Serotonin modulates the central pattern generator for locomotion in the isolated lamprey spinal cord.

The central pattern generator for locomotion in the spinal cord of the lamprey can be activated in vitro by the addition of D-glutamate to the bathing saline. Serotonin has no effects when bath-applied alone, but it modulates the D-glutamate-activated swimming pattern. Three major effects are observed: a dose-dependent reduction in the frequency of rhythmic ventral root burst discharge; enhancement of the intensity of burst discharge, due in part to the recruitment of previously inactive motoneurones; prolongation of the intersegmental phase lag. Motoneurone activation appears to result from enhanced synaptic drive from the central pattern generator; no direct effects of serotonin on the motoneurones themselves (resting potential, input resistance or threshold for action potential generation) were observed. Theoretical and experimental studies suggest that the prolongation of the intersegmental phase lag results at least in part from differential effects of serotonin on segmental oscillators in different parts of the spinal cord. Isolated caudal pieces of the cord were more strongly affected by serotonin than isolated rostral pieces. We propose that serotonin may be an endogenous modulator of the central pattern generator for locomotion in the lamprey. It may have a role in the generation of a family of related undulatory movements (swimming, crawling, burrowing) by a single central pattern generator.

[1]  Shik Ml,et al.  Control of walking and running by means of electric stimulation of the midbrain , 1966 .

[2]  D. M. Wilson.  Central nervous mechanisms for the generation of rhythmic behaviour in arthropods. , 1966, Symposia of the Society for Experimental Biology.

[3]  G. Orlovsky.  The effect of different descending systems on flexor and extensor activity during locomotion. , 1972, Brain research.

[4]  S. Barasi,et al.  THE MODIFICATION OF LUMBAR MOTONEURONE EXCITABILITY BY STIMULATION OF A PUTATIVE 5‐HYDROXYTRYPTAMINE PATHWAY , 1974, British journal of pharmacology.

[5]  S. Rossignol,et al.  Phase dependent reflex reversal during walking in chronic spinal cats , 1975, Brain Research.

[6]  S. Grillner,et al.  On the Generation and Performance of Swimming in Fish , 1976 .

[7]  Laurent Descarries,et al.  Quantitative data on serotonin nerve terminals in adult rat neocortex , 1976, Brain Research.

[8]  Warren O. Wickelgren,et al.  Physiological and anatomical characteristics of reticulospinal neurones in lamprey , 1977 .

[9]  L. Descarries,et al.  Serotonin nerve terminals in the locus coeruleus of adult rat: A radioautographic study , 1978, Brain Research.

[10]  C. C. Boylls.  Prolonged alterations of muscle activity induced in locomoting premammillary cats by microstimulation of the inferior olive , 1978, Brain Research.

[11]  P. Stein.  Motor systems, with specific reference to the control of locomotion. , 1978, Annual review of neuroscience.

[12]  A. Beaudet,et al.  The monoamine innervation of rat cerebral cortex: Synaptic and nonsynaptic axon terminals , 1978, Neuroscience.

[13]  Masao Udo,et al.  Hyperflexion and changes in interlimb coordination of locomotion induced by cooling of the cerebellar intermediate cortex in normal cats , 1979, Brain Research.

[14]  S H Snyder,et al.  Multiple serotonin receptors: differential binding of [3H]5-hydroxytryptamine, [3H]lysergic acid diethylamide and [3H]spiroperidol. , 1979, Molecular pharmacology.

[15]  C. Rovainen.  Neurobiology of lampreys. , 1979, Physiological reviews.

[16]  F. Zajac,et al.  Effects of stimulalating Deiters' nucleus and memdial longitudinal fasciculus on the timing of the fictive locomotor rhythm induced in cats by DOPA , 1979, Brain Research.

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

[18]  M. Roberts,et al.  The responses of motoneurones to 5-hydroxytryptamine , 1980, Neuropharmacology.

[19]  M. Roberts,et al.  THE EFFECTS OF CHRONIC SECTION OF DORSAL ROOTS ON THE RESPONSIVENESS OF MOTONEURONES TO 5‐HYDROXYTRYPTAMINE AND A SUBSTANCE P ANALOGUE , 1981, British journal of pharmacology.

[20]  S. Grillner.  Control of Locomotion in Bipeds, Tetrapods, and Fish , 1981 .

[21]  S. Snyder,et al.  Two distinct central serotonin receptors with different physiological functions. , 1981, Science.

[22]  H. Yamamura,et al.  Discrimination of Multiple [3H]5‐Hydroxytryptamine Binding Sites by the Neuroleptic Spiperone in Rat Brain , 1981, Journal of neurochemistry.

[23]  J. Buchanan,et al.  Activities of identified interneurons, motoneurons, and muscle fibers during fictive swimming in the lamprey and effects of reticulospinal and dorsal cell stimulation. , 1982, Journal of neurophysiology.

[24]  I. Cooke,et al.  6 – Hormones and Neurosecretion , 1982 .

[25]  P. Holmes,et al.  The nature of the coupling between segmental oscillators of the lamprey spinal generator for locomotion: A mathematical model , 1982, Journal of mathematical biology.

[26]  S. Grillner,et al.  On peripheral control mechanisms acting on the central pattern generators for swimming in the dogfish. , 1982, The Journal of experimental biology.

[27]  Y. Jan,et al.  Peptidergic transmission in sympathetic ganglia of the frog. , 1982, The Journal of physiology.

[28]  G. Augustine,et al.  Amine modulation of the neurogenic Limulus heart. , 1982, Journal of neurobiology.

[29]  S. Peroutka,et al.  Recognition of multiple serotonin receptor binding sites. , 1982, Advances in biochemical psychopharmacology.

[30]  P. Monroe,et al.  Characterization of Multiple [3H]5–Hydroxytryptamine Binding Sites in Rat Spinal Cord Tissue , 1983, Journal of neurochemistry.

[31]  D. Maxwell,et al.  Fine structure of serotonin-containing axons in the marginal zone of the rat spinal cord , 1983, Brain Research.

[32]  P. Wallén,et al.  On the control of myotomal motoneurones during "fictive swimming" in the lamprey spinal cord in vitro. , 1983, Acta physiologica Scandinavica.

[33]  G. Carpenter,et al.  Which behavior does the lamprey central motor program mediate? , 1983, Science.

[34]  W. Kristan,et al.  Neurons controlling the initiation, generation and modulation of leech swimming. , 1983, Symposia of the Society for Experimental Biology.

[35]  R. Neuman,et al.  Pharmacological antagonism of facilitatory but not inhibitory effects of serotonin and norepinephrine on excitability of spinal motoneurons , 1983, Neuropharmacology.

[36]  R. Harris-Warrick,et al.  Serotonergic innervation and modulation of the stomatogastric ganglion of three decapod crustaceans (Panulirus interruptus, Homarus americanus and Cancer irroratus). , 1984, The Journal of experimental biology.

[37]  R. Harris-Warrick,et al.  Cellular mechanisms for modulation of posture by octopamine and serotonin in the lobster , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  S. Rossignol,et al.  Phase-dependent responses evoked in limb muscles by stimulation of medullary reticular formation during locomotion in thalamic cats. , 1984, Journal of neurophysiology.

[39]  S. Grillner,et al.  The edge cell, a possible intraspinal mechanoreceptor. , 1984, Science.

[40]  P. Wallén,et al.  Fictive locomotion in the lamprey spinal cord in vitro compared with swimming in the intact and spinal animal. , 1984, The Journal of physiology.

[41]  R. Harris-Warrick,et al.  Distribution of serotonergic neurons and processes in the lamprey spinal cord , 1985, Neuroscience.