Abstract
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.
Highlights
Rhythmic movements of animals arise from coordinated assemblies of local neuronal networks, so-called ‘‘central pattern generators’’ (CPGs), which produce rhythmically-recurring patterns of motor output [1,2] that are continuously adjusted by sensory information [3]
By taking advantage of the profound remodeling of spinal locomotor circuitry that occurs during metamorphosis ([11]; Figure 8A), we have found that following unilateral labyrinthectomy (UL) in late pre-metamorphosis, the distributed spinal networks controlling adult hindlimb propulsive movements and body orientation have become asymmetrically coordinated, suggesting the involvement of compensatory processes in the construction of the underlying connectivity during metamorphosis (Figure 8C)
The same vestibular lesion made in juvenile frogs after metamorphosis had terminated did not lead to an adaptive network response during subsequent maturation to adulthood, and swimming in these animals remained permanently impaired (Figure 8B)
Summary
Rhythmic movements of animals arise from coordinated assemblies of local neuronal networks, so-called ‘‘central pattern generators’’ (CPGs), which produce rhythmically-recurring patterns of motor output [1,2] that are continuously adjusted by sensory information [3] Amongst such sensory cues in vertebrates, vestibular information is involved in the control of locomotor and postural behavior [4] as well as corrective eye movements [5]. Vestibular compensation, which has been proposed to account for such functional restorations in terrestrial species (see [7]), consists of a gradual re-equilibration of activity in the brainstem vestibular nuclei of the two sides and implicates the use of body proprioceptive information ascending from the spinal cord (see [8]) Such compensatory plasticity has been extensively studied in brainstem nuclei, surprisingly very little is known about the long-term effects of a vestibular lesion on downstream locomotor networks in the spinal cord
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