Adaptation of orientation vectors of otolith-related central vestibular neurons to gravity

Abstract

Behavioral experiments indicate that central pathways that process otolith-ocular and perceptual information have adaptive capabilities. Because polarization vectors of otolith afferents are directly related to the electro-mechanical properties of the hair cell bundle, it is unlikely that they change their direction of excitation. This indicates that the adaptation must take place in central pathways. Here we demonstrate for the first time that otolith polarization vectors of canal-otolith convergent neurons in the vestibular nuclei have adaptive capability. A total of 10 vestibular-only and vestibular-plus-saccade neurons were recorded extracellularly in two monkeys before and after they were in side-down positions for 2 h. The spatial characteristics of the otolith input were determined from the response vector orientation (RVO), which is the projection of the otolith polarization vector, onto the head horizontal plane. The RVOs had no specific orientation before animals were in side-down positions but moved toward the gravitational axis after the animals were tilted for extended periods. Vector reorientations varied from 0 to 109 degrees and were linearly related to the original deviation of the RVOs from gravity in the position of adaptation. Such reorientation of central polarization vectors could provide the basis for changes in perception and eye movements related to prolonged head tilts relative to gravity or in microgravity.

FIG. 1.

Determination of otolith response vector orientation (RVO) of a central vestibular neuron relative to the acceleration of gravity, a_g, in head coordinates. A: direction of a_g in head coordinates (↑) in 15° increments about a yaw axis from 180° (left) to 360° (right) during head tilts from upright. The opposite directions of a_g and g are shown by the ↓ and ↑ on the right. B: 30° head tilts about the horizontal axis (— in A). C: changes of the firing rate of unit 6 to each head tilt. The last 20 s, i.e., the steady-state otolith response was used for analysis. D: sensitivity of the neuron shown in C (ordinate) as a function of orientation of a_g in head coordinates (abscissa).- - -, a sinusoidal fit to the data, where b is the orientation of the maximal sensitivity (S_max), which is the RVO. E: orientation of the RVO relative to a_g in head coordinates. Angles are positive in head coordinates in a counterclockwise direction, according to a right hand rule. The maximal excitation in tilt for this VO neuron was when the orientation of g was 58° in head coordinates which is the RVO.

FIG. 2.

Changes in the RVO of vestibular-only (VO) and vestibular-plus-saccade (VPS) units induced by side-down tilt for 2 h. A: sensitivity of unit 1 (ordinate) plotted as a function of the orientation of a_g in the horizontal plane of the head (abscissa) before (open circles) and after (filled circles) side-down adaptation. B (units 1–5): changes in RVO of neurons (dashed arrow to black arrow) after being in a side down position for 2 h with a_g along the interaural axis. The aVOR gain was decreased in this position. The change in the RVO was the smaller angle between the 2 polarizations. C (units 6–10): changes in RVO (dashed arrow to black arrow) induced by holding the head stationary in a side-down position. In both B and C, the RVO changed its orientation toward the gravitational axis. P values of the RVO changes were significant in 6 of the 10 neurons. D: shifts in RVO of six neuron that were on the same side of the mid-sagittal plane, as a function of angular displacement from the gravitational axis. The solid line is the linear regression and the dashed lines show ±1 SD. Units 1 and 6 had changes across the mid-sagittal plane. The 8 of 10 neurons that had RVO changes are shown in black. Two units with no changes in RVO are shown by the gray symbols.