Amphibian metamorphosis includes a complete reorganization of an organism's locomotory system from axial-based swimming in larvae to limbed propulsion in the young adult. At critical stages during this behavioural switch, larval and adult motor systems operate in the same animal, commensurate with a gradual and dynamic reconfiguration of spinal locomotor circuitry. To study this plasticity, we have developed isolated preparations of the spinal cord and brainstem from pre-to post-metamorphic stages of the amphibian Xenopus laevis, in which spinal motor output patterns expressed spontaneously or in the presence of NMDA correlate with locomotor behaviour in the freely swimming animal. Extracellular ventral root recordings along the spinal cord of pre-metamorphic tadpoles revealed motor output corresponding to larval axial swimming, whereas postmetamorphic animals expressed motor patterns appropriate for bilaterally synchronous hindlimb flexion-extension kicks. However, in vitro recordings from metamorphic climax stages, with the tail and the limbs both functional, revealed two distinct motor patterns that could occur either independently or simultaneously, albeit at very different frequencies. Activity at 0.5-1 Hz in lumbar ventral roots corresponded to bipedal extension-flexion cycles, while the second, faster pattern (2-5 Hz) recorded from tail ventral roots corresponded to larval-like swimming. These data indicate that at intermediate stages during metamorphosis separate networks, one responsible for segmentally organized axial locomotion and another for more localized appendicular rhythm generation, coexist in the spinal cord and remain functional after isolation in vitro. These preparations now afford the opportunity to explore the cellular basis of locomotor network plasticity and reconfiguration necessary for behavioural changes during development.

Brain networks memorize previous performance to adjust their output in light of past experience. These activity-dependent modifications generally result from changes in synaptic strengths or ionic conductances, and ion pumps have only rarely been demonstrated to play a dynamic role. Locomotor behavior is produced by central pattern generator (CPG) networks and modified by sensory and descending signals to allow for changes in movement frequency, intensity, and duration, but whether or how the CPG networks recall recent activity is largely unknown. In Xenopus frog tadpoles, swim bout duration correlates linearly with interswim interval, suggesting that the locomotor network retains a short-term memory of previous output. We discovered an ultraslow, minute-long afterhyperpolarization (usAHP) in network neurons following locomotor episodes. The usAHP is mediated by an activity- and sodium spike-dependent enhancement of electrogenic Na(+)/K(+) pump function. By integrating spike frequency over time and linking the membrane potential of spinal neurons to network performance, the usAHP plays a dynamic role in short-term motor memory. Because Na(+)/K(+) pumps are ubiquitously expressed in neurons of all animals and because sodium spikes inevitably accompany network activity, the usAHP may represent a phylogenetically conserved but largely overlooked mechanism for short-term memory of neural network function.

The multipolar somata of dorsolateral commissural (dlc) interneurons (Roberts and Clarke, 1982) lie in a superficial dorsolateral position in the spinal cord of Xenopus laevis embryos. By applying horseradish peroxidase to one-half of the 100 microm diameter spinal cord, these neurons have been backfilled. Their dendritic branching pattern, commissural axonal projection and distribution near the time of hatching is described. Using Lucifer yellow-filled microelectrodes a population of sensory interneurons with dlc morphology has been identified. They have multipolar somata in a dorsolateral superficial position, obliquely projecting dendrites and a ventral commissural axon. They receive presumed monosynaptic excitation in response to electrical stimulation of sensory neurites in the skin on the same side as the soma. During fictive swimming activity in curarized embryos the dlc interneurons are rhythmically inhibited in time with ventral root discharge on the same side. Dlc interneurons can fire multiple impulses and can turn on fictive swimming when stimulated by intracellular current injection. Skin stimulation is followed by excitatory postsynaptic potentials (EPSPs) in contralateral ventral rhythmic neurons. These EPSPs are reduced by the application of NMDA receptor antagonist. We conclude that dlc interneurons are excited by primary skin afferent Rohon - Beard neurons, carry sensory information across the spinal cord to excite neurons on the opposite side by release of an excitatory amino acid transmitter and participate in reflexes and in the initiation of swimming.

Vertebrate locomotion must be adaptable in light of changing environmental, organismal, and developmental demands. Much of the underlying flexibility in the output of central pattern generating (CPG) networks of the spinal cord and brain stem is endowed by neuromodulation. This review provides a synthesis of current knowledge on the way that various neuromodulators modify the properties of and connections between CPG neurons to sculpt CPG network output during locomotion.