Vestibular compensation in lampreys: restoration of symmetry in reticulospinal commands

Abstract

SUMMARY Removal of a vestibular organ (unilateral labyrinthectomy, UL) in the lamprey results in a loss of equilibrium, so that the animal rolls (rotates around its longitudinal axis) when swimming. Owing to vestibular compensation,UL animals gradually restore postural equilibrium and, in a few weeks, swim without rolling. Important elements of the postural network in the lamprey are the reticulospinal (RS) neurons, which are driven by vestibular input and transmit commands for postural corrections to the spinal cord. As shown previously, a loss of equilibrium after UL is associated with disappearance of vestibular responses in the contralateral group of RS neurons. Are these responses restored in animals after compensation? To answer this question, we recorded vestibular responses in RS neurons (elicited by rotation of the compensated animal in the roll plane) by means of chronically implanted electrodes. We found that the responses re-appeared in the compensated animals. This result supports the hypothesis that the loss of equilibrium after UL was caused by asymmetry in supraspinal motor commands, and the recovery of postural control in compensated animals was due to a restoration of symmetry.

Quantitative Evaluation of a New Posturo-Locomotor Phenotype in a Rodent Model of Acute Unilateral Vestibulopathy

“…Thus, unilateral loss of vestibular input causes inactivation of reticulospinal neurons on the contralateral side. This inactivation impairs the symmetrical activity of the left and right groups of reticulospinal neurons and provokes ipsilesional rotation of the lamprey (58).…”

“…This preferred sense of ipsilesional exploration can be explained by the UVN inducing an asymmetry of muscle tone (56), an increase in weight applied to the ipsilesional paw (55), an ipsilesional shift of their environment on the retina (57), or an ipsilesional path deviation (36). Another possibility comes from a model of vestibular compensation in lampreys (58). The opposite and symmetrical activity of both the left and right groups of reticulospinal neurons allow the lamprey to swim straight.…”

The role of the substantia nigra in posture control

“…Previous work has shown that the reticulospinal system can generate movements that resist the effects of postural disturbances in any direction (Zelenin et al ., ). In the lamprey, for example, reticulospinal neurons can receive inputs from the vestibular nuclei and other sensory systems, which report the current values of sensory variables relevant to posture control and send projections to motor neurons, which in turn produce movements that resist the effect of disturbances (Pavlova et al ., ; Zelenin et al ., ). Two complementary types of reticulospinal neurons were found to control posture in a particular axis of rotation – they were activated by rotation in opposite directions and produced movements generating torques counteracting the postural disturbances.…”

Dual Spinal Lesion Paradigm in the Cat: Evolution of the Kinematic Locomotor Pattern

“…A subsequent lesion of the labyrinth on the other side induced a postural reaction on the newly lesioned side, although all vestibular inputs were now absent. Later studies showed that circuit and biochemical plasticity at different level of the CNS, including the spinal cord, may contribute to vestibular compensation (Deliagina 1997a,b;Dieringer 1995;Pavlova and Deliagina 2003;Pavlova et al 2004;Straka and Dieringer 1995;Vibert et al 1999a,b). Of particular interest is a paper (Galiana et al 1984) showing how a simple change in the weighting of excitability between the vestibular nuclei could account for the Bechterew phenomenon.…”