Electrophysiological signatures of intentional social coordination in the 10–12Hz range

This study sought to investigate the effects of manipulating social coordination on brain synchronization/de-synchronization in the mu band. Mu activation is associated with understanding and coordinating motor acts and may play a key role in mediating social interaction. Members of a dyad were required to interact with one another in a rhythmic finger movement coordination task under various instructions: intrinsic where each member of the dyad was instructed to maintain their own and ignore their partner's movement; in-phase where they were asked to synchronize with their partner's movement; and anti-phase where they were instructed to syncopate with their partner's movement. EEG and movement data were recorded simultaneously from both subjects during all three tasks and a control condition. Log power ratios of EEG activity in the active conditions versus control were used to assess the effect of task context on synchronization/de-synchronization in the mu spectral domain. Results showed clear and systematic modulation of mu band activity in the 10-12 Hz range as a function of coordination context. In the left hemisphere general levels of alpha-mu suppression increased progressively as one moved from intrinsic through in-phase to anti-phase contexts but with no specific central-parietal focus. In contrast the right hemisphere displayed context-specific changes in the central-parietal region. The intrinsic condition showed a right synchronization which disappeared with the in-phase context even as de-synchronization remained greater in the left hemisphere. Anti-phase was associated with larger mu suppression in the right in comparison with left at central-parietal region. Such asymmetrical changes were highly correlated with changing behavioral dynamics. These specific patterns of activation and deactivation of mu activity suggest that localized neural circuitry in right central-parietal regions mediates how individuals interpret the movements of others in the context of their own actions. A right sided mechanism in the 10-12 Hz range appears to be involved in integrating the mutual information among the members of a dyad that enables the dynamics of social interaction to unfold in time.

[1]  Chen Li,et al.  Motor and Nonmotor Domains in the Monkey Dentate , 2002, Annals of the New York Academy of Sciences.

[2]  K. Dujardin,et al.  Event-related desynchronization (ERD) patterns during memory processes: effects of aging and task difficulty. , 1995, Electroencephalography and clinical neurophysiology.

[3]  Blake W. Johnson,et al.  Mu rhythm modulation during observation of an object-directed grasp. , 2004, Brain research. Cognitive brain research.

[4]  V. Ramachandran,et al.  The human mirror neuron system: a link between action observation and social skills. , 2007, Social cognitive and affective neuroscience.

[5]  H. Brownell,et al.  Acquired `theory of mind' impairments following stroke , 1999, Cognition.

[6]  G. Pfurtscheller,et al.  Topographical display and interpretation of event-related desynchronization during a visual-verbal task , 2005, Brain Topography.

[7]  S. Cochin,et al.  Perception of motion and qEEG activity in human adults. , 1998, Electroencephalography and clinical neurophysiology.

[8]  J. Kelso,et al.  Toward a theory of apractic syndromes , 1981, Brain and Language.

[9]  J. Pineda,et al.  Recognition of point-light biological motion: Mu rhythms and mirror neuron activity , 2007, Behavioural Brain Research.

[10]  J. Kelso,et al.  The Complementary Nature , 2006 .

[11]  Febo Cincotti,et al.  Human Cortical Electroencephalography (EEG) Rhythms during the Observation of Simple Aimless Movements: A High-Resolution EEG Study , 2002, NeuroImage.

[12]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[13]  Bin He,et al.  Electrophysiological neuroimaging: Cortical correlates of alpha rhythm modulation , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[14]  M. Brass,et al.  The inhibition of imitative and overlearned responses: a functional double dissociation , 2005, Neuropsychologia.

[15]  Joseph P. McCleery,et al.  EEG evidence for mirror neuron dysfunction in autism spectrum disorders. , 2005, Brain research. Cognitive brain research.

[16]  Daniel M. Wolpert,et al.  Where does your own action influence your perception of another person's action in the brain? , 2006, NeuroImage.

[17]  S. Muthukumaraswamy,et al.  Modulation of the human mirror neuron system during cognitive activity. , 2008, Psychophysiology.

[18]  V. Ramachandran,et al.  The simulating social mind: the role of the mirror neuron system and simulation in the social and communicative deficits of autism spectrum disorders. , 2007, Psychological bulletin.

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

[20]  L. Oberman,et al.  What goads cigarette smokers to smoke? Neural adaptation and the mirror neuron system , 2006, Brain Research.

[21]  G. Rizzolatti,et al.  Action for perception: a motor-visual attentional effect. , 1999 .

[22]  Natalie Sebanz,et al.  Prediction in Joint Action: What, When, and Where , 2009, Top. Cogn. Sci..

[23]  J. Decety,et al.  Gender Differences in the Mu Rhythm of the Human Mirror-Neuron System , 2008, PloS one.

[24]  Y. Paulignan,et al.  An Interference Effect of Observed Biological Movement on Action , 2003, Current Biology.

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

[26]  Ettore Lettich,et al.  Ten Percent Electrode System for Topographic Studies of Spontaneous and Evoked EEG Activities , 1985 .

[27]  Naznin Virji-Babul,et al.  Changes in mu rhythm during action observation and execution in adults with Down syndrome: Implications for action representation , 2008, Neuroscience Letters.

[28]  Mark Mühlau,et al.  Left inferior parietal dominance in gesture imitation: an fMRI study , 2005, Neuropsychologia.

[29]  A. Fuchs,et al.  Coordination: Neural, Behavioral and Social Dynamics , 2008 .

[30]  R. Hari,et al.  The brain in time: insights from neuromagnetic recordings , 2010, Annals of the New York Academy of Sciences.

[31]  Walter Wg,et al.  The electrical activity of the brain. , 1949 .

[32]  Margot J. Taylor,et al.  Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. , 2000, Psychophysiology.

[33]  S-J Blakemore,et al.  Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. , 2005, Brain : a journal of neurology.

[34]  W. Klimesch.  Memory processes, brain oscillations and EEG synchronization. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  H. Gastaut,et al.  EEG changes during cinematographic presentation; moving picture activation of the EEG. , 1954, Electroencephalography and clinical neurophysiology.

[36]  R P Lesser,et al.  Functional significance of the mu rhythm of human cortex: an electrophysiologic study with subdural electrodes. , 1993, Electroencephalography and clinical neurophysiology.

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

[38]  A. Opstal.  Dynamic Patterns: The Self-Organization of Brain and Behavior , 1995 .

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

[40]  W. Klimesch,et al.  Event-related phase reorganization may explain evoked neural dynamics , 2007, Neuroscience & Biobehavioral Reviews.

[41]  J. Pineda.  The functional significance of mu rhythms: Translating “seeing” and “hearing” into “doing” , 2005, Brain Research Reviews.

[42]  J. Pineda,et al.  Mirroring and mu rhythm involvement in social cognition: Are there dissociable subcomponents of theory of mind? , 2009, Biological Psychology.

[43]  S. Bentin,et al.  Mirror activity in the human brain while observing hand movements: A comparison between EEG desynchronization in the μ-range and previous fMRI results , 2009, Brain Research.

[44]  M. Tomasello,et al.  Understanding and sharing intentions: The origins of cultural cognition , 2005, Behavioral and Brain Sciences.

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

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

[47]  Fred L. Steinberg,et al.  Cortical and subcortical networks underlying syncopated and synchronized coordination revealed using fMRI , 2002 .

[48]  J. A. Scott Kelso,et al.  Coordination Dynamics of Large-scale Neural Circuitry Underlying Rhythmic Sensorimotor Behavior , 2009, Journal of Cognitive Neuroscience.

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

[50]  G. Rizzolatti,et al.  Action for perception: a motor-visual attentional effect. , 1999, Journal of experimental psychology. Human perception and performance.

[51]  A. Meltzoff,et al.  Explaining Facial Imitation: A Theoretical Model. , 1997, Early development & parenting.

[52]  J. Kelso,et al.  Attentional demands reflect learning‐induced alterations of bimanual coordination dynamics , 2002, The European journal of neuroscience.

[53]  J. Kelso,et al.  Social coordination dynamics: Measuring human bonding , 2008, Social neuroscience.

[54]  F. Lacquaniti,et al.  Representing spatial information for limb movement: role of area 5 in the monkey. , 1995, Cerebral cortex.

[55]  V B Mountcastle,et al.  The view from within: pathways to the study of perception. , 1975, The Johns Hopkins medical journal.

[56]  Line Garnero,et al.  Inter-Brain Synchronization during Social Interaction , 2010, PloS one.

[57]  J. W. Kuhlman,et al.  Functional topography of the human mu rhythm. , 1978, Electroencephalography and clinical neurophysiology.

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

[59]  E. Procyk,et al.  Brain activity during observation of actions. Influence of action content and subject's strategy. , 1997, Brain : a journal of neurology.

[60]  G Pfurtscheller,et al.  Computational model of thalamo-cortical networks: dynamical control of alpha rhythms in relation to focal attention. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[61]  A. Fuchs,et al.  Cortical and subcortical networks underlying syncopated and synchronized coordination revealed using fMRI. Functional magnetic resonance imaging. , 2002, Human brain mapping.

[62]  G. Rizzolatti,et al.  Resonance behaviors and mirror neurons. , 1999, Archives italiennes de biologie.

[63]  A. Fuchs,et al.  A phase transition in human brain and behavior , 1992 .

[64]  Olivier Oullier,et al.  Social Coordination, from the Perspective of Coordination Dynamics , 2009, Encyclopedia of Complexity and Systems Science.

[65]  W J Ray,et al.  EEG activity during cognitive processing: influence of attentional factors. , 1985, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[67]  G. Ermentrout.  Dynamic patterns: The self-organization of brain and behavior , 1997 .

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

[69]  J. Decety,et al.  Top down effect of strategy on the perception of human biological motion: a pet investigation. , 1998, Cognitive neuropsychology.

[70]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

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

[72]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[73]  Febo Cincotti,et al.  Human Movement-Related Potentials vs Desynchronization of EEG Alpha Rhythm: A High-Resolution EEG Study , 1999, NeuroImage.

[74]  Michael J. Richardson,et al.  Dynamics of Interpersonal Coordination , 2008 .

[75]  A. Fuchs,et al.  Event‐related changes in neuromagnetic activity associated with syncopation and synchronization timing tasks , 2001, Human brain mapping.

[76]  Patrick Haggard,et al.  Somatosensory effects of action inhibition: a study with the stop-signal paradigm , 2010, Experimental Brain Research.

[77]  J. Kelso,et al.  From the Cover : The phi complex as a neuromarker of human social coordination , 2007 .

[78]  T. Pedley,et al.  Beta and Mu Rhythms , 1990, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[79]  Silvia Comani,et al.  Striatal Activity during Intentional Switching Depends on Pattern Stability , 2010, The Journal of Neuroscience.