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The Journal of Neurophysiology Vol. 84 No. 4 October 2000, pp. 2113-2132
Copyright ©2000 by the American Physiological Society
Department of Neurobiology, Washington University School of Medicine; and Department of Research, Central Institute for the Deaf, St. Louis, Missouri 63110
Angelaki, Dora E. and
J. David Dickman.
Spatiotemporal Processing of Linear Acceleration: Primary
Afferent and Central Vestibular Neuron Responses. J. Neurophysiol. 84: 2113-2132, 2000. Spatiotemporal convergence
and two-dimensional (2-D) neural tuning have been proposed as a major
neural mechanism in the signal processing of linear acceleration. To
examine this hypothesis, we studied the firing properties of primary
otolith afferents and central otolith neurons that respond exclusively
to horizontal linear accelerations of the head (0.16-10 Hz) in alert
rhesus monkeys. Unlike primary afferents, the majority of central
otolith neurons exhibited 2-D spatial tuning to linear acceleration. As a result, central otolith dynamics vary as a function of movement direction. During movement along the maximum sensitivity direction, the
dynamics of all central otolith neurons differed significantly from
those observed for the primary afferent population. Specifically at low
frequencies (
0.5 Hz), the firing rate of the majority of central
otolith neurons peaked in phase with linear velocity, in contrast to
primary afferents that peaked in phase with linear acceleration. At
least three different groups of central response dynamics were
described according to the properties observed for motion along the
maximum sensitivity direction. "High-pass" neurons exhibited
increasing gains and phase values as a function of frequency. "Flat" neurons were characterized by relatively flat gains and constant phase lags (~20-55°). A few neurons ("low-pass") were characterized by decreasing gain and phase as a function of frequency. The response dynamics of central otolith neurons suggest that the
~90° phase lags observed at low frequencies are not the result of a
neural integration but rather the effect of nonminimum phase behavior,
which could arise at least partly through spatiotemporal convergence.
Neither afferent nor central otolith neurons discriminated between
gravitational and inertial components of linear acceleration. Thus
response sensitivity was indistinguishable during 0.5-Hz pitch
oscillations and fore-aft movements. The fact that otolith-only central
neurons with "high-pass" filter properties exhibit semicircular canal-like dynamics during head tilts might have important consequences for the conclusions of previous studies of sensory convergence and
sensorimotor transformations in central vestibular neurons.
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