Alternation of agonists and antagonists during turtle hindlimb motor rhythms

In a variety of vertebrates, including turtle, many classical and contemporary studies of spinal cord neuronal networks generating rhythmic motor behaviors emphasize a Reciprocal Model with alternation of agonists and antagonists, alternation of excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs), and reciprocal inhibition. Some studies of spinal cord neuronal networks, including some in turtle during scratch motor rhythms, describe a Balanced Model with concurrent EPSPs and IPSPs. The present report reviews turtle spinal cord studies and concludes that there is support for a Combined Model with both alternating and concurrent excitation and inhibition, that is, characteristics of both the Reciprocal and the Balanced Models, in the same spinal cord neuronal network for scratch reflex in turtle. Studies of spinal cord neuronal networks for locomotion in a variety of vertebrates also support a Combined Model.

[1]  O. Kiehn.  Locomotor circuits in the mammalian spinal cord. , 2006, Annual review of neuroscience.

[2]  D. McCrea,et al.  Organization of mammalian locomotor rhythm and pattern generation , 2008, Brain Research Reviews.

[3]  A. Berkowitz,et al.  Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: phase analyses , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  P. Stein,et al.  Step, swim, and scratch motor patterns in the turtle. , 2000, Journal of neurophysiology.

[5]  Toshiaki Endo,et al.  Asymmetric operation of the locomotor central pattern generator in the neonatal mouse spinal cord. , 2008, Journal of neurophysiology.

[6]  P. Stein,et al.  Bilateral control of hindlimb scratching in the spinal turtle: contralateral spinal circuitry contributes to the normal ipsilateral motor pattern of fictive rostral scratching , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  G. A. Robertson,et al.  Motor neuron synaptic potentials during fictive scratch reflex in turtle , 1982, Journal of comparative physiology.

[8]  J. Hounsgaard,et al.  Metabotropic Modulation of Motoneurons by Scratch-Like Spinal Network Activity , 2003, The Journal of Neuroscience.

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

[10]  O Kiehn,et al.  Analysis of EPSCs and IPSCs carrying rhythmic, locomotor-related information in the isolated spinal cord of the neonatal rat. , 1997, Journal of neurophysiology.

[11]  P. Stein,et al.  Timing of knee-related spinal neurons during fictive rostral scratching in the turtle. , 2003, Journal of Neurophysiology.

[12]  J. Feldman,et al.  Concurrent Inhibition and Excitation of Phrenic Motoneurons during Inspiration: Phase-Specific Control of Excitability , 1999, The Journal of Neuroscience.

[13]  T. Brown.  The intrinsic factors in the act of progression in the mammal , 1911 .

[14]  P. Stein,et al.  Reconstruction of Flexor/Extensor Alternation during Fictive Rostral Scratching by Two-Site Stimulation in the Spinal Turtle with a Transverse Spinal Hemisection , 1998, The Journal of Neuroscience.

[15]  J. Hounsgaard,et al.  Signaling in large-scale neural networks , 2009, Cognitive Processing.

[16]  Alan Roberts,et al.  Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord , 2004, The Journal of Neuroscience.

[17]  S. Currie,et al.  Glycinergic Inhibition Contributes to the Generation of Rostral Scratch Motor Patterns in the Turtle Spinal Cord , 1997, The Journal of Neuroscience.

[18]  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.

[19]  P. Stein,et al.  In vitro motor program for the rostral scratch reflex generated by the turtle spinal cord , 1983, Brain Research.

[20]  P. Stein,et al.  Spinal cord coordination of hindlimb movements in the turtle: interlimb temporal relationships during bilateral scratching and swimming. , 1997, Journal of neurophysiology.

[21]  S. Currie,et al.  Reciprocal interactions in the turtle hindlimb enlargement contribute to scratch rhythmogenesis. , 1999, Journal of neurophysiology.

[22]  P. Stein,et al.  Three forms of the scratch reflex in the spinal turtle: movement analyses. , 1985, Journal of neurophysiology.

[23]  P. Stein,et al.  Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: broad tuning to regions of the body surface , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Paul S. G. Stein,et al.  Central program for scratch reflex in turtle , 1980, Journal of comparative physiology.

[25]  Paul S. G. Stein,et al.  Motor pattern deletions and modular organization of turtle spinal cord , 2008, Brain Research Reviews.

[26]  Frances S. Chance,et al.  Gain Modulation from Background Synaptic Input , 2002, Neuron.

[27]  D G Stuart,et al.  The segmental motor system--advances, issues, and possibilities. , 1999, Progress in brain research.

[28]  P. Stein,et al.  Modular Organization of Turtle Spinal Interneurons during Normal and Deletion Fictive Rostral Scratching , 2002, The Journal of Neuroscience.

[29]  G. A. Robertson,et al.  Synaptic control of hindlimb motoneurones during three forms of the fictive scratch reflex in the turtle. , 1988, The Journal of physiology.

[30]  Ari Berkowitz,et al.  Physiology and morphology of shared and specialized spinal interneurons for locomotion and scratching. , 2008, Journal of neurophysiology.

[31]  S. Currie,et al.  Right-left interactions between rostral scratch networks generate rhythmicity in the preenlargement spinal cord of the turtle. , 1997, Journal of neurophysiology.

[32]  J. Hounsgaard,et al.  Intense Synaptic Activity Enhances Temporal Resolution in Spinal Motoneurons , 2008, PloS one.

[33]  S. Grillner,et al.  A new class of small inhibitory interneurones in the lamprey spinal cord , 1988, Brain Research.

[34]  P. Stein,et al.  Scratch-swim hybrids in the spinal turtle: blending of rostral scratch and forward swim. , 2000, Journal of neurophysiology.

[35]  Ari Berkowitz,et al.  Spinal Interneurons That Are Selectively Activated during Fictive Flexion Reflex , 2007, The Journal of Neuroscience.

[36]  S. Currie.  Fictive hindlimb motor patterns evoked by AMPA and NMDA in turtle spinal cord-hindlimb nerve preparations , 1999, Journal of Physiology-Paris.

[37]  S. Currie,et al.  Crossed commissural pathways in the spinal hindlimb enlargement are not necessary for right left hindlimb alternation during turtle swimming. , 2007, Journal of neurophysiology.

[38]  Sten Grillner,et al.  Biological Pattern Generation: The Cellular and Computational Logic of Networks in Motion , 2006, Neuron.

[39]  P. Stein.  Neuronal control of turtle hindlimb motor rhythms , 2005, Journal of Comparative Physiology A.

[40]  G. A. Robertson,et al.  Three forms of the scratch reflex in the spinal turtle: central generation of motor patterns. , 1985, Journal of neurophysiology.

[41]  P. Stein,et al.  Cutaneous dermatomes for initiation of three forms of the scratch reflex in the spinal turtle , 1990, The Journal of comparative neurology.

[42]  S. Currie,et al.  Right Left Hindlimb Alternation During Turtle Swimming Crossed Commissural Pathways in the Spinal Hindlimb Enlargement Are Not Necessary , 2000 .

[43]  T. Brown.  On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system , 1914, The Journal of physiology.

[44]  A. Berkowitz.  Physiology and morphology indicate that individual spinal interneurons contribute to diverse limb movements. , 2005, Journal of neurophysiology.

[45]  R. Calabrese,et al.  Serotonergic Modulation of Locomotion in Zebrafish—Endogenous Release and Synaptic Mechanisms , 2009, The Journal of Neuroscience.

[46]  T. Ruigrok,et al.  The organization of motoneurons in the turtle lumbar spinal cord , 1984, The Journal of comparative neurology.

[47]  W. Smith.  The Integrative Action of the Nervous System , 1907, Nature.

[48]  J. Hounsgaard,et al.  Periodic High-Conductance States in Spinal Neurons during Scratch-Like Network Activity in Adult Turtles , 2005, The Journal of Neuroscience.

[49]  S. Currie,et al.  Sensory-evoked pocket scratch motor patterns in the in vitro turtle spinal cord: reduction of excitability by an N-methyl-D-aspartate antagonist. , 1996, Journal of neurophysiology.

[50]  Ole Kiehn,et al.  Activity of Renshaw Cells during Locomotor-Like Rhythmic Activity in the Isolated Spinal Cord of Neonatal Mice , 2006, The Journal of Neuroscience.

[51]  J. Jing,et al.  Distinct Inhibitory Neurons Exert Temporally Specific Control over Activity of a Motoneuron ReceivingConcurrent Excitation and Inhibition , 2009, The Journal of Neuroscience.

[52]  A. Berkowitz,et al.  Somato-dendritic morphology predicts physiology for neurons that contribute to several kinds of limb movements. , 2006, Journal of neurophysiology.

[53]  Frances S. Chance,et al.  Drivers and modulators from push-pull and balanced synaptic input. , 2005, Progress in brain research.

[54]  N Dale,et al.  Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord. , 1985, The Journal of physiology.

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

[56]  M. A. Masino,et al.  Engrailed-1 Expression Marks a Primitive Class of Inhibitory Spinal Interneuron , 2004, The Journal of Neuroscience.

[57]  A. Crowe,et al.  Multicyclic scratch reflex movements in the terrapinpseudemys scripta elegans , 1982, Journal of comparative physiology.

[58]  Toshiaki Endo,et al.  Excitatory components of the mammalian locomotor CPG , 2008, Brain Research Reviews.

[59]  P. Stein,et al.  Spinal cord coordination of hindlimb movements in the turtle: intralimb temporal relationships during scratching and swimming. , 1997, Journal of neurophysiology.

[60]  Rune W. Berg,et al.  Balanced Inhibition and Excitation Drive Spike Activity in Spinal Half-Centers , 2007, Science.

[61]  E. Marder,et al.  Principles of rhythmic motor pattern generation. , 1996, Physiological reviews.

[62]  P. Stein,et al.  Interruptions of fictive scratch motor rhythms by activation of cutaneous flexion reflex afferents in the turtle , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  Y. Frégnac,et al.  Visual input evokes transient and strong shunting inhibition in visual cortical neurons , 1998, Nature.

[64]  Adilson E. Motter,et al.  Networks in Motion , 2012, ArXiv.

[65]  S. Currie,et al.  Electrically evoked locomotor activity in the turtle spinal cord hemi-enlargement preparation , 2008, Neuroscience Letters.

[66]  J. A. Kahn.  Patterns of synaptic inhibition in motoneurons and interneurons during fictive swimming in the lamprey, as revealed by Cl− injections , 1982, Journal of comparative physiology.

[67]  P. Stein,et al.  Variations in motor patterns during fictive rostral scratching in the turtle: knee-related deletions. , 2004, Journal of neurophysiology.