Adaptation of orientation of central otolith-only neurons

Abstract

Otolith-only neurons were recorded extracellularly in the vestibular nuclei before and after cynomolgus monkeys were held on-side for up to 3 hr. The aim was to determine whether the polarization vectors of these neurons reorient toward the spatial vertical as do canal-otolith convergent neurons. Otolith input was characterized by tilting the animal 30 degrees from the upright position while positioning the head in different directions in yaw. This determined the response vector orientation (RVO), that is, the projection of the otolith polarization vector onto the head horizontal plane. Changes in the RVO of otolith-only neurons ranged from 2 degrees -16 degrees , which was on average considerably less than the changes previously noted in canal-otolith convergent vestibulo-only (VO) and vestibular plus saccade (VPS) neurons, which ranged up to 109 degrees. Some of the otolith-only neurons had marked sensitivity changes. These findings suggest that otolith-only neurons tend to maintain a head-fixed orientation during prolonged head tilts relative to gravity. In contrast, canal-convergent VO and VPS neurons optimize their response vector orientation to gravity when the head is oriented for prolonged periods.

Figures

Figure 1. Neuronal response of an otolith-only neuron (Unit #1) to head tilts from the upright from different head orientations in yaw

A, Direction of the acceleration of gravity (ag, arrows) in head coordinates in 15° increments about a yaw axis from 180° (left) to 360° (right). B, 30° head tilts about the horizontal axis, shown in A by the horizontal line. C, D, Neuronal firing rate (FR) for each head tilt, obtained before (C) and after 2 hrs (D) of head reorientation in a side down position. The horizontal dashed lines represent the average firing rate of this neuron in the upright position.

Figure 2. Neuronal response of the otolith only neuron (Unit #5) to head tilts from the upright for different head orientations in yaw

Scheme as in Fig. 1.

Figure 3

A, Sensitivity of the otolith-only neurons plotted as a function of orientation of the acceleration of gravity (ag) in head coordinates. The sinusoidal fits (lines) to the data measured before (open circles), after 1 hr (open triangles), after 2 hrs (filled circles) and after 3 hrs (open diamonds) of head orientation in side down position. B, RVO of each neuron before (solid arrows) and after 1, 2 and 3 hrs (dotted arrows) of adaptation. The RVO`s are presented as if the head was always positioned left side down (LSD), as shown in the insert for Unit #1.