Spinal efference copy signaling and gaze stabilization during locomotion in juvenile Xenopus frogs.

G. von Uckermann, D. Le Ray, D. Combes, H. Straka, J. Simmers
Journal of Neuroscience. 2013-03-06; 33(10): 4253-4264
DOI: 10.1523/jneurosci.4521-12.2013

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In swimming Xenopus laevis tadpoles, gaze stabilization is achieved by efference
copies of spinal locomotory CPG output that produce rhythmic extraocular motor
activity appropriate for minimizing motion-derived visual disturbances. During
metamorphosis, Xenopus switches its locomotory mechanism from larval tail-based
undulatory movements to bilaterally synchronous hindlimb kick propulsion in the
adult. The change in locomotory mode leads to body motion dynamics that no longer
require conjugate left-right eye rotations for effective retinal image
stabilization. Using in vivo kinematic analyses, in vitro electrophysiological
recordings and specific CNS lesions, we have investigated spino-extraocular motor
coupling in the juvenile frog and the underlying neural pathways to understand
how gaze control processes are altered in accordance with the animal’s change in
body plan and locomotor strategy. Recordings of extraocular and limb motor nerves
during spontaneous “fictive” swimming in isolated CNS preparations revealed that
there is indeed a corresponding change in spinal efference copy control of
extraocular motor output. In contrast to fictive larval swimming where
alternating bursts occur in bilateral antagonistic horizontal extraocular nerves,
during adult fictive limb-kicking, these motor nerves are synchronously active in
accordance with the production of convergent eye movements during the linear head
accelerations resulting from forward propulsion. Correspondingly, the neural
pathways mediating spino-extraocular coupling have switched from contralateral to
strictly ipsilateral ascending influences that ensure a coactivation of bilateral
extraocular motoneurons with synchronous left-right limb extensions. Thus,
adaptive developmental plasticity during metamorphosis enables spinal CPG-driven
extraocular motor activity to match the changing requirements for eye movement
control during self-motion.

DOI: 10.1523/JNEUROSCI.4521-12.2013
PMCID: PMC6704964
PMID: 23467343 [Indexed for MEDLINE]

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