Ubiquity of motor networks in the spinal cord of vertebrates
Introduction
Most animals need to move to find food, sexual partners and to escape from predators. This necessity for movement led to the establishment, during evolution, of several locomotor strategies adapted to the life medium of the animals. In vertebrates, such as fishes or snakes, propulsion is sustained by rhythmic undulatory trunk movements while bipeds or quadrupeds locomote using rhythmic coordinated movements of the limbs. Some “transitional” organisms, as for example the newt, can adopt either locomotor strategy depending on the medium. In terrestrial mammals, it appears that the biomechanical processes underlying locomotion can not solely be described by alternating limb movements but also require complex coordinated trunk movements and postural regulation. The neuronal basis for these various kinds of rhythmic motor behaviours have been studied throughout the vertebrate phylum. An understanding that the motor patterns are centrally generated in the spinal cord by specific neuronal networks called central pattern generators (CPGs) has emerged.
The motor patterns generated by the spinal cord are varied and extend from phrenic bursts to limb movements. The aim of this review is to focus on locomotion-related networks and to describe the interactions between such neuronal assemblies. Special attention will be given to results obtained in the in vitro neonatal rat spinal cord preparation.
Section snippets
Different forms of rhythmic motor activities generated in the spinal cord
Two kinds of rhythmic motor patterns are generated by the spinal cord. First, there are motor patterns such as controlling forelimb and hindlimb movements (for review see [34]), swimming 33, 44, flying [54], hatching (for review see [3]), scratching, paw-shake [62] (for a review on scratching and paw-shake see [57]), and trunk muscle movements [31]. This is not an exhaustive list but includes the more commonly studied motor behaviours. Second, there are postural patterns which are under strong
The neonatal rat spinal cord preparation
Before describing the coupling between neuronal networks, we will briefly introduce the neonatal rat spinal cord preparation (Fig. 1A), which allows us to study these various motor networks under isolating conditions. Over the last 10 years, the isolated spinal cord of the neonatal rat has been used to study both the developmental aspects and the cellular bases of locomotor activity. In this preparation, locomotor like activity can be elicited by bath-application of various neurotransmitters
Interactions between spinal motor networks
Distinct neuronal networks are thought to underlie different motor activities. The networks that subserve these various motor activities, however, do not normally operate in isolation but interact with each other, according to behavioural needs. Interactions within the spinal cord are probably complex and to date, little information is available concerning the coupling between the different motor networks.
Generation of motor pattern by specialized networks
The spinal cord consists of multiple networks each of them with its own specificity, that can share neuronal elements. Virtually all spinal levels are susceptible to exhibit rhythmic activation and the various neuronal networks will be active according to their particular and specific properties during motor tasks. The question that arises is to know if all spinal segments in the cord possess the same capabilities to generate motor patterns or if some contain key elements for one type of motor
Conclusion
Various findings indicate that the spinal cord in quadrupeds is not an homogeneous chain of equipotent networks, as it is the case for example in organisms which exhibit an anguilliform swimming such as lamprey 32, 33. On one side one should consider the activity recorded at the segmental level for back muscle activity along the axis of the body and. On the other side more specialized areas corresponding to hindlimbs will largely influence the functioning of the trunk muscles. As revealed by
Acknowledgements
The authors warmly thank Dr. C. E. Gee for critical reading of the manuscript and correcting the language.
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Probing spinal circuits controlling walking in mammals
2010, Biochemical and Biophysical Research CommunicationsCitation Excerpt :These neurons are the Pitx2+ and acetylcholinergic neurons, called V0C, since they are derived from the V0 population. V0C neurons are shown to be the exclusive source of the well-known large acetylcholinergic C-boutons that were first discovered on motor neurons more than 40 years ago [66]. The V0C neurons are rhythmically active during locomotor-like activity and genetic inactivation of these cells reduces the amplitude of the locomotor output in a task-dependent way [26].
Distributed neural networks for controlling human locomotion. Lessons from normal and SCI subjects
2009, Brain Research BulletinCitation Excerpt :However, opinions diverge as to whether the mammalian CPGs are localized or distributed [49,64], and the details of such circuitry in the human spinal cord are still largely unknown [8,17,22,28,51,59,83]. A major site for CPG activity in the upper lumbar segments may serve a pace-maker role, together with other, perhaps separate generator sites in more caudal segments [9,50,55]. The cervical segments of the cord also contain pattern-generating oscillators for coordinating the upper limbs.
Plasticity properties of CPG circuits in humans: Impact on gait recovery
2009, Brain Research BulletinCitation Excerpt :Numerous evidence in experimental models as well as in humans indicates that CPG circuits are indeed innate. On the other hand, controversy exist on the exact location of the CPG circuits and recent research in humans [16,38] and in animal models [4,6] indicated that spinal CPG circuits may not be localized but distributed throughout the spinal cord (see also Ivanenko, this issue). This lack of precise localization of CPG properties, at least in the spinal cord, question what is innate in CPG circuits.
Coordinated network functioning in the spinal cord: An evolutionary perspective
2006, Journal of Physiology ParisCitation Excerpt :Based on behavioural experiments first performed on neonatal rats during swimming, where a strong coordination exists between fore- and hindlimb EMG rhythmic activities (Cazalets et al., 1990), the spinal localisation of the forelimb locomotor generators was later investigated in spinal cord preparations in vitro. When chemically activated by neuroactive agents such as NMA and serotonin (Fig. 4B), rhythmic ventral root activity was found to be generated at the cervical (C8) level of the cord and in an in-phase coordination with homolateral lumbar (L5) output, similar to that observed in the freely moving animal (Cazalets and Bertrand, 2000b; Juvin et al., 2005). Using a partitioned spinal cord preparation that restricts the superfusion of NMDA/5-HT to the cervico-thoracic levels, synchronous bursting was found to occur in homolateral C7 to T1 ventral roots (extensor motoneurons), and an alternation with both the contralateral side of the cord and homolateral C3–C5 roots (flexor motoneurons, Fig. 4B, Ballion et al., 2001).
The early development of motor control in neonate rat
2006, Comptes Rendus - PalevolCitation Excerpt :The coordinated firing of the motoneurons controlling these muscles is organised at the level of the spinal cord by neural networks, called central pattern generators (CPG) [68]. A rostral CPG, located between C7-T1, controls the fore limbs [3], and a lumbar CPG, located between L1–L5 controls the hind limbs [13,14,36]. CPGs are made of two lateral hemi-neural networks, that rhythmically stimulate a pool of motoneurons through glutamatergic synapses and inhibit the motoneurons of the ipsilateral antagonist muscles and the contralateral agonist muscles through glycinergic commissural interneurons (see [26] for a recent review).
Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord
2003, Progress in Neurobiology
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Present address: Université de Montréal, Dépt de Physiologie, CP 6128, succ. Centre Ville H3C 3J7 Montréal, Quebec, Canada.