and EHA rotations, although a
significant response modulation was present during translation. Thus
this subpopulation of otolith + canal cells, which included neurons
with either high- or low-pass dynamics to translation, appear to
selectively ignore the component of otolith-selective activation that
is due to changes in the orientation of the head relative to gravity.
Thus contrary to primary otolith afferents and otolith-only central
neurons that respond equivalently to tilts relative to gravity and
translational movements, approximately one-third of the otolith + canal
cells seem to encode a true estimate of the translational component of
the imposed passive head and body movement.
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