Two-dimensional spatiotemporal coding of linear acceleration in vestibular nuclei neurons

Abstract

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.

Visual Neurons in the Pigeon Brain Encode the Acceleration of Stimulus Motion

“…It seems likely that the plateau-shaped speed-tuning curve is an adaptation that is directly related to sensing stimulus acceleration, and it was striking to us that some neurons showed plateau-shaped tuning curves and acceleration sensitivity for motion in one direction paired with a peaked tuning curve and acceleration insensitivity for motion in the opposite direction. We doubt that the visual responses to acceleration are attributable to "jerk" defined as the rate of changes in acceleration in previous studies on the vestibular system (Angelaki et al, 1993;Jones et al, 1998) because the acceleration we used is constant.…”

Computation of Inertial Motion: Neural Strategies to Resolve Ambiguous Otolith Information

“…Such computational steps have been often proposed to occur within single neurons or assemblies of neurons (Torre and Poggio, 1978;Koch et al, 1983;Shen, 1989). Furthermore, head angular velocity signals (), as well as both linear acceleration (␣) and its time derivative (␣) signals have been shown to coexist in single vestibular brainstem neurons (Angelaki et al, 1993). These computational schemes and the conclusions reached based on the results of this study are only pertinent to frequencies higher than 0.1 Hz in which semicircular canal afferents can provide veridical information about head angular velocity.…”

Development of the Vestibular System

“…The properties of central otolith neurons in coding head movements near the horizontal plane have been studied in postnatal [35,[76][77][78] and adult rats [77,[79][80][81]. With the use of such natural stimuli as off-vertical axis rotation (OVAR) [77,78,[82][83][84][85] and horizontal linear acceleration [79][80][81], the best vectors of central otolith neurons of adult animals were found to point in all directions on the horizontal plane.…”

“…With the use of such natural stimuli as off-vertical axis rotation (OVAR) [77,78,[82][83][84][85] and horizontal linear acceleration [79][80][81], the best vectors of central otolith neurons of adult animals were found to point in all directions on the horizontal plane. Such a uniform spatial distribution was also observed in the cerebellar fastigial nucleus [82] and medial medullary reticular formation [86] of adult cats.…”