Modular Organization of Finger Movements by the Human Central Nervous System

The motor system may generate automated movements, such as walking, by combining modular spinal motor synergies. However, it remains unknown whether a modular neuronal architecture is sufficient to generate the unique flexibility of human finger movements, which rely on cortical structures. Here we show that finger movements evoked by transcranial magnetic stimulation (TMS) of the primary motor cortex reproduced distinctive features of the spatial representation of voluntary movements as identified in previous neuroimaging studies, consistent with naturalistic activation of neuronal elements. Principal component analysis revealed that the dimensionality of TMS-evoked movements was low. Principal components extracted from TMS-induced finger movements resembled those derived from end-postures of voluntary movements performed to grasp imagined objects, and a small subset of them was sufficient to reconstruct these movements with remarkable fidelity. The motor system may coordinate even the most dexterous movements by using a modular architecture involving cortical components.

[1]  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.

[2]  Peter L. Strick,et al.  Stimulating research on motor cortex , 2002, Nature Neuroscience.

[3]  M. Schieber,et al.  Limited functional grouping of neurons in the motor cortex hand area during individuated finger movements: A cluster analysis. , 1999, Journal of neurophysiology.

[4]  A. Kleinschmidt,et al.  Somatotopy in the Human Motor Cortex Hand Area. A High‐Resolution Functional MRI Study , 1997, The European journal of neuroscience.

[5]  F A Mussa-Ivaldi,et al.  Computations underlying the execution of movement: a biological perspective. , 1991, Science.

[6]  A T Barker,et al.  The history and basic principles of magnetic nerve stimulation. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[7]  J. Murphy,et al.  Spatial organization of precentral cortex in awake primates. III. Input-output coupling. , 1978, Journal of neurophysiology.

[8]  J. Foley.  The co-ordination and regulation of movements , 1968 .

[9]  Steve I Perlmutter,et al.  Functional properties of primate spinal interneurones during voluntary hand movements. , 2002, Advances in experimental medicine and biology.

[10]  R B Stein,et al.  Movements generated by intraspinal microstimulation in the intermediate gray matter of the anesthetized, decerebrate, and spinal cat. , 2004, Canadian journal of physiology and pharmacology.

[11]  Rupert Lanzenberger,et al.  Finger Somatotopy in Human Motor Cortex , 2001, NeuroImage.

[12]  G. Deuschl,et al.  The pathophysiology of tremor , 2001, Muscle & nerve.

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

[14]  T. Aflalo,et al.  Partial tuning of motor cortex neurons to final posture in a free-moving paradigm. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Francesco Lacquaniti,et al.  Control of Fast-Reaching Movements by Muscle Synergy Combinations , 2006, The Journal of Neuroscience.

[16]  J. Rothwell,et al.  Techniques and mechanisms of action of transcranial stimulation of the human motor cortex , 1997, Journal of Neuroscience Methods.

[17]  Marco Santello,et al.  Patterns of Hand Motion during Grasping and the Influence of Sensory Guidance , 2002, The Journal of Neuroscience.

[18]  Dylan F. Cooke,et al.  Arm movements evoked by electrical stimulation in the motor cortex of monkeys. , 2005, Journal of neurophysiology.

[19]  T Brochier,et al.  Patterns of muscle activity underlying object-specific grasp by the macaque monkey. , 2004, Journal of neurophysiology.

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

[21]  S. Small,et al.  Somatotopy in human primary motor and somatosensory hand representations revisited. , 2001, Cerebral cortex.

[22]  E. Bizzi,et al.  Low dimensionality of supraspinally induced force fields. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  E. Bizzi,et al.  Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activated by low threshold cutaneous stimulation , 1999, Experimental Brain Research.

[24]  Dylan F. Cooke,et al.  The Cortical Control of Movement Revisited , 2002, Neuron.

[25]  M. Graziano,et al.  Mapping from motor cortex to biceps and triceps altered by elbow angle. , 2004, Journal of neurophysiology.

[26]  Emilio Bizzi,et al.  Combinations of muscle synergies in the construction of a natural motor behavior , 2003, Nature Neuroscience.

[27]  D. G. Lawrence,et al.  The functional organization of the motor system in the monkey. II. The effects of lesions of the descending brain-stem pathways. , 1968, Brain : a journal of neurology.

[28]  Tamar Flash,et al.  Motor primitives in vertebrates and invertebrates , 2005, Current Opinion in Neurobiology.

[29]  M. Hallett,et al.  Rapid plasticity of human cortical movement representation induced by practice. , 1998, Journal of neurophysiology.

[30]  J. Rothwell,et al.  The physiological basis of transcranial motor cortex stimulation in conscious humans , 2004, Clinical Neurophysiology.

[31]  Christian Ethier,et al.  Linear Summation of Cat Motor Cortex Outputs , 2006, The Journal of Neuroscience.

[32]  M. Graziano,et al.  Complex Movements Evoked by Microstimulation of Precentral Cortex , 2002, Neuron.

[33]  Miguel A. L. Nicolelis,et al.  Brain–machine interfaces to restore motor function and probe neural circuits , 2003, Nature Reviews Neuroscience.

[34]  M. Schieber,et al.  How somatotopic is the motor cortex hand area? , 1993, Science.

[35]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[36]  H C Kwan,et al.  Spatial organization of precentral cortex in awake primates. II. Motor outputs. , 1978, Journal of neurophysiology.

[37]  F. Lacquaniti,et al.  Coordination of Locomotion with Voluntary Movements in Humans , 2005, The Journal of Neuroscience.

[38]  E. Bizzi,et al.  Linear combinations of primitives in vertebrate motor control. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Alvaro Pascual-Leone,et al.  Handbook of transcranial magnetic stimulation , 2002 .

[40]  Gene H. Golub,et al.  Matrix computations , 1983 .

[41]  Marc H Schieber,et al.  Human finger independence: limitations due to passive mechanical coupling versus active neuromuscular control. , 2004, Journal of neurophysiology.

[42]  F. Lacquaniti,et al.  Five basic muscle activation patterns account for muscle activity during human locomotion , 2004, The Journal of physiology.

[43]  J. F. Soechting,et al.  Postural Hand Synergies for Tool Use , 1998, The Journal of Neuroscience.

[44]  Martha Flanders,et al.  Flexibility and Repeatability of Finger Movements During Typing: Analysis of Multiple Degrees of Freedom , 1997, Journal of Computational Neuroscience.

[45]  F. A. Mussa-lvaldi,et al.  Convergent force fields organized in the frog's spinal cord , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  Tomaso Poggio,et al.  Generalization in vision and motor control , 2004, Nature.

[47]  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.

[48]  J. B. Preston,et al.  Two representations of the hand in area 4 of a primate. I. Motor output organization. , 1982, Journal of neurophysiology.

[49]  G. Edelman,et al.  Solving Bernstein's problem: a proposal for the development of coordinated movement by selection. , 1993, Child development.

[50]  J. F. Soechting,et al.  Biological constraints simplify the recognition of hand shapes , 2003, IEEE Transactions on Biomedical Engineering.

[51]  R.B. Stein,et al.  The role of neuromuscular properties in determining the end-point of a movement , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[52]  J. Donoghue,et al.  Shared neural substrates controlling hand movements in human motor cortex. , 1995, Science.

[53]  Carolyn R. Mason,et al.  Hand synergies during reach-to-grasp. , 2001, Journal of neurophysiology.

[54]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

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

[56]  Gene H. Golub,et al.  Matrix computations (3rd ed.) , 1996 .

[57]  R. Porter,et al.  Corticospinal Function and Voluntary Movement , 1993 .

[58]  Emilio Bizzi,et al.  Shared and specific muscle synergies in natural motor behaviors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.