Localization and organization of the central pattern generator for hindlimb locomotion in newborn rat

An in vitro preparation of newborn rat isolated brainstem/spinal cord was used in order to locate the spinal network responsible in mammals for producing patterned locomotor activity. The spinal cord was partitioned by building Vaseline walls at various lumbar levels. When a mixture of serotonin and N-methyl-D,L-aspartate was bath applied to the upper lumbar cord (L1/L2 segments), rhythmic locomotor-like activity was induced and recorded in all the lumbar segments (from L1 to L5). Conversely, when the mixture of transmitters was bath applied to the lower lumbar cord, only tonic activity was induced in the lower lumbar segments. Intracellular recordings performed on motoneurons revealed that during elicited L1/L2 locomotor-like activity, they received a rhythmic synaptic drive that was often below the threshold for spiking, because the excitability of the neurons was too low. When the L1/L2 segments were isolated, their burst production capacities remained. The network located at the L1/L2 level was found to be responsible not only for generating the rhythm but also for organizing its alternating pattern. We demonstrated that the rhythmic synaptic drive that the motoneurons receive during locomotor-like activity comes directly from the L1/L2 network and that there is no relay at the segmental level. We conclude from our study that the network that organizes locomotion in the newborn rat is not segmentally distributed but is restricted to a specific part of the cord. This finding has important consequences, since it means that it is now feasible to study the activity of the rhythmic spinal network independently from that of the motoneurons.

[1]  M. S. Berry,et al.  Criteria for distinguishing between monosynaptic and polysynaptic transmission , 1976, Brain Research.

[2]  W. Kristan,et al.  Rhythmic swimming activity in neurones of the isolated nerve cord of the leech. , 1976, The Journal of experimental biology.

[3]  F. Delcomyn Neural basis of rhythmic behavior in animals. , 1980, Science.

[4]  S. Grillner,et al.  Does the central pattern generation for locomotion in lamprey depend on glycine inhibition? , 1980, Acta physiologica Scandinavica.

[5]  S. Grillner,et al.  Activation of NMDA-receptors elicits "fictive locomotion" in lamprey spinal cord in vitro. , 1981, Acta physiologica Scandinavica.

[6]  A. Roberts,et al.  The central nervous origin of the swimming motor pattern in embryos of Xenopus laevis. , 1982, The Journal of experimental biology.

[7]  D. F. Davey,et al.  Death of motorneurons during the postnatal loss of polyneuronal innervation of rat muscles , 1983, The Journal of comparative neurology.

[8]  Jordan Lm Factors determining motoneuron rhythmicity during fictive locomotion. , 1983 .

[9]  L. Jordan Factors determining motoneuron rhythmicity during fictive locomotion. , 1983, Symposia of the Society for Experimental Biology.

[10]  J. Clarke,et al.  Initiation and control of swimming in amphibian embryos. , 1983, Symposia of the Society for Experimental Biology.

[11]  R. Harris-Warrick,et al.  Strychnine eliminates alternating motor output during fictive locomotion in the lamprey , 1984, Brain Research.

[12]  S. Grillner Neurobiological bases of rhythmic motor acts in vertebrates. , 1985, Science.

[13]  A. Iriki,et al.  Localization of central rhythm generator involved in cortically induced rhythmical masticatory jaw-opening movement in the guinea pig. , 1986, Journal of neurophysiology.

[14]  C. Jahr,et al.  Ia afferent excitation of motoneurones in the in vitro new‐born rat spinal cord is selectively antagonized by kynurenate. , 1986, The Journal of physiology.

[15]  N. Kudo,et al.  N-Methyl-d,l-aspartate-induced locomotor activity in a spinal cord-indlimb muscles preparation of the newborn rat studied in vitro , 1987, Neuroscience Letters.

[16]  S. Soffe Ionic and pharmacological properties of reciprocal inhibition in Xenopus embryo motoneurones. , 1987, The Journal of physiology.

[17]  C. Buisseret-Delmas,et al.  An attempt to localize the lumbar locomotor generator in the rabbit using 2-deoxy-[14C]glucose autoradiography , 1988, Neuroscience Letters.

[18]  J. P. Lund The generation of mastication by the mammalian central nervous system , 1988 .

[19]  R. A. Davidoff Neural Control of Rhythmic Movements in Vertebrates , 1988, Neurology.

[20]  J. C. Smith,et al.  Neural mechanisms generating locomotion studied in mammalian brain stem‐spinal cord in vitro , 1988, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[21]  P. Stein,et al.  Spinal cord segments containing key elements of the central pattern generators for three forms of scratch reflex in the turtle , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  F. Clarac,et al.  Two types of motor rhythm induced by NMDA and amines in an in vitro spinal cord preparation of neonatal rat , 1990, Neuroscience Letters.

[23]  A. Chrachri,et al.  Fictive locomotion in the fourth thoracic ganglion of the crayfish, Procambarus clarkii , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  F. Clarac,et al.  Variability as a characteristic of immature motor systems: an electromyographic study of swimming in the newborn rat , 1990, Behavioural Brain Research.

[25]  F. Clarac,et al.  A cooling/heating system for use with in vitro preparations: study of temperature effects on newborn rat rhythmic activities , 1991, Journal of Neuroscience Methods.

[26]  S. Grillner,et al.  The neural network underlying locomotion in lamprey-synaptic and cellular mechanisms , 1991, Neuron.

[27]  H. Hultborn,et al.  Induction of fos expression by activity in the spinal rhythm generator for scratching , 1992, Brain Research.

[28]  A. Lev-Tov,et al.  In vitro studies of prolonged synaptic depression in the neonatal rat spinal cord. , 1992, The Journal of physiology.

[29]  F. Clarac,et al.  Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. , 1992, The Journal of physiology.

[30]  Michael J. O'Donovan,et al.  Regionalization and intersegmental coordination of rhythm-generating networks in the spinal cord of the chick embryo , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  F. Clarac,et al.  Oscillatory properties of the central pattern generator for locomotion in neonatal rats. , 1993, Journal of neurophysiology.

[32]  Keith T. Sillar,et al.  Physiological and developmental aspects of intersegmental coordination in Xenopus embryos and tadpoles , 1993 .

[33]  O. Kiehn,et al.  Sulphorhodamine‐labelled cells in the neonatal rat spinal cord following chemically induced locomotor activity in vitro. , 1994, The Journal of physiology.