Vestibular compensation in lampreys: role of vision at different stages of recovery of equilibrium control.

The main motor disorder evoked by unilateral labyrinthectomy (UL) in the lamprey (Lampetra fluviatilis) is a complete loss of equilibrium and rolling (rotation about the longitudinal axis) during swimming. A previous study has shown that the recovery of equilibrium control in the lamprey takes, on average, 33 days. However, lampreys were able to maintain equilibrium if UL was combined with removal of the ipsilateral eye ('surgical compensation' of the vestibular deficit). It was suggested that tonic excitatory inflow, rather than specific information about the orientation of the animal in space delivered by the remaining eye, is important for the recovery of equilibrium control. In the present study, a number of experiments were designed to test this hypothesis. It was found that illumination of the eye contralateral to the UL or continuous electrical stimulation (10 Hz) of the corresponding optic nerve resulted in immediate restoration of equilibrium control. The same result was obtained when the vestibular nerve on the UL side was stimulated. Thus, the roll control system in the lamprey, driven by only one labyrinth, is able to maintain equilibrium provided that the lack of tonic inflow from the missing labyrinth is compensated for by tonic vestibular or visual input. The present study has also shown that the importance of visual input for maintaining equilibrium after UL decreases with time. In animals that achieved a high degree of compensation, removal of the eyes on day 23 after UL evoked decompensation, whereas removal on day 70 did not. A reduction of the significance of visual input was also observed in surgically compensated UL lampreys. In these animals, removal of the remaining eye on days 1-3 after the first surgery resulted in a complete loss of equilibrium, removal on day 7 resulted in a partial loss, whereas removal on days 48-55 did not affect the postural stability. Three lines of evidence suggest that asymmetrical visual input evokes plastic changes in the roll control system. (i) In one group of animals, initially one eye was removed, and then 50 days later the labyrinth ipsilateral to the missing eye and remaining eye were removed. These animals exhibited a mild impairment of equilibrium control, in contrast to the animals in which both surgeries were performed simultaneously. (ii) In another group of animals, initially one eye was removed, and then 50 days later the remaining eye and both labyrinths were removed. These animals exhibited rolling towards the eye that remained intact for longer. (iii) A short-term electrical stimulation (5-10 min daily for 3 days) of the optic nerve (contralateral to UL) in blinded animals considerably improved the equilibrium control compared with that of non-stimulated animals; the improvement was observed for 60 days after stimulation.