Selective responses in right inferior frontal and supramarginal gyri differentiate between observed movements of oneself vs. another

The fact that inferior frontal (IFg) and supramarginal (SMg) gyri respond to both self-generated and observed actions has been interpreted as evidence for a perception-action linking mechanism (mirroring). Yet, the brain readily distinguishes between percepts generated by one's own movements vs. those of another. Do IFg and/or SMg respond differentially to these visual stimuli even when carefully matched? We used BOLD fMRI to address this question as participants made repetitive bimanual hand movements while viewing either live visual feedback or perceptually similar, pre-recorded video of an actor. As expected, bilateral IFg and SMg increased activity during both conditions. However, right SMg and IFg responded differentially during live visual feedback vs. matched recordings. These mirror system areas may distinguish self-generated percepts by detecting subtle spatio-temporal differences between predicted and actual sensory feedback and/or visual and somatosensory signals.

[1]  Timothy Edward John Behrens,et al.  Connection patterns distinguish 3 regions of human parietal cortex. , 2006, Cerebral cortex.

[2]  Jean Decety,et al.  Leader or follower? Involvement of the inferior parietal lobule in agency , 2002, Neuroreport.

[3]  N. Kanwisher,et al.  fMRI Adaptation Reveals Mirror Neurons in Human Inferior Parietal Cortex , 2008, Current Biology.

[4]  S. Blakemore,et al.  Action prediction in the cerebellum and in the parietal lobe , 2003, Experimental Brain Research.

[5]  G. G. Gallop.  Chimpanzees: self-recognition. , 1970, Science.

[6]  E. Zohary,et al.  Mirror-image representation of action in the anterior parietal cortex , 2008, Nature Neuroscience.

[7]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

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

[9]  Alfonso Caramazza,et al.  Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans , 2009, Proceedings of the National Academy of Sciences.

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

[11]  Istvan Molnar-Szakacs,et al.  Self-face recognition activates a frontoparietal “mirror” network in the right hemisphere: an event-related fMRI study , 2005, NeuroImage.

[12]  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.

[13]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[14]  Marco Iacoboni,et al.  The self across the senses: an fMRI study of self-face and self-voice recognition. , 2008, Social cognitive and affective neuroscience.

[15]  Crossmodal action representations 1 2 Surface-based information mapping reveals crossmodal vision-action 3 representations in human parietal and occipitotemporal cortex 4 5 6 , 2010 .

[16]  S. Blakemore,et al.  Delusions of alien control in the normal brain , 2003, Neuropsychologia.

[17]  D. Wolpert,et al.  Internal models in the cerebellum , 1998, Trends in Cognitive Sciences.

[18]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[19]  D. Wolpert,et al.  Motor prediction , 2001, Current Biology.

[20]  Marc Jeannerod,et al.  Modulating the experience of agency: a positron emission tomography study , 2003, NeuroImage.

[21]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[22]  Nava Rubin,et al.  Brain areas selective for both observed and executed movements. , 2007, Journal of neurophysiology.

[23]  M. Jeannerod,et al.  Beyond Consciousness of External Reality: A “Who” System for Consciousness of Action and Self-Consciousness , 1998, Consciousness and Cognition.

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

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

[26]  Atsushi Sato,et al.  Illusion of sense of self-agency: discrepancy between the predicted and actual sensory consequences of actions modulates the sense of self-agency, but not the sense of self-ownership , 2005, Cognition.

[27]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[28]  J. Krakauer,et al.  A computational neuroanatomy for motor control , 2008, Experimental Brain Research.

[29]  Á. Pascual-Leone,et al.  Neurology: Self-recognition and the right hemisphere , 2001, Nature.

[30]  David J. Turk,et al.  The angular gyrus computes action awareness representations. , 2008, Cerebral cortex.

[31]  G. Luppino,et al.  Cortical connections of the inferior parietal cortical convexity of the macaque monkey. , 2006, Cerebral cortex.

[32]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[33]  Justin L. Gardner,et al.  Executed and Observed Movements Have Different Distributed Representations in Human aIPS , 2008, The Journal of Neuroscience.

[34]  H. Freund.  Higher-order motor disorders : from neuroanatomy and neurobiology to clinical neurology , 2005 .

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

[36]  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.

[37]  D M Wolpert,et al.  Predicting the Consequences of Our Own Actions: The Role of Sensorimotor Context Estimation , 1998, The Journal of Neuroscience.

[38]  C. Frith,et al.  Self-awareness and action , 2003, Current Opinion in Neurobiology.

[39]  Karl J. Friston,et al.  Evidence of Mirror Neurons in Human Inferior Frontal Gyrus , 2009, The Journal of Neuroscience.

[40]  M. Iacoboni,et al.  The self and social cognition: the role of cortical midline structures and mirror neurons , 2007, Trends in Cognitive Sciences.

[41]  Andrew N. Meltzoff,et al.  Neural circuits involved in imitation and perspective-taking , 2006, NeuroImage.

[42]  G. Gallup.  Chimpanzees: Self-Recognition , 1970, Science.

[43]  A. Meltzoff,et al.  A PET Exploration of the Neural Mechanisms Involved in Reciprocal Imitation , 2002, NeuroImage.

[44]  P. Haggard,et al.  Neural signatures of body ownership: a sensory network for bodily self-consciousness. , 2007, Cerebral cortex.

[45]  K. Grabska.  DISORDERS OF BODY SCHEME AFTER STROKE , 2007 .