Géraldine von Uckermann, François M. Lambert, Denis Combes, Hans Straka and John Simmers
Locomotion in all vertebrates, including humans, requires compensatory eye and head adjustments to maintain stable gaze and avoid perturbation of visual information processing.
Here, using the amphibian Xenopus, we have addressed the issue of how effective gaze stabilization during locomotion is achieved through development at the central neural network level.
Effectively, the article builds on two previous studies (Lambert et al. (2012) Curr Biol 22: 1649-1658; von Uckermann et al. (2013) J Neurosci: 33 4253-4264) which reported for the first time how so-called “efference copies” of the spinal cord motor commands responsible for generating locomotor behavior may also be employed in driving compensatory eye movements in order to maintain visual acuity. These two papers showed, respectively, how spinal pattern generating circuitry is able to drive laterally-directed compensatory eye movements in the larval frog that swim with an undulatory, side-to-side tail motion. By contrast, in the post-metamorphic adult, bilaterally-synchronous kicking by the new hind-limbs generates linear forward motion and correspondingly, efference copy from the lumbar CPG produces convergent stabilizing eye movements.
The goal of the present study was to understand how the switch in this spino-extraocular motor coupling strategy occurs during the course of metamorphic development. In particular we aimed to evaluate the contribution of the axial (tail-swimming) CPG versus the hindlimb CPG at key transitional metamorphic stages when the animals use both tail undulatory and hind-limb kicking locomotion. By employing semi-intact and completely isolated CNS preparations associated with eye movement and motor nerve recordings our data show how a dynamic adaptive interplay between spinal locomotor and extraocular motor circuitry enables efference copies arising from either the axial or hindlimb CPGs to sustain effective gaze stabilizing movements, but with the latter becoming progressively more predominant as metamorphosis proceeds.
