Predictive representation of other people's actions in joint action planning: An EEG study

It has been postulated that when people engage in joint actions they form internal representations not only of their part of the joint task but of their co-actors' parts of the task as well. However, empirical evidence for this claim is scarce. By means of high-density electroencephalography, this study investigated whether one represents and simulates the action of an interaction partner when planning to perform a joint action. The results showed that joint action planning compared with individual action planning resulted in amplitude modulations of the frontal P3a and parietal P3b event-related potentials, which are associated with stimulus classification, updating of representations, and decision-making. Moreover, there was evidence for anticipatory motor simulation of the partner's action in the amplitude and peak latency of the late, motor part of the Contingent Negative Variation, which was correlated with joint action performance. Our results provide evidence that when people engage in joint tasks, they represent in advance each other's actions in order to facilitate coordination.

[1]  Warren H. Meck,et al.  Contingent negative variation and its relation to time estimation: a theoretical evaluation , 2011, Front. Integr. Neurosci..

[2]  J. Decety,et al.  How Would You Feel versus How Do You Think She Would Feel? A Neuroimaging Study of Perspective-Taking with Social Emotions , 2004, Journal of Cognitive Neuroscience.

[3]  Hannes Rakoczy,et al.  Minds, persons, and space: An fMRI investigation into the relational complexity of higher-order intentionality , 2008, Consciousness and Cognition.

[4]  S. Blakemore,et al.  Motor activation prior to observation of a predicted movement , 2004, Nature Neuroscience.

[5]  Wolfgang Prinz,et al.  Twin Peaks: An ERP Study of Action Planning and Control in Coacting Individuals , 2006, Journal of Cognitive Neuroscience.

[6]  Harold Bekkering,et al.  Fast responders have blinders on: ERP correlates of response inhibition in competition , 2008, Cortex.

[7]  Brian A. Lopez,et al.  P3a from visual stimuli: task difficulty effects. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[8]  Günther Knoblich,et al.  Favouritism in the motor system: social interaction modulates action simulation , 2010, Biology Letters.

[9]  M. Scherg,et al.  Localizing P300 Generators in Visual Target and Distractor Processing: A Combined Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2004, The Journal of Neuroscience.

[10]  Karl J. Friston,et al.  Predictive coding: an account of the mirror neuron system , 2007, Cognitive Processing.

[11]  Rolf Verleger,et al.  P3b: Towards some decision about memory , 2008, Clinical Neurophysiology.

[12]  Henk Aarts,et al.  When competition merges people's behavior: Interdependency activates shared action representations , 2010 .

[13]  E. Maguire,et al.  A Temporoparietal and Prefrontal Network for Retrieving the Spatial Context of Lifelike Events , 2001, NeuroImage.

[14]  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.

[15]  E. John,et al.  Evoked-Potential Correlates of Stimulus Uncertainty , 1965, Science.

[16]  O. Blanke,et al.  Neural Basis of Embodiment: Distinct Contributions of Temporoparietal Junction and Extrastriate Body Area , 2006, The Journal of Neuroscience.

[17]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[18]  Arne D. Ekstrom,et al.  Single-Neuron Responses in Humans during Execution and Observation of Actions , 2010, Current Biology.

[19]  J. Decety,et al.  Motor cognition: a new paradigm to study self–other interactions , 2004, Current Opinion in Neurobiology.

[20]  U. Castiello,et al.  The case of Dr. Jekyll and Mr. Hyde: A kinematic study on social intention , 2008, Consciousness and Cognition.

[21]  C. Vesper,et al.  Motion coordination affects movement parameters in a joint pick-and-place task , 2009, Quarterly journal of experimental psychology.

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

[23]  J. Decety,et al.  Effect of subjective perspective taking during simulation of action: a PET investigation of agency , 2001, Nature Neuroscience.

[24]  Angela Sirigu,et al.  Body and movement: Consciousness in the parietal lobes , 2010, Neuropsychologia.

[25]  Martin Garwicz,et al.  Authenticity, Depression, and Deep Brain Stimulation , 2011, Front. Integr. Neurosci..

[26]  Dana Samson,et al.  Left temporoparietal junction is necessary for representing someone else's belief , 2004, Nature Neuroscience.

[27]  R. Miall,et al.  A system in the human brain for predicting the actions of others , 2004, Nature Neuroscience.

[28]  G. Fink,et al.  Being with virtual others: Neural correlates of social interaction , 2006, Neuropsychologia.

[29]  Jiajin Yuan,et al.  Event-related potential correlates of the collective self-relevant effect , 2009, Neuroscience Letters.

[30]  D. Kourtis,et al.  Neurophysiology of Implicit Timing in Serial Choice Reaction-Time Performance , 2006, The Journal of Neuroscience.

[31]  Kenneth M. Heilman,et al.  Left-Hemisphere Motor Dominance in Righthandersi , 1980, Cortex.

[32]  G. Aschersleben,et al.  The Theory of Event Coding (TEC): a framework for perception and action planning. , 2001, The Behavioral and brain sciences.

[33]  H. Gray,et al.  P300 as an index of attention to self-relevant stimuli , 2004 .

[34]  A. Nowicka,et al.  Allocation of attention to self-name and self-face: An ERP study , 2010, Biological Psychology.

[35]  W. Prinz.  Perception and Action Planning , 1997 .

[36]  Frank Van Overwalle,et al.  Understanding others' actions and goals by mirror and mentalizing systems: A meta-analysis , 2009, NeuroImage.

[37]  Jiang Qiu,et al.  The neural basis of self-evaluation processing in social judgment , 2010, Neuroreport.

[38]  J. Sommerville,et al.  Shared representations between self and other: a social cognitive neuroscience view , 2003, Trends in Cognitive Sciences.

[39]  E. Donchin,et al.  Is the P300 component a manifestation of context updating? , 1988, Behavioral and Brain Sciences.

[40]  Robert Oostenveld,et al.  Motor-cortical beta oscillations are modulated by correctness of observed action , 2008, NeuroImage.

[41]  A. Gunji,et al.  Event-related potentials of self-face recognition in children with pervasive developmental disorders , 2009, Brain and Development.

[42]  K. Zilles,et al.  Neural Correlates of First-Person Perspective as One Constituent of Human Self-Consciousness , 2004, Journal of Cognitive Neuroscience.

[43]  Christian Keysers,et al.  Expanding the mirror: vicarious activity for actions, emotions, and sensations , 2009, Current Opinion in Neurobiology.

[44]  Hartmut Leuthold,et al.  Planning of rapid aiming movements and the contingent negative variation: are movement duration and extent specified independently? , 2009, Psychophysiology.

[45]  H. Walter,et al.  The intentional network: How the brain reads varieties of intentions , 2007, Neuropsychologia.

[46]  Andrea Brovelli,et al.  EEG dynamics of the frontoparietal network during reaching preparation in humans , 2007, NeuroImage.

[47]  H. Bekkering,et al.  Modulation of activity in medial frontal and motor cortices during error observation , 2004, Nature Neuroscience.

[48]  G. Knoblich,et al.  Action coordination in groups and individuals: learning anticipatory control. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

[49]  H. Sackeim,et al.  Parietal cortex and representation of the mental Self. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[50]  W. Prinz,et al.  How two share a task: corepresenting stimulus-response mappings. , 2005, Journal of experimental psychology. Human perception and performance.

[51]  I. Jentzsch,et al.  Neural correlates of advance movement preparation: a dipole source analysis approach. , 2001, Brain research. Cognitive brain research.

[52]  Lindsey J. Powell,et al.  It's the Thought That Counts , 2006, Psychological science.

[53]  Piotr Jaskowski,et al.  Evidence for an Integrative Role of P3b in Linking Reaction to Perception , 2005 .

[54]  D. Linden.  The P300: Where in the Brain Is It Produced and What Does It Tell Us? , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[55]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

[56]  W. Walter,et al.  Contingent Negative Variation : An Electric Sign of Sensori-Motor Association and Expectancy in the Human Brain , 1964, Nature.

[57]  Wen-Jui Kuo,et al.  A common coding framework in self–other interaction: evidence from joint action task , 2006, Experimental Brain Research.

[58]  W. Prinz,et al.  Perceptual resonance: action-induced modulation of perception , 2007, Trends in Cognitive Sciences.

[59]  Richard A. Andersen,et al.  FMRI evidence for a 'parietal reach region' in the human brain , 2003, Experimental Brain Research.

[60]  G. Rizzolatti,et al.  The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations , 2010, Nature Reviews Neuroscience.

[61]  J. Decety,et al.  The power of simulation: Imagining one's own and other's behavior , 2006, Brain Research.

[62]  Josef Perner,et al.  Do visual perspective tasks need theory of mind? , 2006, NeuroImage.

[63]  D. Rosenbaum.  Human movement initiation: specification of arm, direction, and extent. , 1980, Journal of experimental psychology. General.

[64]  G. Potts.  An ERP index of task relevance evaluation of visual stimuli , 2004, Brain and Cognition.

[65]  C. Delpuech,et al.  Subject's own name as a novel in a MMN design: A combined ERP and PET study , 2008, Brain Research.

[66]  K M Heilman,et al.  Left-hemisphere motor dominance in righthanders. , 1980, Cortex; a journal devoted to the study of the nervous system and behavior.

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

[68]  Hartmut Leuthold,et al.  Advance movement preparation of eye, foot, and hand: a comparative study using movement-related brain potentials. , 2002, Brain research. Cognitive brain research.

[69]  Wen-Jui Kuo,et al.  Action Co-representation is Tuned to Other Humans , 2008, Journal of Cognitive Neuroscience.

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

[71]  Rolf Ulrich,et al.  Preparing for Action: Inferences from CNV and LRP , 2004 .

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

[73]  Hugo D. Critchley,et al.  Brain activity relating to the contingent negative variation: an fMRI investigation , 2004, NeuroImage.

[74]  Günther Knoblich,et al.  The joint flanker effect: sharing tasks with real and imagined co-actors , 2011, Experimental Brain Research.

[75]  W. Prinz,et al.  Representing others' actions: just like one's own? , 2003, Cognition.

[76]  Cordula Vesper,et al.  A minimal architecture for joint action , 2010, Neural Networks.

[77]  J. Summers,et al.  The behavioural and electrophysiological effects of visual task difficulty and bimanual coordination mode during dual-task performance , 2009, Experimental Brain Research.

[78]  N. Sebanz,et al.  The GROOP effect: Groups mimic group actions , 2011, Cognition.

[79]  O. Blanke,et al.  The Out-of-Body Experience: Disturbed Self-Processing at the Temporo-Parietal Junction , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[80]  D. Rujescu,et al.  The neural basis of the P300 potential. Focus on the time-course of the underlying cortical generators. , 2004, European archives of psychiatry and clinical neuroscience.

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

[82]  Steven Laureys,et al.  Neural mechanisms involved in the detection of our first name: a combined ERPs and PET study , 2005, Neuropsychologia.

[83]  G. Fink,et al.  Neural correlates of the first-person-perspective , 2003, Trends in Cognitive Sciences.

[84]  J. Polich.  Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.