Localization and connectivity in spinal interneuronal networks: the adduction-caudal extension-flexion rhythm in the frog.

We have previously reported that focal intraspinal N-methyl-d-aspartate (NMDA) iontophoresis in the frog elicits a motor output, which is organized in terms of its constituent isometric force directions at the ipsilateral ankle and its topography. Furthermore, the associated EMG patterns can be reconstructed as the linear combinations of seven muscle synergies, labeled A to G. We now focus on one of the most common NMDA-elicited outputs, the adduction-caudal extension-flexion rhythm, and examine the relationship between the different force phases in terms of synergies and topography. Two distinct EMG patterns produce caudal extensions, and only one of the two patterns is used at most sites. The key synergy combinations for the two patterns are B + e and D + c (strongest synergies capitalized). These two patterns map at distinct locations in the lumbar cord. Within individual sites rhythms, we find linkages among the synergies used to produce adductions, the onsets of flexions after caudal extensions, and the synergy pattern producing the caudal extensions. For example, the synergy composition of adductions at B + e caudal extension sites is dominated by E + b and at D + c caudal extension sites by C + d. The two types of adductions map at distinct locations, situated between the two caudal extension regions. Specifically the linked patterns of caudal extension-adduction interleave rostrocaudally in a CE2-ADD1-ADD2-CE1 sequence, where 1 and 2 refer to the two pattern types. The implications of this topography and connectivity with respect to motor systems organization and behaviors are discussed.

[1]  E. H. Dunn The number and size of the nerve fibers innervating the skin and muscles of the thigh in the frog (Rana virescens brachycephala, cope) , 1900 .

[2]  John W. Tukey,et al.  Exploratory Data Analysis. , 1979 .

[3]  J. A. Hartigan,et al.  A k-means clustering algorithm , 1979 .

[4]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  G E Loeb,et al.  Activity of spindle afferents from cat anterior thigh muscles. I. Identification and patterns during normal locomotion. , 1985, Journal of neurophysiology.

[6]  E. Fetz,et al.  Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimuli in primates: evidence for functional groups of CM cells. , 1985, Journal of neurophysiology.

[7]  E. G. Jones,et al.  Relationship of intrinsic connections to forelimb movement representations in monkey motor cortex: a correlative anatomic and physiological study. , 1991, Journal of neurophysiology.

[8]  A Keller,et al.  The patterns and synaptic properties of horizontal intracortical connections in the rat motor cortex. , 1993, Journal of neurophysiology.

[9]  A Keller,et al.  Intrinsic connections between representation zones in the cat motor cortex. , 1993, Neuroreport.

[10]  H. Chiel,et al.  Neural architectures for adaptive behavior , 1994, Trends in Neurosciences.

[11]  O Kiehn,et al.  Distribution of Networks Generating and Coordinating Locomotor Activity in the Neonatal Rat Spinal Cord In Vitro: A Lesion Study , 1996, The Journal of Neuroscience.

[12]  J. Gossard,et al.  Supraspinal and segmental signals can be transmitted through separate spinal cord pathways to enhance locomotor activity in extensor muscles in the cat , 1997, Experimental Brain Research.

[13]  Deliagina Vestibular compensation in lampreys: impairment and recovery of equilibrium control during locomotion , 1997, The Journal of experimental biology.

[14]  R. Stein,et al.  Identification, Localization, and Modulation of Neural Networks for Walking in the Mudpuppy (Necturus Maculatus) Spinal Cord , 1998, The Journal of Neuroscience.

[15]  C. Capaday,et al.  Intracortical connections between motor cortical zones controlling antagonistic muscles in the cat: a combined anatomical and physiological study , 1998, Experimental Brain Research.

[16]  E. Bizzi,et al.  Spinal cord modular organization and rhythm generation: an NMDA iontophoretic study in the frog. , 1998, Journal of neurophysiology.

[17]  E. Bizzi,et al.  The construction of movement by the spinal cord , 1999, Nature Neuroscience.

[18]  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.

[19]  J. Gossard,et al.  Bulbospinal control of spinal cord pathways generating locomotor extensor activities in the cat , 2000, The Journal of physiology.

[20]  S. Rossignol,et al.  Initiating or Blocking Locomotion in Spinal Cats by Applying Noradrenergic Drugs to Restricted Lumbar Spinal Segments , 2000, The Journal of Neuroscience.

[21]  P. Cheney,et al.  Correlations between corticomotoneuronal (CM) cell postspike effects and cell-target muscle covariation. , 2000, Journal of neurophysiology.

[22]  S. Giszter,et al.  Output Units of Motor Behavior: An Experimental and Modeling Study , 2000, Journal of Cognitive Neuroscience.

[23]  A. Berkowitz Rhythmicity of spinal neurons activated during each form of fictive scratching in spinal turtles. , 2001, Journal of neurophysiology.

[24]  E. Bizzi,et al.  Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. , 2001, Journal of neurophysiology.

[25]  A. Berkowitz,et al.  Broadly tuned spinal neurons for each form of fictive scratching in spinal turtles. , 2001, Journal of neurophysiology.

[26]  P. Cheney,et al.  Consistent Features in the Forelimb Representation of Primary Motor Cortex in Rhesus Macaques , 2001, The Journal of Neuroscience.

[27]  M. Schieber Constraints on somatotopic organization in the primary motor cortex. , 2001, Journal of neurophysiology.

[28]  T G Deliagina,et al.  Modifications of vestibular responses of individual reticulospinal neurons in lamprey caused by unilateral labyrinthectomy. , 2002, Journal of neurophysiology.

[29]  M. Garwicz Spinal reflexes provide motor error signals to cerebellar modules—relevance for motor coordination , 2002, Brain Research Reviews.

[30]  Hans Holmberg,et al.  Spinal Sensorimotor Transformation: Relation between Cutaneous Somatotopy and a Reflex Network , 2002, The Journal of Neuroscience.

[31]  Martin Garwicz,et al.  Common principles of sensory encoding in spinal reflex modules and cerebellar climbing fibres , 2002, The Journal of physiology.

[32]  J. Cazalets,et al.  The respective contribution of lumbar segments to the generation of locomotion in the isolated spinal cord of newborn rat , 2002, The European journal of neuroscience.

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

[34]  Jens Schouenborg,et al.  Modular organisation and spinal somatosensory imprinting , 2002, Brain Research Reviews.

[35]  C. Matesz,et al.  Ascending and descending projections of the lateral vestibular nucleus in the frog Rana esculenta , 2002, The Journal of comparative neurology.

[36]  Emilio Bizzi,et al.  Coordination and localization in spinal motor systems , 2002, Brain Research Reviews.

[37]  R. Stein,et al.  Differential distribution of interneurons in the neural networks that control walking in the mudpuppy (Necturus maculatus) spinal cord , 2002, Experimental Brain Research.

[38]  H. Straka,et al.  Differential spatial organization of otolith signals in frog vestibular nuclei. , 2003, Journal of neurophysiology.

[39]  A. Georgopoulos,et al.  Modular organization of directionally tuned cells in the motor cortex: Is there a short-range order? , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  O. Kiehn,et al.  Functional Identification of Interneurons Responsible for Left-Right Coordination of Hindlimbs in Mammals , 2003, Neuron.

[41]  E. Jankowska,et al.  Are Crossed Actions of Reticulospinal and Vestibulospinal Neurons on Feline Motoneurons Mediated by the Same or Separate Commissural Neurons? , 2003, The Journal of Neuroscience.

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

[43]  J. Schouenborg,et al.  Functional organization of the nociceptive withdrawal reflexes , 2004, Experimental Brain Research.

[44]  H. Hultborn,et al.  Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat , 2004, Experimental Brain Research.

[45]  P. Cheney,et al.  Properties of primary motor cortex output to forelimb muscles in rhesus macaques. , 2004, Journal of neurophysiology.

[46]  J. Schouenborg,et al.  A survey of spinal dorsal horn neurones encoding the spatial organization of withdrawal reflexes in the rat , 2004, Experimental Brain Research.

[47]  Serge Rossignol,et al.  Critical points in the forelimb fictive locomotor cycle and motor coordination: evidence from the effects of tonic proprioceptive perturbations in the cat. , 2004, Journal of neurophysiology.

[48]  A. M. Degtyarenko,et al.  Disynaptic vestibulospinal and reticulospinal excitation in cat lumbosacral motoneurons: modulation during fictive locomotion , 1996, Experimental Brain Research.

[49]  E. Bizzi,et al.  Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors , 2005, The Journal of Neuroscience.

[50]  M. Garwicz,et al.  Anatomical and physiological foundations of cerebellar information processing , 2005, Nature Reviews Neuroscience.