Soon after birth, freely moving quadrupeds can express locomotor activity with coordinated forelimb and hindlimb movements. To investigate the neural mechanisms underlying this coordination, we used an isolated spinal cord preparation from neonatal rats. Under bath-applied 5-HT, N-methyl-D,L-aspartate (NMA), and dopamine (DA), the isolated cord generates fictive locomotion in which homolateral cervicolumbar extensor motor bursts occur in phase opposition, as does bursting in homologous (left-right) extensor motoneurons. This coordination corresponded to a walking gait monitored with EMG recordings in the freely behaving animal. Functional decoupling of the cervical and lumbar generators in vitro by sucrose blockade at the thoracic cord level revealed independent rhythmogenic capabilities with similar cycle frequencies in the two locomotor regions. When the cord was partitioned at different thoracic levels and 5-HT/NMA/DA was applied to the more caudal compartment, the ability of the lumbar generators to drive their cervical counterparts increased with the proportion of chemically exposed thoracic segments. Blockade of synaptic inhibition at the lumbar level caused synchronous bilateral lumbar rhythmicity that, surprisingly, also was able to impose bilaterally synchronous bursting at the unblocked cervical level. Furthermore, after a midsagittal section from spinal segments C1 to T7, and during additional blockade of cervical synaptic inhibition, the cord exposed to 5-HT/NMA/DA continued to produce a coordinated fictive walking pattern similar to that observed in control. Thus, in the newborn rat, a caudorostral propriospinal excitability gradient appears to mediate interlimb coordination, which relies more on asymmetric axial connectivity (both excitatory and inhibitory) between the lumbar and cervical generators than on differences in their inherent rhythmogenic capacities.

These results therefore challenge our traditional understanding of how animals offset the disruptive effects of propulsive body movements on visual processing. Specifically, our finding that predictive efference copies of intrinsic, rhythmic neural signals produced by the locomotory CPG supersede, rather than supplement, reactive vestibulo-ocular reflexes in order to drive image-stabilizing eye adjustments during larval frog swimming, represents a hitherto unreported mechanism for vertebrate ocular motor control.

In the stomatogastric nervous system (STNS) of the lobster Homarus gammarus, the rhythmic discharge of a pair of identified modulatory neurons (PS cells) is able to construct de novo a functional network from neurons otherwise belonging to other functional networks. The PS interneurons are electrically coupled and possess endogenous oscillatory properties that can be activated synaptically by stimulation of an identified sensory pathway. PS neurons themselves project synaptically onto the three major neural networks (esophageal, gastric mill, and pyloric) of the STNS. When a PS is rhythmically active in vitro, either spontaneously (rarely) or in response to direct stimulation, it dramatically restructures the otherwise independent activity patterns of all three target networks. This functional reconfiguration elicited by a single cell does not rely on changes in neuronal allegiance to pre-existing circuits, or on a simple merger of these different circuits. Rather, PS is responsible for the creation of an entirely new motor rhythm in that, via its widespread synaptic connections, the interneuron is able to subjugate the ongoing activity of the three STNS circuits and selectively appropriate individual elements to its own intrinsic rhythm. In addition, PS excites motor neurons that innervate dilator muscles of a valve situated between the esophagus and the stomach. The reorganization of the regional foregut motor rhythms by the interneuron is therefore coordinated to the opening of this valve, which itself carries sensory receptors that have been found to activate bursting in PS. Our data suggest that the role of PS in massively restructuring stomatogastric output is to generate a unique motor pattern appropriate for swallowing-like behavior. In a wider context, moreover, the results demonstrate that a neural network may not exist as a predefined entity within the CNS, but may be dynamically assembled according to changing behavioral circumstances.

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.

Adaptive behavior relies on complex neural processing in multiple interacting networks of both motor and sensory systems. One such interaction employs intrinsic neuronal signals, so-called 'corollary discharge' or 'efference copy', that may be used to predict the sensory consequences of a specific behavioral action, thereby enabling self-generated (reafferent) sensory information and extrinsic (exafferent) sensory inflow to be dissociated. Here, by using well-established examples, we seek to identify the distinguishing features of corollary discharge and efference copy within the framework of predictive motor-to-sensory system coordination. We then extend the more general concept of predictive signaling by showing how neural replicas of a particular motor command not only inform sensory pathways in order to gate reafferent stimulation, but can also be used to directly coordinate distinct and otherwise independent behaviors to the original motor task. Moreover, this motor-to-motor pairing may additionally extend to a gating of sensory input to either or both of the coupled systems. The employment of predictive internal signaling in such motor systems coupling and remote sensory input control thus adds to our understanding of how an organism's central nervous system is able to coordinate the activity of multiple and generally disparate motor and sensory circuits in the production of effective behavior.

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Effective quadrupedal locomotion requires a close coordination between the spatially distant central pattern generators (CPGs) controlling forelimb and hindlimb movements. Using isolated preparations of the neonatal rat spinal cord, we explore the role of intervening thoracic circuitry in cervicolumbar CPG coordination and the contribution to this remote coupling of limb somatosensory inputs. In preparations activated with bath-applied N-methyl-D,L-aspartate, serotonin, and dopamine, the coordination between locomotor-related bursts recorded in cervical and lumbar ventral roots was substantially weakened, although not abolished, when the thoracic segments were selectively withheld from neurochemical stimulation or were exposed to a low Ca 2ϩ solution to block synaptic transmission. Moreover, cervicolumbar CPG coordination was reduced after a thoracic midsagittal section, suggesting that cross-cord projections participate in the anteroposterior coupling. In quiescent preparations, either cyclic or tonic electrical stimulation of low-threshold afferent pathways in C8 or L2 dorsal roots (DRs) could elicit coordinated ventral root bursting at both cervical and lumbar levels via an activation of the underlying CPG networks. When lumbar rhythmogenesis was prevented by local synaptic transmission blockade, L2 DR stimulation could still drive left-right alternating cervical bursting in preparations otherwise exposed to normal bathing medium. In contrast, when the cervical generators were selectively blocked, C8 DR stimulation was unable to activate the lumbar CPGs. Thus, in the newborn rat, anteroposterior limb coordination relies on active burst generation within midcord thoracic circuitry that additionally conveys ascending and weaker descending coupling influences of distant limb proprioceptive inputs to the cervical and lumbar generators, respectively.

During active movements, neural replicas of the underlying motor commands may assist in adapting motion-detecting sensory systems to an animal's own behaviour. The transmission of such motor efference copies to the mechanosensory periphery offers a potential predictive substrate for diminishing sensory responsiveness to self-motion during vertebrate locomotion. Here, using semi-isolated in vitro preparations of larval Xenopus, we demonstrate that shared efferent neural pathways to hair cells of vestibular endorgans and lateral line neuromasts express cyclic impulse bursts during swimming that are directly driven by spinal locomotor circuitry. Despite common efferent innervation and discharge patterns, afferent signal encoding at the two mechanosensory peripheries is influenced differentially by efference copy signals, reflecting the different organization of body/water motion-detecting processes in the vestibular and lateral line systems. The resultant overall gain reduction in sensory signal encoding in both cases, which likely prevents overstimulation, constitutes an adjustment to increased stimulus magnitudes during locomotion.