Metamorphosis-induced changes in the coupling of spinal thoraco-lumbar motor outputs during swimming in Xenopus laevis

Anna Beyeler, Charles Métais, Denis Combes, John Simmers, Didier Le Ray
Journal of Neurophysiology. 2008-09-01; 100(3): 1372-1383
DOI: 10.1152/jn.00023.2008

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Anuran metamorphosis includes a complete remodeling of the animal’s biomechanical
apparatus, requiring a corresponding functional reorganization of underlying
central neural circuitry. This involves changes that must occur in the
coordination between the motor outputs of different spinal segments to harmonize
locomotor and postural functions as the limbs grow and the tail regresses. In
premetamorphic Xenopus laevis tadpoles, axial motor output drives rostrocaudally
propagating segmental myotomal contractions that generate propulsive body
undulations. During metamorphosis, the anterior axial musculature of the tadpole
progressively evolves into dorsal muscles in the postmetamorphic froglet in which
some of these back muscles lose their implicit locomotor function to serve
exclusively in postural control in the adult. To understand how locomotor and
postural systems interact during locomotion in juvenile Xenopus, we have
investigated the coordination between postural back and hindlimb muscle activity
during free forward swimming. Axial/dorsal muscles, which contract in bilateral
alternation during undulatory swimming in premetamorphic tadpoles, change their
left-right coordination to become activated in phase with bilaterally synchronous
hindlimb extensions in locomoting juveniles. Based on in vitro
electrophysiological experiments as well as specific spinal lesions in vivo, a
spinal cord region was delimited in which propriospinal interactions are directly
responsible for the coordination between leg and back muscle contractions. Our
findings therefore indicate that dynamic postural adjustments during adult
Xenopus locomotion are mediated by local intraspinal pathways through which the
lumbar generator for hindlimb propulsive kicking provides caudorostral commands
to thoracic spinal circuitry controlling the dorsal trunk musculature.

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