Vestibular compensation in lampreys: impairment and recovery of equilibrium control during locomotion

Abstract

Removal of a vestibular organ (unilateral labyrinthectomy, UL) in the lamprey (Lampetra fluviatilis) results in a loss of equilibrium, so that the animal rolls (rotates around its longitudinal axis) almost continuously when swimming. This paper describes (i) UL-evoked disturbances of the pattern of locomotory movements responsible for rolling, (ii) recovery of equilibrium control after UL (vestibular compensation), and (iii) the role of vision in the recovery of equilibrium control. It was found that rolling is caused by an asymmetry in the undulatory locomotory movements, with larger deviations of the head towards the side with an intact labyrinth. The rolling appeared to be synchronized with the undulatory locomotory rhythm: during one complete roll turn (360 °), two cycles of locomotion were performed. A characteristic feature of the UL-induced motor deficit in the lamprey is the alternation of episodes of impaired swimming (with a distortion of the body shape and of the locomotor pattern and with a loss of equilibrium) with episodes of normal swimming (without any marked distortion of the locomotor pattern or loss of equilibrium). In the course of recovery after UL, the duration and frequency of the appearance of episodes of normal swimming increased, whereas episodes of impaired swimming became less frequent and shorter. The recovery of equilibrium control and the role of vision in recovery were investigated in lampreys with different combinations of lesions to the vestibular and visual sensory organs. In group 1 (UL only) animals, the time required for 80 % recovery was, on average, 33 days. In group 2 (UL and removal of both eyes) and in group 3 (UL and removal of the contralateral eye) animals, vestibular compensation was considerably retarded, and normal functioning of the roll control system was not regained even 3 months after UL. In contrast, in group 4 (UL and removal of the ipsilateral eye) animals, no impairment of the equilibrium control was observed, and the animals swam without rolling immediately after surgery. These findings indicate (i) that the visual system is important for the process of vestibular compensation, and (ii) that the deficiency in equilibrium control caused by UL can be abolished by means of unilateral (contralateral to UL) visual input. The hypothesis is advanced that the main UL-evoked motor deficit in the lamprey (loss of equilibrium) is primarily caused not by a persistent static distortion of the body shape, but by a loss of function of the roll control system responsible for stabilization of the dorsal-side-up orientation during swimming. A conceptual model of the roll control system of the lamprey, formulated in our previous studies, is used here to present arguments in favour of this hypothesis.