Vestibular Lesion-Induced Developmental Plasticity in Spinal Locomotor Networks during Xenopus laevis Metamorphosis
PLoS ONE. 2013-08-12; 8(8): e71013
DOI: 10.1371/journal.pone.0071013
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During frog metamorphosis, the vestibular sensory system remains unchanged, while
spinal motor networks undergo a massive restructuring associated with the
transition from the larval to adult biomechanical system. We investigated in
Xenopus laevis the impact of a pre- (tadpole stage) or post-metamorphosis
(juvenile stage) unilateral labyrinthectomy (UL) on young adult swimming
performance and underlying spinal locomotor circuitry. The acute disruptive
effects on locomotion were similar in both tadpoles and juvenile frogs. However,
animals that had metamorphosed with a preceding UL expressed restored swimming
behavior at the juvenile stage, whereas animals lesioned after metamorphosis
never recovered. Whilst kinematic and electrophysiological analyses of the
propulsive system showed no significant differences in either juvenile group, a
3D biomechanical simulation suggested that an asymmetry in the dynamic control of
posture during swimming could account for the behavioral restoration observed in
animals that had been labyrinthectomized before metamorphosis. This hypothesis
was subsequently supported by in vivo electromyography during free swimming and
in vitro recordings from isolated brainstem/spinal cord preparations.
Specifically, animals lesioned prior to metamorphosis at the larval stage
exhibited an asymmetrical propulsion/posture coupling as a post-metamorphic young
adult. This developmental alteration was accompanied by an ipsilesional decrease
in propriospinal coordination that is normally established in strict left-right
symmetry during metamorphosis in order to synchronize dorsal trunk muscle
contractions with bilateral hindlimb extensions in the swimming adult. Our data
thus suggest that a disequilibrium in descending vestibulospinal information
during Xenopus metamorphosis leads to an altered assembly of adult spinal
locomotor circuitry. This in turn enables an adaptive compensation for the
dynamic postural asymmetry induced by the vestibular imbalance and the
restoration of functionally-effective behavior.