The segmental motor system--advances, issues, and possibilities.

Publisher Summary This chapter discusses the segmental motor system. This term is useful in both invertebrate and vertebrate motor control neuroscience with respect to the work on (1) the properties and central actions of posture and movement-related sensory feedback from the body's somatic structures, (2) interneuron (IN) and motoneuron (MN) discharge properties, MN recruitment properties, and the associations among MN, muscle fiber (MF), and motor unit (MU) properties for the graded development of muscle force, and (3) segmental pattern generation for the elaboration of intrinsic/rhythmic and learned skillful movements. Each of these areas is being addressed currently from the molecular/cellular to the behavioral level of analysis in a wide variety of invertebrate and vertebrate species. Each has a particular attraction for life and physical scientists, including roboticists, and each, in time, can provide a seamless integration between fundamental and applied clinical science. This chapter discusses selected issues that are relevant to the operation of an interdisciplinary training program in movement neuroscience. One primary goal of such programs should be to emphasize a broad perspective and interest in movement neuroscience, from the molecular/cellular to the behavioral level of analysis. Another guiding principle, which is often underemphasized at international conferences, is to truly mentor trainees, network them with senior scientists, and extol their work.

[1]  P. Sah,et al.  USE OF MURINE MUTANTS TO STUDY GLYCINE RECEPTOR FUNCTION , 1999, Clinical and Experimental Pharmacology and Physiology.

[2]  Jaynie F. Yang,et al.  Self-sustained firing of human motor units , 1998, Neuroscience Letters.

[3]  A. Lindsay,et al.  Distribution of effective synaptic currents underlying recurrent inhibition in cat triceps surae motoneurons. , 1991, Journal of neurophysiology.

[4]  E. Jankowska.  Interneuronal relay in spinal pathways from proprioceptors , 1992, Progress in Neurobiology.

[5]  R. Katz,et al.  Recurrent inhibition in humans , 1999, Progress in Neurobiology.

[6]  D. Kernell,et al.  Quantitative aspects of repetitive firing of mammalian motoneurones, caused by injected currents , 1963, The Journal of physiology.

[7]  D. Denny-Brown,et al.  Interpretation of the electromyogram. , 1949, Archives of neurology and psychiatry.

[8]  D. Denny-Brown,et al.  FIBRILLATION AND FASCICULATION IN VOLUNTARY MUSCLE , 1938 .

[9]  P. Schwindt,et al.  Calcium currents in acutely isolated human neocortical neurons. , 1993, Journal of neurophysiology.

[10]  S. Grillner,et al.  Vertebrate Locomotion‐A Lamprey Perspective a , 1998, Annals of the New York Academy of Sciences.

[11]  Ole Kiehn,et al.  Neuromodulation of vertebrate motor neuron membrane properties , 1992, Current Opinion in Neurobiology.

[12]  Olive C. Smith,et al.  ACTION POTENTIALS FROM SINGLE MOTOR UNITS IN VOLUNTARY CONTRACTION , 1934 .

[13]  O Kiehn,et al.  Bistable firing properties of soleus motor units in unrestrained rats. , 1989, Acta physiologica Scandinavica.

[14]  B J Schmidt,et al.  NMDA Receptor Activation Triggers Voltage Oscillations, Plateau Potentials and Burstinq in Neonatal Rat Lumbar Motoneurons ln Vitro , 1997, The European journal of neuroscience.

[15]  J. Buchanan,et al.  Electrophysiological properties of identified classes of lamprey spinal neurons. , 1993, Journal of neurophysiology.

[16]  L. Jordan,et al.  TTX-resistant NMDA receptor-mediated voltage oscillations in mammalian lumbar motoneurons. , 1994, Journal of neurophysiology.

[17]  J. Hounsgaard,et al.  Ca2+‐Mediated Plateau Potentials in a Subpopulation of Interneurons in the Ventral Horn of the Turtle Spinal Cord , 1992, The European journal of neuroscience.

[18]  P. Gillespie.  Feeling force: mechanical transduction by vertebrates and invertebrates. , 1996, Chemistry & biology.

[19]  B. Walmsley,et al.  Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats. , 1978, Journal of neurophysiology.

[20]  P. Jonas,et al.  Corelease of two fast neurotransmitters at a central synapse. , 1998, Science.

[21]  R S Johansson,et al.  Control of fingertip forces in multidigit manipulation. , 1999, Journal of neurophysiology.

[22]  P. A. Getting.  Understanding Central Pattern Generators: Insights Gained from the Study of Invertebrate Systems , 1986 .

[23]  R. G. Williamson,et al.  Motor units and fiber types of primary ankle extensors of the skunk (Mephitis mephitis). , 1977, Journal of neurophysiology.

[24]  D. Burke,et al.  Does the nervous system depend on kinesthetic information to control natural limb movements , 1992 .

[25]  R. Creed,et al.  Reflex Activity of the Spinal Cord , 1933 .

[26]  R K Powers,et al.  Effective synaptic current can be estimated from measurements of neuronal discharge. , 1992, Journal of neurophysiology.

[27]  C. Heckman,et al.  Can Ib axons be selectively activated by electrical stimuli in human subjects? , 1984, Experimental Neurology.

[28]  Perspectives of motor behavior and its neural basis , 1997 .

[29]  G. Watson,et al.  A comparison of hair bundle mechanoreceptors in sea anemones and vertebrate systems. , 1999, Current topics in developmental biology.

[30]  A. Taylor,et al.  Alpha and Gamma Motor Systems , 1995, Springer US.

[31]  R. Harris-Warrick.  In: Dynamic Biological Networks: The Stomatogastric Nervous System , 1992 .

[32]  C. Heckman,et al.  Tendon vibration-induced inhibition of human and cat triceps surae group I reflexes: Evidence of selective Ib afferent fiber activation , 1986, Experimental Neurology.

[33]  S. Grillner.  Locomotion in vertebrates: central mechanisms and reflex interaction. , 1975, Physiological reviews.

[34]  R. Harris-Warrick,et al.  Serotonergic stretch receptors induce plateau properties in a crustacean motor neuron by a dual-conductance mechanism. , 1992, Journal of neurophysiology.

[35]  H. Wigström,et al.  Prolonged activation of soleus motoneurones following a conditioning train in soleus Ia afferents — A case for a reverberating loop? , 1975, Neuroscience Letters.

[36]  Properties and segmental actions of mammalian muscle receptors: an update. , 1982, Federation proceedings.

[37]  S. Garland,et al.  Role of muscle afferents in the inhibition of motoneurons during fatigue. , 1995, Advances in experimental medicine and biology.

[38]  E K Stauffer,et al.  Analysis of muscle receptor connections by spike-triggered averaging. 1. Spindle primary and tendon organ afferents. , 1976, Journal of neurophysiology.

[39]  O Kiehn,et al.  Response properties of motoneurones in a slice preparation of the turtle spinal cord. , 1988, The Journal of physiology.

[40]  Randall K. Powers,et al.  How different afferent inputs control motoneuron discharge and the output of the motoneuron pool , 1993, Current Opinion in Neurobiology.

[41]  K. Lucas.  On the gradation of activity in a skeletal muscle‐fibre , 1905, The Journal of physiology.

[42]  Lawrence C. Rome,et al.  Why animals have different muscle fibre types , 1988, Nature.

[43]  O Kiehn,et al.  Plateau properties in mammalian spinal interneurons during transmitter-induced locomotor activity , 1996, Neuroscience.

[44]  D G Stuart,et al.  Animal solutions to problems of movement control: the role of proprioceptors. , 1988, Annual review of neuroscience.

[45]  S. Mori,et al.  Lumbar Interneurons Involved in the Generation of Fictive Locomotion in Cats a , 1998, Annals of the New York Academy of Sciences.

[46]  A. Prochazka,et al.  Muscle Receptors and Movement , 1981, Palgrave Macmillan UK.

[47]  S. Mense,et al.  Nociception from skeletal muscle in relation to clinical muscle pain , 1993, Pain.

[48]  Pankaj Sah,et al.  Ca2+-activated K+ currents in neurones: types, physiological roles and modulation , 1996, Trends in Neurosciences.

[49]  S. Grillner,et al.  N-methyl-D-aspartate receptor-induced, inherent oscillatory activity in neurons active during fictive locomotion in the lamprey , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  P A Getting,et al.  Emerging principles governing the operation of neural networks. , 1989, Annual review of neuroscience.

[51]  Paul S. G. Stein,et al.  Motor control : from movement trajectories to neural mechanisms , 1985 .

[52]  C. Heckman,et al.  The Physiological Control of Motoneuron Activity , 1996 .

[53]  E Henneman,et al.  Terminals of Single Ia Fibers: Distribution within a Pool of 300 Homonymous Motor Neurons , 1968, Science.

[54]  A. Momiyama,et al.  Functional correlation of fetal and adult forms of glycine receptors with developmental changes in inhibitory synaptic receptor channels , 1992, Neuron.

[55]  K Matsuyama,et al.  Stimulation of a restricted region in the midline cerebellar white matter evokes coordinated quadrupedal locomotion in the decerebrate cat. , 1999, Journal of neurophysiology.

[56]  L. Jordan,et al.  Control of functional systems in the brainstem and spinal cord , 1992, Current Opinion in Neurobiology.

[57]  C. Sherrington,et al.  Reflexes in Response to Stretch (Myotatic Reflexes) , 1924 .

[58]  M. Moulins,et al.  Modulation and dynamic specification of motor rhythm-generating circuits in crustacea , 1995, Journal of Physiology-Paris.

[59]  Douglas G. Stuart,et al.  Neural Control of Locomotion , 1976, Advances in Behavioral Biology.

[60]  Schmitz Rj.  Clinical Applications in Surface Electromyography: Chronic Musculoskeletal Pain. , 1999 .

[61]  F. Edwards,et al.  ATP receptor-mediated synaptic currents in the central nervous system , 1992, Nature.

[62]  R. Burke.  Motor Units: Anatomy, Physiology, and Functional Organization , 1981 .

[63]  O Kiehn,et al.  Serotonin‐induced bistability of turtle motoneurones caused by a nifedipine‐sensitive calcium plateau potential. , 1989, The Journal of physiology.

[64]  R M Reinking,et al.  A commentary on muscle unit properties in cat hindlimb muscles , 1980, Journal of morphology.

[65]  C. Heckman,et al.  Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. , 1998, Journal of neurophysiology.

[66]  D. McCrea.  Can sense be made of spinal interneuron circuits , 1992 .

[67]  M. Binder,et al.  Multiple mechanisms of spike-frequency adaptation in motoneurones , 1999, Journal of Physiology-Paris.

[68]  L. Rome,et al.  The whistle and the rattle: the design of sound producing muscles. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[69]  S. Blackshaw.  Stretch receptors and body wall muscle in leeches. , 1993, Comparative biochemistry and physiology. Comparative physiology.

[70]  W. Rall.  Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. , 1967, Journal of neurophysiology.

[71]  R. A. Davidoff.  Handbook of the spinal cord , 1983 .

[72]  H Hultborn,et al.  Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. , 1998, Journal of neurophysiology.

[73]  Renaming the "Henneman Size Principle" , 1998, Science.

[74]  U Proske,et al.  The role of muscle receptors in the detection of movements , 2000, Progress in Neurobiology.

[75]  P. Schwindt,et al.  Role of a persistent inward current in motoneuron bursting during spinal seizures. , 1980, Journal of neurophysiology.

[76]  E. Henneman.  Relation between size of neurons and their susceptibility to discharge. , 1957, Science.

[77]  Alan J. McComas.  Neuromuscular Function and Disorders , 1979 .

[78]  T. Sears,et al.  Monosynaptic excitation of motoneurones from secondary endings of muscle spindles , 1974, Nature.

[79]  A. Lundberg,et al.  Interneurones in the spinal cord , 1981, Trends in Neurosciences.

[80]  John C. Eccles (1903-1997) , 1997, Trends in neurosciences.

[81]  J. Buchanan.  Lamprey spinal interneurons and their roles in swimming activity. , 1996, Brain, behavior and evolution.

[82]  M. Gorassini,et al.  Activation patterns of hindlimb motor units in the awake rat and their relation to motoneuron intrinsic properties. , 1999, Journal of neurophysiology.

[83]  M. Fitzgerald.  Symposium on Muscle Receptors , 1963, Neurology.

[84]  J. Massion.  Movement, posture and equilibrium: Interaction and coordination , 1992, Progress in Neurobiology.

[85]  D. Lindsley,et al.  ELECTRICAL ACTIVITY OF HUMAN MOTOR UNITS DURING VOLUNTARY CONTRACTION , 1935 .

[86]  Ole Kiehn,et al.  Neuronal mechanisms for generating locomotor activity , 1998 .

[87]  J. Feldman,et al.  PreBötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. , 1998, Annual review of physiology.

[88]  W. Rathmayer,et al.  Muscle fiber types in crabs: studies on single identified muscle fibers , 1987 .

[89]  C. Sherrington,et al.  Recruitment Type of Reflexes , 1923 .

[90]  P. Schwindt,et al.  Mechanisms underlying burst and regular spiking evoked by dendritic depolarization in layer 5 cortical pyramidal neurons. , 1999, Journal of neurophysiology.

[91]  D. F. Russell,et al.  Bursting neural networks: a reexamination. , 1978, Science.

[92]  K. Pearson.  Common principles of motor control in vertebrates and invertebrates. , 1993, Annual review of neuroscience.

[93]  P. H. Silver.  Two spectral sensitivity curves of Xenopus laevis obtained by using the melanophore response to light on white and black backgrounds , 1963, Journal of Physiology.

[94]  Douglas G. Stuart,et al.  Henneman's ‘size principle’: current issues , 1984, Trends in Neurosciences.

[95]  D. McCrea.  Neuronal Basis of Afferent‐evoked Enhancement of Locomotor Activitya , 1998, Annals of the New York Academy of Sciences.

[96]  D. Stuart.  Muscle Receptors, Mammalian , 1988 .

[97]  T. Eken.  Spontaneous electromyographic activity in adult rat soleus muscle. , 1998, Journal of neurophysiology.

[98]  B. Schmidt,et al.  Whole cell recordings of lumbar motoneurons during locomotor-like activity in the in vitro neonatal rat spinal cord. , 1998, Journal of neurophysiology.

[99]  G. R. Mines.  On the summation of contractions , 1913, The Journal of physiology.

[100]  H Hultborn.  Plateau potentials and their role in regulating motoneuronal firing. , 1999, Progress in brain research.

[101]  S. Mori,et al.  Morphology of single pontine reticulospinal axons in the lumbar enlargement of the cat: A study using the anterograde tracer PHA‐L , 1999, The Journal of comparative neurology.

[102]  W Rall,et al.  Matching dendritic neuron models to experimental data. , 1992, Physiological reviews.

[103]  R. Reinking,et al.  Uniformity of metabolic enzymes within individual motor units , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[104]  W. C. Groat,et al.  Unitary excitatory synaptic currents in preganglionic neurons mediated by two distinct groups of interneurons in neonatal rat sacral parasympathetic nucleus. , 1996, Journal of neurophysiology.

[105]  C. Heckman,et al.  Bistability in spinal motoneurons in vivo: systematic variations in rhythmic firing patterns. , 1998, Journal of neurophysiology.

[106]  R. Reinking,et al.  Analysis of muscle receptor connections by spike-triggered averaging. 2. Spindle group II afferents. , 1976, Journal of neurophysiology.

[107]  V. Gurfinkel,et al.  Locomotor‐like movements evoked by leg muscle vibration in humans , 1998, The European journal of neuroscience.

[108]  Paul S. G. Stein.  Neurons, networks, and motor behavior , 1999 .

[109]  C. L. Cleland,et al.  Neural mechanisms underlying the clasp-knife reflex in the cat. I. Characteristics of the reflex. , 1990, Journal of neurophysiology.

[110]  M. Gorassini,et al.  Models of ensemble firing of muscle spindle afferents recorded during normal locomotion in cats , 1998, The Journal of physiology.

[111]  J. MacLean,et al.  NMDA receptor-mediated oscillatory activity in the neonatal rat spinal cord is serotonin dependent. , 1998, Journal of neurophysiology.

[112]  M D Binder,et al.  Computer simulation of the steady-state input-output function of the cat medial gastrocnemius motoneuron pool. , 1991, Journal of neurophysiology.

[113]  C. Sherrington.  Ferrier lecture.—Some functional problems attaching to convergence , 1929 .

[114]  S. Grillner,et al.  Selection and initiation of motor behavior , 1997 .

[115]  T. Nichols.  A biomechanical perspective on spinal mechanisms of coordinated muscular action: an architecture principle. , 1994, Acta anatomica.

[116]  N. A. Bernshteĭn,et al.  Human motor actions : Bernstein reassessed , 1984 .

[117]  P. Stein,et al.  Spinal Motor Patterns in the Turtle a , 1998, Annals of the New York Academy of Sciences.

[118]  K Matsuyama,et al.  Segment‐specific branching patterns of single vestibulospinal tract axons arising from the lateral vestibular nucleus in the cat: A PHA‐L tracing study , 1999, The Journal of comparative neurology.

[119]  L. Vyklický,et al.  Properties of NMDA receptors in rat spinal cord motoneurons , 1999, The European journal of neuroscience.

[120]  H Hultborn,et al.  Input‐output relations in the pathway of recurrent inhibition to motoneurones in the cat. , 1979, The Journal of physiology.

[121]  Judith P. Swazey,et al.  The Neurosciences: Paths of Discovery, I , 1992, Birkhäuser Boston.

[122]  M D Binder,et al.  Analysis of effective synaptic currents generated by homonymous Ia afferent fibers in motoneurons of the cat. , 1988, Journal of neurophysiology.

[123]  N. A. Bernstein.  Dexterity and Its Development , 1996 .

[124]  P. S. Dickinson,et al.  Interactions among neural networks for behavior , 1995, Current Opinion in Neurobiology.

[125]  Thomas A. Keil,et al.  Functional morphology of insect mechanoreceptors , 1997, Microscopy research and technique.

[126]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[127]  Andrew J. Fuglevand,et al.  Contractile Properties of Human Motor Units: Is Man a Gat? , 1998 .

[128]  J. Munson,et al.  Membrane electrical properties and prediction of motor-unit type of medial gastrocnemius motoneurons in the cat. , 1985, Journal of neurophysiology.

[129]  Marc D. Binder,et al.  The Segmental motor system , 1990 .

[130]  P. D. Cheney,et al.  Corticomotoneuronal connections of precentral cells detected by post-spike averages of EMG activity in behaving monkeys , 1976, Brain Research.

[131]  R B Stein,et al.  New methods for analysing motor function in man and animals. , 1972, Brain research.

[132]  R. Brownstone,et al.  Development of L‐type calcium channels and a nifedipine‐sensitive motor activity in the postnatal mouse spinal cord , 1999, The European journal of neuroscience.

[133]  R. B. Wuerker,et al.  Membrane impedance changes during synaptic transmission in cat spinal motoneurons. , 1967, Journal of neurophysiology.

[134]  R. Calabrese.  Cellular, synaptic, network, and modulatory mechanisms involved in rhythm generation , 1998, Current Opinion in Neurobiology.

[135]  H Hultborn,et al.  Short-term plasticity in hindlimb motoneurons of decerebrate cats. , 1998, Journal of neurophysiology.

[136]  O. Kiehn,et al.  Prolonged firing in motor units: evidence of plateau potentials in human motoneurons? , 1997, Journal of neurophysiology.

[137]  J. Fleshman,et al.  Rheobase, input resistance, and motor-unit type in medial gastrocnemius motoneurons in the cat. , 1981, Journal of neurophysiology.

[138]  L. Mendell,et al.  Properties of somata of spinal dorsal root ganglion cells differ according to peripheral receptor innervated. , 1988, Journal of neurophysiology.

[139]  D. Jenkinson,et al.  COMPARATIVE PHYSIOLOGY OF SWEATING , 1973, The British journal of dermatology.

[140]  R. Reinking,et al.  Properties of spinal motoneurons and interneurons in the adult turtle: Provisional classification by cluster analysis , 1998, The Journal of comparative neurology.

[141]  P. Stein,et al.  Neurobiology of Vertebrate Locomotion , 1986, Wenner-Gren Center International Symposium Series.

[142]  R. Schmidt.  The articular polymodal nociceptor in health and disease. , 1996, Progress in brain research.

[143]  D. Kernell,et al.  Input conductance, axonal conduction velocity and cell size among hindlimb motoneurones of the cat , 1981, Brain Research.

[144]  W Rall,et al.  Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. , 1967, Journal of neurophysiology.

[145]  D. Stuart,et al.  Functional anatomy of the association between motor units and muscle receptors , 1978 .

[146]  A. Selverston,et al.  Basic Principles for Generating Motor Output in the Stomatogastric Ganglion , 1998, Annals of the New York Academy of Sciences.

[147]  D. Kernell.  The Limits of Firing Frequency in Cat Lumbosacral Motoneurones Possessing Different Time Course of Afterhyperpolarization , 1965 .

[148]  J. Wessberg,et al.  Is human muscle spindle afference dependent on perceived size of error in visual tracking? , 1997, Experimental Brain Research.

[149]  O. Kiehn,et al.  Bistability of alpha‐motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5‐hydroxytryptophan. , 1988, The Journal of physiology.

[150]  J Palka,et al.  The evolution of insect wings and their sensory apparatus. , 1997, Brain, behavior and evolution.

[151]  R M Enoka,et al.  The Interface Between Biomechanics and Neurophysiology In the Study of Movement: Some Recent Approaches , 1985, Exercise and sport sciences reviews.

[152]  P. G. Nelson,et al.  Anomalous rectification in cat spinal motoneurons and effect of polarizing currents on excitatory postsynaptic potential. , 1967, Journal of neurophysiology.

[153]  E. Liddell.  Charles Scott Sherrington 1857-1952 , 1952, Obituary Notices of Fellows of the Royal Society.

[154]  Alan J. McComas,et al.  Skeletal Muscle: Form and Function , 1996 .

[155]  D. Kernell,et al.  Algebraical summation in synaptic activation of motoneurones firing within the ‘primary range’ to injected currents , 1966, The Journal of physiology.

[156]  J. Fetcho.  The spinal motor system in early vertebrates and some of its evolutionary changes. , 1992, Brain, behavior and evolution.

[157]  P. Matthews,et al.  Mammalian muscle receptors and their central actions , 1974 .

[158]  S. Gilman,et al.  Derek E Denny-Brown (1901–1981): His Life and Influence on American Neurology , 1998, Journal of medical biography.

[159]  D. Stuart,et al.  A commentary on the segmental motor system of the turtle: Implications for the study of its cellular mechanisms and interactions , 1995, Journal of morphology.

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

[161]  H. Wigström,et al.  Maintained changes in motoneuronal excitability by short‐lasting synaptic inputs in the decerebrate cat. , 1988, The Journal of physiology.

[162]  R E Burke,et al.  Composite nature of the monosynaptic excitatory postsynaptic potential. , 1967, Journal of neurophysiology.

[163]  U. Windhorst,et al.  Overview: potential role of segmental motor circuitry in muscle fatigue. , 1995, Advances in experimental medicine and biology.

[164]  D. Westbury.  Electrophysiological characteristics of spinal gamma motoneurons in the cat , 1981 .