Don't Do It! Cortical Inhibition and Self-attribution during Action Observation

Numerous studies suggest that both self-generated and observed actions of others activate overlapping neural networks, implying a shared, agent-neutral representation of self and other. Contrary to the shared representation hypothesis, we recently showed that the human motor system is not neutral with respect to the agent of an observed action [Schtz-Bosbach, S., Mancini, B., Aglioti, S. M., & Haggard, P. Self and other in the human motor system. Current Biology, 16, 18301834, 2006]. Observation of actions attributed to another agent facilitated the motor system, whereas observation of identical actions linked to the self did not. Here we investigate whether the absence of motor facilitation for observing one's own actions reflects a specific process of cortical inhibition associated with self-representation. We analyzed the duration of the silent period induced by transcranial magnetic stimulation of the motor cortex in active muscles as an indicator of motor inhibition. We manipulated whether an observed action was attributed to another agent, or to the subjects themselves, using a manipulation of body ownership on the basis of the rubber hand illusion. Observation of actions linked to the self led to longer silent periods than observation of a static hand, but the opposite effect occurred when observing identical actions attributed to another agent. This finding suggests a specific inhibition of the motor system associated with self-representation. Cortical suppression for actions linked to the self might prevent inappropriate perseveration within the motor system.

[1]  Matthew R Longo,et al.  Imitative response tendencies following observation of intransitive actions. , 2006, Journal of experimental psychology. Human perception and performance.

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

[3]  M. Hallett,et al.  Role of intracortical mechanisms in the late part of the silent period to transcranial stimulation of the human motor cortex , 1995, Acta neurologica Scandinavica.

[4]  C. Frith,et al.  Experiencing Oneself vs Another Person as Being the Cause of an Action: The Neural Correlates of the Experience of Agency , 2002, NeuroImage.

[5]  D. Wolpert,et al.  Abnormalities in the awareness and control of action. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  P. Haggard Conscious intention and motor cognition , 2005, Trends in Cognitive Sciences.

[7]  J. Rothwell,et al.  Transcranial magnetic stimulation: new insights into representational cortical plasticity , 2002, Experimental Brain Research.

[8]  J. Brasil-Neto,et al.  Postexercise facilitation of motor evoked potentials elicited by ipsilateral voluntary contraction , 1999, Muscle & nerve.

[9]  Ulf Ziemann,et al.  The role of GABA(B) receptors in intracortical inhibition in the human motor cortex. , 2006, Experimental brain research.

[10]  M. Jeannerod,et al.  Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients , 1997, Cognition.

[11]  Ellin Kofsky Scholnick,et al.  Conceptual Development : Piaget's Legacy , 1999 .

[12]  K J Werhahn,et al.  Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans , 1999, The Journal of physiology.

[13]  S. C. Gandevia,et al.  Effect of contraction strength on responses in biceps brachii and adductor pollicis to transcranial magnetic stimulation , 1997, Experimental Brain Research.

[14]  M. Hallett,et al.  Optimal Focal Transcranial Magnetic Activation of the Human Motor Cortex: Effects of Coil Orientation, Shape of the Induced Current Pulse, and Stimulus Intensity , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[15]  Manos Tsakiris,et al.  A specific role for efferent information in self-recognition , 2005, Cognition.

[16]  D. Wolpert,et al.  Sensorimotor attenuation by central motor command signals in the absence of movement , 2006, Nature Neuroscience.

[17]  Alfons Schnitzler,et al.  The silent period after transcranial magnetic stimulation is of exclusive cortical origin: evidence from isolated cortical ischemic lesions in man , 1994, Neuroscience Letters.

[18]  H. Théoret,et al.  Modulation of Motor Cortex Excitability by Physical Similarity with an Observed Hand Action , 1995, PLoS ONE.

[19]  P. Haggard,et al.  Self and Other in the Human Motor System , 2006, Current Biology.

[20]  D. Wolpert,et al.  Central cancellation of self-produced tickle sensation , 1998, Nature Neuroscience.

[21]  M. Erb,et al.  Observing one’s hand become anarchic: An fMRI study of action identification , 2003, Consciousness and Cognition.

[22]  Stefano Facchini,et al.  Motor facilitation of the human cortico-spinal system during observation of bio-mechanically impossible movements , 2005, NeuroImage.

[23]  Toshio Higashi,et al.  Increased corticospinal excitability during direct observation of self-movement and indirect observation with a mirror box , 2007, Neuroscience Letters.

[24]  M Hallett,et al.  Changes in motor cortex excitability during ipsilateral hand muscle activation in humans , 2000, Clinical Neurophysiology.

[25]  B. Shahani,et al.  Motor inhibition and excitation are independent effects of magnetic cortical stimulation , 1992, Annals of neurology.

[26]  M. Jeannerod Neural Simulation of Action: A Unifying Mechanism for Motor Cognition , 2001, NeuroImage.

[27]  O. Güntürkün,et al.  Laterality in the rubber hand illusion , 2011, Laterality.

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

[29]  I. Tarkka,et al.  CHARACTERISTICS OF THE SILENT PERIOD AFTER TRANSCRANIAL MAGNETIC STIMULATION , 1994, American journal of physical medicine & rehabilitation.

[30]  M. Jeannerod,et al.  Limited conscious monitoring of motor performance in normal subjects , 1998, Neuropsychologia.

[31]  A Berardelli,et al.  Cortical mechanisms mediating the inhibitory period after magnetic stimulation of the facial motor area , 1997, Muscle & nerve.

[32]  Marc Jeannerod,et al.  Agency, simulation and self-identification , 2004 .

[33]  P. Ashby,et al.  Mechanism of the silent period following transcranial magnetic stimulation Evidence from epidural recordings , 1999, Experimental Brain Research.

[34]  M. Denckla The human frontal lobes: Functions and disorders , 1999 .

[35]  Sven Bernecker,et al.  Knowledge : readings in contemporary epistemology , 2000 .

[36]  W. Dunlap,et al.  Meta-Analysis of Experiments With Matched Groups or Repeated Measures Designs , 1996 .

[37]  C E Chapman,et al.  Active versus passive touch: factors influencing the transmission of somatosensory signals to primary somatosensory cortex. , 1994, Canadian journal of physiology and pharmacology.

[38]  L. Weiskrantz,et al.  Preliminary Observations on Tickling Oneself , 1971, Nature.

[39]  Sachiko Koyama,et al.  Gating of somatosensory evoked responses during active finger movements: magnetoencephalographic studies , 1995, Journal of the Neurological Sciences.

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

[41]  W. Prinz,et al.  Compatibility between Observed and Executed Finger Movements: Comparing Symbolic, Spatial, and Imitative Cues , 2000, Brain and Cognition.

[42]  Marcel Brass,et al.  The Inhibition of Imitative Response Tendencies , 2001, NeuroImage.

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

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

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

[46]  R. Mutani,et al.  Magnetic brain stimulation: the silent period after the motor evoked potential. , 1992, Neurology.

[47]  M. Jeannerod,et al.  Sense of body and sense of action both contribute to self-recognition , 2002, Cognition.

[48]  J Valls-Solé,et al.  Topography of the inhibitory and excitatory responses to transcranial magnetic stimulation in a hand muscle. , 1993, Electroencephalography and clinical neurophysiology.

[49]  Y. Lamarre,et al.  Modulation of the cutaneous responsiveness of neurones in the primary somatosensory cortex during conditioned arm movements in the monkey , 2004, Experimental Brain Research.

[50]  Nadim Joni Shah,et al.  Neural Representations of Self versus Other: Visual-Spatial Perspective Taking and Agency in a Virtual Ball-tossing Game , 2006, Journal of Cognitive Neuroscience.

[51]  Cosimo Urgesi,et al.  Corticospinal facilitation during first and third person imagery , 2005, Experimental Brain Research.

[52]  Zafiris J Daskalakis,et al.  Transcranial magnetic stimulation: a new investigational and treatment tool in psychiatry. , 2002, The Journal of neuropsychiatry and clinical neurosciences.

[53]  D. Wolpert,et al.  Abnormalities in the awareness of action , 2002, Trends in Cognitive Sciences.

[54]  M. Jeannerod Simulation of action as a unifying concept for motor cognition. , 2003 .

[55]  G. Claxton Why Can't We Tickle Ourselves? , 1975, Perceptual and motor skills.

[56]  B. Steinhoff,et al.  Effects of antiepileptic drugs on motor cortex excitability in humans: A transcranial magnetic stimulation study , 1996, Annals of neurology.

[57]  B Conrad,et al.  Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia , 1998, Muscle & nerve.

[58]  Manuel Carreiras,et al.  Hands on the future: facilitation of cortico‐spinal hand‐representation when reading the future tense of hand‐related action verbs , 2010, The European journal of neuroscience.

[59]  Jean Decety,et al.  When the self represents the other: A new cognitive neuroscience view on psychological identification , 2003, Consciousness and Cognition.

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

[61]  Michela Romani,et al.  Motor facilitation during action observation: topographic mapping of the target muscle and influence of the onlooker's posture , 2006, The European journal of neuroscience.

[62]  E. Wassermann Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[63]  Jacob Cohen,et al.  A power primer. , 1992, Psychological bulletin.

[64]  P. Haggard,et al.  The rubber hand illusion revisited: visuotactile integration and self-attribution. , 2005, Journal of experimental psychology. Human perception and performance.

[65]  D. Stuss,et al.  Principles of frontal lobe function , 2002 .

[66]  John Schwoebel,et al.  The man who executed “imagined” movements: Evidence for dissociable components of the body schema , 2002, Brain and Cognition.

[67]  Stefano Tamburin,et al.  Cutaneomotor integration in human hand motor areas: somatotopic effect and interaction of afferents , 2001, Experimental Brain Research.

[68]  K. Stefan,et al.  Modulation of associative human motor cortical plasticity by attention. , 2004, Journal of neurophysiology.

[69]  Jonathan D. Cohen,et al.  Rubber hands ‘feel’ touch that eyes see , 1998, Nature.

[70]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[71]  S. Boniface,et al.  Magnetic brain stimulation with a double coil: the importance of coil orientation. , 1992, Electroencephalography and clinical neurophysiology.

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

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

[74]  M. Eimer,et al.  Effects of masked stimuli on motor activation: behavioral and electrophysiological evidence. , 1998, Journal of experimental psychology. Human perception and performance.

[75]  Antonia F. de C. Hamilton,et al.  Understanding actors and object-goals in the human brain , 2010, NeuroImage.

[76]  Richard P. DeShon,et al.  Combining effect size estimates in meta-analysis with repeated measures and independent-groups designs. , 2002, Psychological methods.

[77]  P. Haggard,et al.  Action observation and execution: What is shared? , 2008, Social neuroscience.

[78]  A Rothenberger,et al.  Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. , 1997, The American journal of psychiatry.

[79]  E. Kunesch,et al.  Paired associative stimulation. , 2004, Supplements to Clinical neurophysiology.

[80]  J. Summers,et al.  Mirror, mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability , 2005, Experimental Brain Research.

[81]  J. Marshall,et al.  The neural consequences of conflict between intention and the senses. , 1999, Brain : a journal of neurology.

[82]  D. Wolpert Computational approaches to motor control , 1997, Trends in Cognitive Sciences.

[83]  R. Mutani,et al.  Parkinson's disease rigidity , 1991, Neurology.

[84]  R N Lemon,et al.  Task dependence of responses in first dorsal interosseous muscle to magnetic brain stimulation in man. , 1993, The Journal of physiology.

[85]  J. Chapin,et al.  Somatic sensory transmission to the cortex during movement: Gating of single cell responses to touch , 1982, Experimental Neurology.

[86]  M. Jeannerod The mechanism of self-recognition in humans , 2003, Behavioural Brain Research.

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

[88]  M Hallett,et al.  Transcranial magnetic stimulation. Negative effects. , 1995, Advances in neurology.