Repetitive Transcranial Magnetic Stimulation to the Primary Motor Cortex Interferes with Motor Learning by Observing

Neural representations of novel motor skills can be acquired through visual observation. We used repetitive transcranial magnetic stimulation (rTMS) to test the idea that this “motor learning by observing” is based on engagement of neural processes for learning in the primary motor cortex (M1). Human subjects who observed another person learning to reach in a novel force environment imposed by a robot arm performed better when later tested in the same environment than subjects who observed movements in a different environment. rTMS applied to M1 after observation reduced the beneficial effect of observing congruent forces, and eliminated the detrimental effect of observing incongruent forces. Stimulation of a control site in the frontal cortex had no effect on reaching. Our findings represent the first direct evidence that neural representations of motor skills in M1, a cortical region whose role has been firmly established for active motor learning, also underlie motor learning by observing.

[1]  Simon J. Bennett,et al.  General motor representations are developed during action-observation , 2010, Experimental Brain Research.

[2]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[3]  Laura Petrosini,et al.  “Do What I Do” and “Do How I Do”: Different Components of Imitative Learning Are Mediated by Different Neural Structures , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[4]  T. Flash,et al.  The coordination of arm movements: an experimentally confirmed mathematical model , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  C. Heyes,et al.  Motor learning by observation: Evidence from a serial reaction time task , 2002, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[6]  Andrew A G Mattar,et al.  Motor Learning by Observing , 2005, Neuron.

[7]  Hagai Bergman,et al.  Emerging Patterns of Neuronal Responses in Supplementary and Primary Motor Areas during Sensorimotor Adaptation , 2005, The Journal of Neuroscience.

[8]  W. T. Thach,et al.  Motor mechanisms of the CNS: cerebrocerebellar interrelations. , 1969, Annual review of physiology.

[9]  G. Rizzolatti,et al.  Understanding motor events: a neurophysiological study , 2004, Experimental Brain Research.

[10]  M. Hallett,et al.  Early consolidation in human primary motor cortex , 2002, Nature.

[11]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  T. Paus,et al.  Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study , 2000, Neuroreport.

[13]  J. Rothwell,et al.  Transcranial magnetic stimulation in cognitive neuroscience – virtual lesion, chronometry, and functional connectivity , 2000, Current Opinion in Neurobiology.

[14]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[15]  A Bandura,et al.  Representational guidance of action production in observational learning: a causal analysis. , 1990, Journal of motor behavior.

[16]  T. Paus Imaging the brain before, during, and after transcranial magnetic stimulation , 1998, Neuropsychologia.

[17]  Ehud Zohary,et al.  Dissociation between Ventral and Dorsal fMRI Activation during Object and Action Recognition , 2005, Neuron.

[18]  Mitsuo Kawato,et al.  MOSAIC Model for Sensorimotor Learning and Control , 2001, Neural Computation.

[19]  Á. Pascual-Leone,et al.  Phase-specific modulation of cortical motor output during movement observation , 2001, Neuroreport.

[20]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. , 1997, Journal of neurophysiology.

[21]  E. Evarts,et al.  Relation of pyramidal tract activity to force exerted during voluntary movement. , 1968, Journal of neurophysiology.

[22]  Philippe A. Chouinard,et al.  Role of the Primary Motor and Dorsal Premotor Cortices in the Anticipation of Forces during Object Lifting , 2005, The Journal of Neuroscience.

[23]  C. Heyes,et al.  SOCIAL LEARNING IN ANIMALS: CATEGORIES AND MECHANISMS , 1994, Biological reviews of the Cambridge Philosophical Society.

[24]  J. Kalaska,et al.  A comparison of movement direction-related versus load direction- related activity in primate motor cortex, using a two-dimensional reaching task , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  R. Shadmehr,et al.  Neural correlates of motor memory consolidation. , 1997, Science.

[26]  A. Bandura Social Foundations of Thought and Action: A Social Cognitive Theory , 1985 .

[27]  E. Vaadia,et al.  Preparatory activity in motor cortex reflects learning of local visuomotor skills , 2003, Nature Neuroscience.

[28]  Paolo Manganotti,et al.  Modulation of motor cortex excitability in the left hemisphere during action observation: a single- and paired-pulse transcranial magnetic stimulation study of self- and non-self-action observation , 2003, Neuropsychologia.

[29]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[30]  C. Heyes,et al.  A Demonstration of Observational Learning in Rats using a Bidirectional Control , 1990, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[31]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 2004, Experimental Brain Research.

[32]  P. Strick,et al.  Relation of basal ganglia, cerebellum, and motor cortex units to ramp and ballistic limb movements. , 1974, Brain research.

[33]  J. Kalaska,et al.  Motor cortex neural correlates of output kinematics and kinetics during isometric-force and arm-reaching tasks. , 2005, Journal of neurophysiology.

[34]  J. Kalaska,et al.  Systematic changes in motor cortex cell activity with arm posture during directional isometric force generation. , 2003, Journal of neurophysiology.

[35]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. , 1997, Journal of neurophysiology.

[36]  Barbara Tversky,et al.  Perspective taking promotes action understanding and learning. , 2006, Journal of experimental psychology. Human perception and performance.

[37]  Stephen H. Scott,et al.  Overlap of internal models in motor cortex for mechanical loads during reaching , 2002, Nature.

[38]  G. Rizzolatti,et al.  Coding of peripersonal space in inferior premotor cortex (area F4). , 1996, Journal of neurophysiology.

[39]  Nicola J. Hodges,et al.  Absence of after-effects for observers after watching a visuomotor adaptation , 2010, Experimental Brain Research.

[40]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[41]  Philippe A. Chouinard,et al.  Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. , 2003, Journal of neurophysiology.

[42]  Scott T. Grafton,et al.  Motor Learning of Compatible and Incompatible Visuomotor Maps , 2001, Journal of Cognitive Neuroscience.

[43]  E. Bizzi,et al.  Cortical correlates of learning in monkeys adapting to a new dynamical environment. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[45]  Sara Torriero,et al.  The What and How of Observational Learning , 2007, Journal of Cognitive Neuroscience.

[46]  Paul B. Johnson,et al.  Making arm movements within different parts of space: dynamic aspects in the primate motor cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  A Bandura,et al.  Translating cognition into action: the role of visual guidance in observational learning. , 1987, Journal of motor behavior.

[48]  Emanuele Lo Gerfo,et al.  Changes in Cerebello-motor Connectivity during Procedural Learning by Actual Execution and Observation , 2011, Journal of Cognitive Neuroscience.

[49]  R Caminiti,et al.  Making arm movements within different parts of space: the premotor and motor cortical representation of a coordinate system for reaching to visual targets , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  Leslie G. Ungerleider,et al.  The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[51]  V. Gallese Action representaion and the inferior parietal lobule , 2000 .

[52]  T. Paus,et al.  Seeing and hearing speech excites the motor system involved in speech production , 2003, Neuropsychologia.

[53]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[54]  M. Hallett,et al.  Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation , 1997, Neurology.

[55]  E. Bizzi,et al.  Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field , 2001, Neuron.

[56]  Albert Bandura,et al.  Role of Symbolic Coding and Rehearsal Processes in Observational Learning. , 1973 .

[57]  E. Evarts Activity of pyramidal tract neurons during postural fixation. , 1969, Journal of neurophysiology.

[58]  L. Craighero,et al.  Modulation of spinal excitability during observation of hand actions in humans , 2001, The European journal of neuroscience.

[59]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[60]  Nitzan Censor,et al.  Using repetitive transcranial magnetic stimulation to study the underlying neural mechanisms of human motor learning and memory , 2010, The Journal of physiology.

[61]  Seyed M. Mirsattari,et al.  Proactive Interference as a Result of Persisting Neural Representations of Previously Learned Motor Skills in Primary Motor Cortex , 2006, Journal of Cognitive Neuroscience.

[62]  A. Murata,et al.  Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4) , 1999, Experimental Brain Research.

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

[64]  J. Flanagan,et al.  Independence of perceptual and sensorimotor predictions in the size–weight illusion , 2000, Nature Neuroscience.

[65]  G. Rizzolatti,et al.  Motor facilitation during action observation: a magnetic stimulation study. , 1995, Journal of neurophysiology.

[66]  Ehud Zohary,et al.  A Mirror Representation of Others' Actions in the Human Anterior Parietal Cortex , 2006, The Journal of Neuroscience.

[67]  S. Scott,et al.  Dissociation between hand motion and population vectors from neural activity in motor cortex , 2022 .

[68]  W. T. Thach Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. , 1978, Journal of neurophysiology.

[69]  Leslie G. Ungerleider,et al.  Formation of a Motor Memory by Action Observation , 2005, The Journal of Neuroscience.

[70]  Dana Maslovat,et al.  Observational practice benefits are limited to perceptual improvements in the acquisition of a novel coordination skill , 2010, Experimental Brain Research.

[71]  R. Johansson,et al.  Prediction Precedes Control in Motor Learning , 2003, Current Biology.

[72]  Sarah E. Criscimagna-Hemminger,et al.  Contributions of the motor cortex to adaptive control of reaching depend on the perturbation schedule. , 2011, Cerebral cortex.

[73]  Marjan Jahanshahi,et al.  Transcranial magnetic stimulation studies of cognition: an emerging field , 2000, Experimental Brain Research.

[74]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 1988, Experimental Brain Research.