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Journal of Neuroscience, Vol 13, 1403-1417, Copyright © 1993 by Society for Neuroscience
Two-dimensional spatiotemporal coding of linear acceleration in vestibular nuclei neurons
DE Angelaki, GA Bush and AA Perachio
Department of Otolaryngology, University of Texas Medical Branch, Galveston 77555.
Response properties of vertical (VC) and horizontal (HC) canal/otolith-
convergent vestibular nuclei neurons were studied in decerebrate rats
during stimulation with sinusoidal linear accelerations (0.2-1.4 Hz) along
different directions in the head horizontal plane. A novel characteristic
of the majority of tested neurons was the nonzero response often elicited
during stimulation along the "null" direction (i.e., the direction
perpendicular to the maximum sensitivity vector, Smax). The tuning ratio
(Smin gain/Smax gain), a measure of the two- dimensional spatial
sensitivity, depended on stimulus frequency. For most vestibular nuclei
neurons, the tuning ratio was small at the lowest stimulus frequencies and
progressively increased with frequency. Specifically, HC neurons were
characterized by a flat Smax gain and an approximately 10-fold increase of
Smin gain per frequency decade. Thus, these neurons encode linear
acceleration when stimulated along their maximum sensitivity direction, and
the rate of change of linear acceleration (jerk) when stimulated along
their minimum sensitivity direction. While the Smax vectors were
distributed throughout the horizontal plane, the Smin vectors were
concentrated mainly ipsilaterally with respect to head acceleration and
clustered around the naso-occipital head axis. The properties of VC neurons
were distinctly different from those of HC cells. The majority of VC cells
showed decreasing Smax gains and small, relatively flat, Smin gains as a
function of frequency. The Smax vectors were distributed ipsilaterally
relative to the induced (apparent) head tilt. In type I anterior or
posterior VC neurons, Smax vectors were clustered around the projection of
the respective ipsilateral canal plane onto the horizontal head plane.
These distinct spatial and temporal properties of HC and VC neurons during
linear acceleration are compatible with the spatiotemporal organization of
the horizontal and the vertical/torsional ocular responses, respectively,
elicited in the rat during linear translation in the horizontal head plane.
In addition, the data suggest a spatially and temporally specific and
selective otolith/canal convergence. We propose that the central otolith
system is organized in canal coordinates such that there is a close
alignment between the plane of angular acceleration (canal) sensitivity and
the plane of linear acceleration (otolith) sensitivity in otolith/canal-
convergent vestibular nuclei neurons.
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