Vestibular control of body orientation in lamprey

Abstract

Maintenance of body orientation (postural control) is a vital motor function of the brain. The general goal of this project was to understand the organization and operation of neuronal networks responsible for postural control. The lamprey (a lower vertebrate) was used as a model animal. The postural control system in the lamprey, driven by vestibular input, maintains a definite orientation of the longitudinal body axis in relation to horizon (pitch angle) and the dorsal-side-up body orientation (roll angle is 0°). Important elements of the postural network are reticulospinal (RS) neurons, which are driven by vestibular input and transmit commands for postural corrections from the brain to the spinal cord.

In in vivo studies, the activity of RS neurons was recorded from their axons in the spinal cord by chronically implanted electrodes. The animals were rotated through 3600 in the roll or pitch plane in order to stimulate vestibular organs. The activity of individual neurons was separated from the mass activity by a spike-sorting program.

Rotation in the pitch plane revealed two groups of neurons (UP and DOWN), responding to nose-up and nose-down rotation, respectively. These groups presumably mediate opposing vestibular reflexes and cause downward and upward turns of the animal. 22% of the RS neurons responding to pitch tilts also responded to roll tilts. This overlap suggests that the RS pathways are partly shared by the pitch and roll control systems.

A unilateral labyrinthectomy (UL) caused continuous rolling of the lamprey. Testing in the roll plane has shown that UL slightly affected responses on the UL side, whereas those on the opposite side disappeared. This asymmetry is the likely cause for the loss of equilibrium. Eye illumination led to a restoration of responses on the side contraleteral to UL, and to a reduction of responses on the opposite side. The restoration of symmetry of RS responses allows one to explain the behavioral effect of eye illumination . restoration of equilibrium.

When animals were tested in the pitch plane before and after UL, in the group UP responses on the UL side changed only slightly, and on the opposite side they disappeared. In the group DOWN, the UL caused only minor changes in vestibular responses. Thus left and right UP subgroups receive their main input from the contralateral labyrinth. By contrast, neurons of group DOWN receive input from both labyrinths. The UL-induced changes in vestibular responses to pitch tilt will disturb the normal activity of the pitch control system.

Normally, a few weeks after UL lampreys restore postural equilibrium (.vestibular compensation.). When behaviorally compensated animals were tested in the roll plane, it was found that vestibular responses on the side contralateral to UL reappeared, partly restoring symmetry in RS responses. These findings support the hypothesis that the recovery of postural control after UL is due to a restoration of symmetry in the RS motor commands.

In vitro experiments were performed on the brainstem-spinal cord preparation, with intracellular stimulation of individual RS and vestibulospinal (VS) neurons, and recording the responses to these stimuli from spinal motoneurons. Most of the neurons produced effects on motor output, enhancing or suppressing it. The effects of VS neurons on different groups of motoneurons were weaker and less diverse than those of RS neurons. The RS and VS patterns of responses and the extent of neuronal projections suggest that VS neurons are responsible for flexion of the rostral part of the body and turns of the head in different planes, whereas RS neurons are responsible for formation of gross motor synergies.