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

Abstract

Beyeler A, Métais C, Combes D, Simmers J, Le Ray D. Metamorphosis-induced changes in the coupling of spinal thoraco-lumbar motor outputs during swimming in Xenopus laevis. J Neurophysiol 100: 1372-1383, 2008. First published July 2, 2008 doi:10.1152/jn.00023.2008. 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.

Opposing Aminergic Modulation of Distinct Spinal Locomotor Circuits and Their Functional Coupling during Amphibian Metamorphosis

“…First, observations and myographic recordings in freely behaving Xenopus at metamorphic climax (Beyeler et al, 2008) indicated that during this critical transitional period the animal is capable of different modes of locomotion according to how far and how fast it wishes to swim, with both the primary tail-based and secondary limb-based systems participating either independently or conjointly in swimming behavior. In the latter condition, moreover, the two locomotor modes may be expressed in distinct rhythms with very different frequencies, or when higher velocities are required, tail oscillations and rhythmic hindlimb kicking occur at the same frequency in cooperative propulsive action.…”

Adaptive plasticity of spino-extraocular motor coupling during locomotion in metamorphosing Xenopus laevis

“…2B). After isolation in vitro, the brainstem/spinal cord of such animals during this transitional period continues to spontaneously generate the motor burst patterns that would normally drive axial or hindlimb muscle contractions underlying the two locomotor modes in vivo (Combes et al, 2004;Beyeler et al, 2008;Rauscent et al, 2009). As seen in the extracellular recordings of Fig.…”

“…To exclude any remaining body-/world motion-related sensory inputs, both optic nerves were transected and the bilateral vestibular endorgans were ablated. The spinal cord and ventral roots (VRs) were exposed until segments 20-25 and motor nerve branches innervating the hindlimb tibialis anterior (ankle flexor, Flex) and plantaris longus (ankle extensor, Ext) muscles, respectively (Beyeler et al, 2008) were identified according to their muscle targets and also dissected free. The rest of the tail and trunk was carefully removed and the isolated preparation (brainstem/spinal cord with the attached spinal motor nerves and extraocular motor innervation of the eyes) was transferred to a Sylgard-lined recording chamber after rinsing in fresh saline.…”

“…While alternating horizontal angular head accelerations predominate during larval tail-based swimming, hindlimb kick propulsion in adult frogs produces mostly translational accelerations (Beyeler et al, 2008;Lambert et al, 2012;von Uckermann et al, 2013). An estimation of the spatio-temporal adequacy of the resultant eye movements during single or combined locomotor modes at metamorphic climax can be made by comparing extraocular motor responses during such self-generated motion with the characteristics of angular and linear vestibulo-ocular reflexes arising from passively imposed motion .…”

“…By contrast, during post-metamorphic adult swimming produced by bilaterally synchronous hindlimb kicking, resultant head/body movements now consist of linear forward accelerations and decelerations during the powerstroke (extension) and returnstroke (flexion) phases, respectively, of each kick cycle (Combes et al, 2004;Beyeler et al, 2008). This in turn requires spino-extraocular motor coupling to generate bilaterally synchronous horizontal extraocular nerve activity for vergent eye motion (von Uckermann et al, 2013) to offset the disruptive visual effects of longitudinal translational forward motion (Rohregger and Dieringer, 2002).…”