Metamorphosis-Induced Changes in the Coupling of Spinal Thoraco-Lumbar Motor Outputs During Swimming in Xenopus laevis

Université de Bordeaux, Centre National de la Recherche Scientifique, Laboratoire Mouvement Adaptation Cognition (UMR 5227) Bordeaux, France.
Journal of Neurophysiology (Impact Factor: 2.89). 08/2008; 100(3):1372-83. DOI: 10.1152/jn.00023.2008
Source: PubMed


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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    • "In several systems, interactions between distinct rhythmically active networks have been also described, as for example between walking and swimmeret movements in crustaceans (Cattaert and Clarac, 1983; Chrachri and Neil, 1993), gastric and pyloric motor rhythms in the crustacean stomatogastric system (Bartos et al., 1999; Faumont et al., 2005), trunk and hindlimb activities in Xenopus (Beyeler et al., 2008; Rauscent et al., 2009), locomotion and respiration (Kawahara et al., 1989; Morin and Viala, 2002), scratching and locomotion (Hao et al., 2011), respiration and swallowing (Gestreau et al., 2000). In the newt, axial neuronal networks switch from sequential motor burst propagation to stationary phase-locked activation of the same axial muscles when the animal switches from swimming to quadrupedal locomotion (Delvolve et al., 1997). "
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    ABSTRACT: Studies devoted to understanding locomotor control have mainly addressed the functioning of the neural circuits controlling leg movements and relatively little is known of the operation of networks that activate trunk muscles in coordination with limb movements. The aim of the present work was (1) to identify the exogenous neurotransmitter cocktail that most strongly activates postural thoracic circuitry; (2) to investigate how the biogenic amines serotonin (5-HT), dopamine (DA), and noradrenaline (NA) modulate the coordination between limb and axial motor networks. Experiments were carried out on in vitro isolated spinal cord preparations from newborn rats. We recorded from ventral roots to monitor hindlimb locomotor and axial postural network activity. Each combination of the three amines with excitatory amino acids (EAAs) elicited coordinated rhythmic motor activity at all segmental levels with specific characteristics. The variability in cycle period was similar with 5-HT and DA while it was significantly higher with NA. DA elicited motor bursts of smaller amplitude in thoracic segments compared to 5-HT and NA, while both DA and NA elicited motor bursts of higher amplitude than 5-HT in the lumbar and sacral segments. The amines modulated the phase relationships of bursts in various segments with respect to the reference lumbar segment. At the thoracic level there was a phase lag between all recorded segments in the presence of 5-HT, while DA and NA elicited synchronous bursting. At the sacral level, 5-HT and DA induced an intersegmental phase shift while relationships became phase-locked with NA. Various combinations of EAAs with two or even all three amines elicited rhythmic motor output that was more variable than with one amine alone. Our results provide new data on the coordinating processes between spinal cord networks, demonstrating that each amine has a characteristic "signature" regarding its specific effect on intersegmental phase relationships.
    Frontiers in Neural Circuits 08/2014; 8:99. DOI:10.3389/fncir.2014.00099 · 3.60 Impact Factor
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    • "At the spinal level, this locomotor-related efference signal also appears to be essential for coordinating back and limb muscle contractions during appendicular swimming or quadrupedal walking. For instance in Xenopus froglets, postural adjustments are mediated by projections that ascend from the hindlimb lumbar CPG to the thoracic spinal circuitry controlling the trunk musculature [53]. Similarly, in neonatal rats, lumbar locomotor CPG-related commands have been found to coordinate trunk curvature with hindlimb stepping [54] and also to contribute to interlimb coordination during locomotion by means of coupling between the lumbar pattern generator and its cervical counterpart [24], [34]. "
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    ABSTRACT: During exercise and locomotion, breathing rate rapidly increases to meet the suddenly enhanced oxygen demand. The extent to which direct central interactions between the spinal networks controlling locomotion and the brainstem networks controlling breathing are involved in this rhythm modulation remains unknown. Here, we show that in isolated neonatal rat brainstem-spinal cord preparations, the increase in respiratory rate observed during fictive locomotion is associated with an increase in the excitability of pre-inspiratory neurons of the parafacial respiratory group (pFRG/Pre-I). In addition, this locomotion-induced respiratory rhythm modulation is prevented both by bilateral lesion of the pFRG region and by blockade of neurokinin 1 receptors in the brainstem. Thus, our results assign pFRG/Pre-I neurons a new role as elements of a previously undescribed pathway involved in the functional interaction between respiratory and locomotor networks, an interaction that also involves a substance P-dependent modulating mechanism requiring the activation of neurokinin 1 receptors. This neurogenic mechanism may take an active part in the increased respiratory rhythmicity produced at the onset and during episodes of locomotion in mammals.
    PLoS ONE 02/2014; 9(2):e89670. DOI:10.1371/journal.pone.0089670 · 3.23 Impact Factor
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    • "From stage 59 to the metamorphic climax, Xenopus still employs axial swimming until the tail is resorbed, although the limbs are by now fully functional and contribute actively to propulsion, either independently or in combination with the tail-based system (see Fig. 3). Here again, the isolated spinal cord of such transitional animals continues to generate spontaneously the motor rhythms that underlie the variable operation of the two coexisting locomotor systems in vivo (Combes et al., 2004; Beyeler et al., 2008). Thus, these in vitro patterns may consist of the faster axial rhythm occurring alone or more often in combination with the slower appendicular rhythm. "
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    ABSTRACT: The amphibian Xenopus laevis represents a highly amenable model system for exploring the ontogeny of central neural networks, the functional establishment of sensory-motor transformations, and the generation of effective motor commands for complex behaviors. Specifically, the ability to employ a range of semi-intact and isolated preparations for in vitro morphophysiological experimentation has provided new insights into the developmental and integrative processes associated with the generation of locomotory behavior during changing life styles. In vitro electrophysiological studies have begun to explore the functional assembly, disassembly and dynamic plasticity of spinal pattern generating circuits as Xenopus undergoes the developmental switch from larval tail-based swimming to adult limb-based locomotion. Major advances have also been made in understanding the developmental onset of multisensory signal processing for reactive gaze and posture stabilizing reflexes during self-motion. Additionally, recent evidence from semi-intact animal and isolated CNS experiments has provided compelling evidence that in Xenopus tadpoles, predictive feed-forward signaling from the spinal locomotor pattern generator are engaged in minimizing visual disturbances during tail-based swimming. This new concept questions the traditional view of retinal image stabilization that in vertebrates has been exclusively attributed to sensory-motor transformations of body/head motion-detecting signals. Moreover, changes in visuomotor demands associated with the developmental transition in propulsive strategy from tail- to limb-based locomotion during metamorphosis presumably necessitates corresponding adaptive alterations in the intrinsic spinoextraocular coupling mechanism. Consequently, Xenopus provides a unique opportunity to address basic questions on the developmental dynamics of neural network assembly and sensory-motor computations for vertebrate motor behavior in general.
    Developmental Neurobiology 04/2012; 72(4):649-63. DOI:10.1002/dneu.20965 · 3.37 Impact Factor
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