Bilateral motor resonance evoked by observation of a one‐hand movement: role of the primary motor cortex

In humans, observation of movement performed by others evokes a subliminal motor resonant response, probably mediated by the mirror neurone system, which reproduces the motor commands needed to execute the observed movement with good spatial and temporal fidelity. Motor properties of the resonant response were here investigated with the ultimate goal of understanding the principles operating in the transformation from observation to internal reproduction of movement. Motor resonance was measured as the modulation of excitability of spinal motoneurones, evoked by the observation of a cyclic flexion‐extension of one hand. The first two experiments showed that the observation of a one‐hand movement always evoked a bimanual resonant response independent of which hand was observed and that these bilateral responses were consistently phase‐linked. H‐reflexes simultaneously recorded in right and left flexor carpi radialis muscles were always modulated ‘in‐phase’ with each other. The goal of the third experiment was to define the role of primary motor cortex in the bilateral resonant response. Bilateral H‐reflexes were recorded during a temporary inactivation induced by transcranial magnetic stimulation over the left cortical hand motor area of observers. The finding that such cortical depression abolished the H‐reflex modulation of only the right flexor carpi radialis motoneurones, leaving it unchanged on the left side, suggested that both primary motor areas were activated by the premotor cortex and transmit the resonant activation through crossed corticospinal pathways. The data provide further evidence that the subliminal activation of motor pathways induced by movement observation is organized according to general rules shared with the control of voluntary movement.

[1]  J. Mazziotta,et al.  Grasping the Intentions of Others with One's Own Mirror Neuron System , 2005, PLoS biology.

[2]  J. Classen,et al.  Inhibitory phenomena in individual motor units induced by transcranial magnetic stimulation. , 1995, Electroencephalography and clinical neurophysiology.

[3]  Alexander Münchau,et al.  Premotor transcranial direct current stimulation (tDCS) affects primary motor excitability in humans , 2008, The European journal of neuroscience.

[4]  Rob Ellis,et al.  Manual asymmetries in visually primed grasping , 2006, Experimental Brain Research.

[5]  N. A. Borghese,et al.  Different Brain Correlates for Watching Real and Virtual Hand Actions , 2001, NeuroImage.

[6]  Fausto Baldissera,et al.  Activation of motor pathways during observation and execution of hand movements , 2008, Social neuroscience.

[7]  M. Petrides,et al.  Orofacial somatomotor responses in the macaque monkey homologue of Broca's area , 2005, Nature.

[8]  G. Rizzolatti,et al.  Activation of human primary motor cortex during action observation: a neuromagnetic study. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[9]  M. Hallett,et al.  Effects of transcranial magnetic stimulation on ipsilateral muscles , 1991, Neurology.

[10]  K. Chiappa,et al.  Facilitation of magnetic motor evoked potential; during the cortical stimulation silent period , 1993, Neurology.

[11]  F. Baldissera,et al.  Anticipatory postural adjustments in arm muscles associated with movements of the contralateral limb and their possible role in interlimb coordination , 2008, Experimental Brain Research.

[12]  F. Baldissera,et al.  Excitability changes in human corticospinal projections to muscles moving hand and fingers while viewing a reaching and grasping action , 2005, The European journal of neuroscience.

[13]  J. Rothwell,et al.  Intracortical circuits modulate transcallosal inhibition in humans , 2007, The Journal of physiology.

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

[15]  C. G. Phillips,et al.  A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis) , 1987, The Journal of comparative neurology.

[16]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[17]  Laura Avanzino,et al.  Suppression of the transcallosal motor output: a transcranial magnetic stimulation study in healthy subjects , 2004, Experimental Brain Research.

[18]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

[19]  O. Boonyarom,et al.  Atrophy and hypertrophy of skeletal muscles: structural and functional aspects , 2006, Acta physiologica.

[20]  F. Baldissera,et al.  Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement , 2005, Brain Research.

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

[22]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[23]  Marco Iacoboni,et al.  Lateralization in motor facilitation during action observation: a TMS study , 2001, NeuroImage.

[24]  M. Hallett,et al.  Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscles , 1996, Experimental Brain Research.

[25]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[26]  Peter J Beek,et al.  Unraveling interlimb interactions underlying bimanual coordination. , 2005, Journal of neurophysiology.

[27]  P. Strick,et al.  Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’ areas , 1979, Brain Research.

[28]  S. Swinnen Intermanual coordination: From behavioural principles to neural-network interactions , 2002, Nature Reviews Neuroscience.

[29]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[30]  R. Hari,et al.  Temporal dynamics of cortical representation for action. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[31]  L. Craighero,et al.  Human motor cortex excitability during the perception of others’ action , 2005, Current Opinion in Neurobiology.

[32]  L. Wilkins Effects of transcranial magnetic stimulation on ipsilateral muscles , 1992, Neurology.

[33]  G. Rizzolatti,et al.  Neural Circuits Underlying Imitation Learning of Hand Actions An Event-Related fMRI Study , 2004, Neuron.

[34]  Carlo Adolfo Porro,et al.  Bilateral representation of sequential finger movements in human cortical areas , 1999, Neuroscience Letters.

[35]  Nadia Bolognini,et al.  Somatic and Motor Components of Action Simulation , 2007, Current Biology.

[36]  Tzvi Ganel,et al.  Hemispheric specialization for the visual control of action is independent of handedness. , 2006, Journal of neurophysiology.

[37]  K. R. Mills,et al.  Magnetic Stimulation of the Human Nervous System , 2000 .

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

[39]  S. Fecteau,et al.  Modulation of motor cortex excitability during action observation in disconnected hemispheres , 2005, Neuroreport.

[40]  P H Ellaway,et al.  Suppression of voluntary motor activity revealed using transcranial magnetic stimulation of the motor cortex in man. , 1994, The Journal of physiology.

[41]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

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

[43]  R. Lemon,et al.  Facilitation from ventral premotor cortex of primary motor cortex outputs to macaque hand muscles. , 2003, Journal of neurophysiology.

[44]  G. Rizzolatti,et al.  Localization of grasp representations in humans by PET: 1. Observation versus execution , 1996, Experimental Brain Research.

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

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

[47]  S. Cochin,et al.  Observation and execution of movement: similarities demonstrated by quantified electroencephalography , 1999, The European journal of neuroscience.

[48]  U. Castiello,et al.  The Human Premotor Cortex Is 'Mirror' Only for Biological Actions , 2004, Current Biology.

[49]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[50]  G. Rizzolatti The mirror neuron system and its function in humans , 2005, Anatomy and Embryology.

[51]  A. Kohn,et al.  Bilateral soleus H-reflexes in humans elicited by simultaneous trains of stimuli: symmetry, variability, and covariance. , 2002, Journal of neurophysiology.

[52]  P. Strick,et al.  Motor areas in the frontal lobe of the primate , 2002, Physiology & Behavior.

[53]  C. Frith,et al.  Dissociable neural pathways for the perception and recognition of expressive and instrumental gestures , 2004, Neuropsychologia.

[54]  R. Lemon,et al.  Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. , 2004, The Journal of Neuroscience.

[55]  J. Rothwell,et al.  Functional Connectivity of Human Premotor and Motor Cortex Explored with Repetitive Transcranial Magnetic Stimulation , 2002, The Journal of Neuroscience.

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

[57]  Kisou Kubota,et al.  Cortical projection to hand-arm motor area from post-arcuate area in macaque monkeys: A histological study of retrograde transport of horseradish peroxidase , 1979, Neuroscience Letters.

[58]  B. Day,et al.  Interhemispheric inhibition of the human motor cortex. , 1992, The Journal of physiology.

[59]  T Brochier,et al.  Simultaneous recording of macaque premotor and primary motor cortex neuronal populations reveals different functional contributions to visuomotor grasp. , 2007, Journal of neurophysiology.

[60]  W D Byblow,et al.  Excitability changes in human forearm corticospinal projections and spinal reflex pathways during rhythmic voluntary movement of the opposite limb , 2004, The Journal of physiology.

[61]  Marc A. Maier,et al.  Pronounced Reduction of Digit Motor Responses Evoked from Macaque Ventral Premotor Cortex after Reversible Inactivation of the Primary Motor Cortex Hand Area , 2008, The Journal of Neuroscience.

[62]  R. J. Seitz,et al.  A fronto‐parietal circuit for object manipulation in man: evidence from an fMRI‐study , 1999, The European journal of neuroscience.