Simultaneous recording of EEG and facial muscle reactions during spontaneous emotional mimicry

The perception of emotional facial expressions induces covert imitation in emotion-specific muscles of the perceiver's face. Neural processes involved in these spontaneous facial reactions remain largely unknown. Here we concurrently recorded EEG and facial EMG in 15 participants watching short movie clips displaying either happy or angry facial expressions. EMG activity was recorded for the zygomaticus major (ZM) that elevates the lips during a smile, and the corrugator supercillii (CS) that knits the eyebrows during a frown. We found increased EMG activity of CS in response to angry expressions, and enhanced EMG activity of ZM for happy expressions, replicating earlier EMG studies. More importantly, we found that the amplitude of an early visual evoked potential (right P1) was larger when ZM activity to happy faces was high, and when CS activity to angry faces was high, as compared to when muscle reactions were low. Conversely, the amplitude of right N170 component was smaller when the intensity of facial imitation was high. These combined EEG-EMG results suggest that early visual processing of face expression may determine the magnitude of subsequent facial imitation, with dissociable effects for P1 and N170. These findings are discussed against the classical dual-route model of face recognition.

[1]  Paul Pauli,et al.  Electromyographic responses to static and dynamic avatar emotional facial expressions. , 2006, Psychophysiology.

[2]  U. Dimberg,et al.  Facial reactions to happy and angry facial expressions: evidence for right hemisphere dominance. , 2000, Psychophysiology.

[3]  D. Grandjean,et al.  Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: Time course and topographic evoked‐potentials mapping , 2005, Human brain mapping.

[4]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[5]  G. Mangun,et al.  Electrophysiological signs of sustained and transient attention to spatial locations , 1995, Neuropsychologia.

[6]  E. Koff,et al.  LATERALIZATION FOR FACIAL EMOTIONAL BEHAVIOR: A METHODOLOGICAL PERSPECTIVE* , 1990 .

[7]  A. Young,et al.  Understanding face recognition. , 1986, British journal of psychology.

[8]  U. Dimberg,et al.  Rapid facial reactions to emotional facial expressions. , 1998, Scandinavian journal of psychology.

[9]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[10]  Joseph E LeDoux.  Emotion Circuits in the Brain , 2000 .

[11]  L. Parr,et al.  Muscles of facial expression in the chimpanzee (Pan troglodytes): descriptive, comparative and phylogenetic contexts , 2006, Journal of anatomy.

[12]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[13]  C. Spielberger,et al.  STAI manual for the State-trait anxiety inventory ("self-evaluation questionnaire") , 1970 .

[14]  Margot J. Taylor,et al.  The development of emotional face processing during childhood. , 2006, Developmental science.

[15]  D I Perrett,et al.  Extracting Prototypical Facial Images from Exemplars , 1993, Perception.

[16]  T. Field,et al.  Discrimination and imitation of facial expression by neonates. , 1982, Science.

[17]  A. Boxtel,et al.  Optimal signal bandwidth for the recording of surface EMG activity of facial, jaw, oral, and neck muscles. , 2001 .

[18]  A. J. Fridlund,et al.  Guidelines for human electromyographic research. , 1986, Psychophysiology.

[19]  Jack van Honk,et al.  Testosterone administration reduces empathetic behavior: A facial mimicry study , 2006, Psychoneuroendocrinology.

[20]  Murray Alpert,et al.  Perceiver and poser asymmetries in processing facial emotion , 1990, Brain and Cognition.

[21]  U. Dimberg,et al.  Unconscious Facial Reactions to Emotional Facial Expressions , 2000, Psychological science.

[22]  Patrik Vuilleumier,et al.  Time course and specificity of event-related potentials to emotional expressions , 2004, Neuroreport.

[23]  W. Sato,et al.  Spontaneous facial mimicry in response to dynamic facial expressions , 2005, Cognition.

[24]  M. Eimer,et al.  An ERP study on the time course of emotional face processing , 2002, Neuroreport.

[25]  R A McCarthy,et al.  Prosopagnosia and structural encoding of faces: evidence from event-related potentials. , 1999, Neuroreport.

[26]  S. Vrana,et al.  Reactions to facial expressions: effects of social context and speech anxiety on responses to neutral, anger, and joy expressions , 2004, Biological Psychology.

[27]  P. Winkielman,et al.  When the social mirror breaks: deficits in automatic, but not voluntary, mimicry of emotional facial expressions in autism. , 2006, Developmental science.

[28]  M. Sonnby-Borgström.  Automatic mimicry reactions as related to differences in emotional empathy. , 2002, Scandinavian journal of psychology.

[29]  S. Hillyard,et al.  Involvement of striate and extrastriate visual cortical areas in spatial attention , 1999, Nature Neuroscience.

[30]  S. Baron-Cohen,et al.  The Empathy Quotient: An Investigation of Adults with Asperger Syndrome or High Functioning Autism, and Normal Sex Differences , 2004, Journal of autism and developmental disorders.

[31]  Robert Oostenveld,et al.  The five percent electrode system for high-resolution EEG and ERP measurements , 2001, Clinical Neurophysiology.

[32]  S. Luck,et al.  Visual event related potentials and attention , 1990 .

[33]  Renlai Zhou,et al.  Effects of Viewing Pleasant and Unpleasant Photographs on Facial EMG Asymmetry , 2004, Perceptual and motor skills.

[34]  M. Junghöfer,et al.  The facilitated processing of threatening faces: an ERP analysis. , 2004, Emotion.

[35]  L. Deouell,et al.  Cognitive Neuroscience: Selective visual streaming in face recognition: evidence from developmental prosopagnosia , 1999 .

[36]  L. Obler,et al.  Right hemisphere emotional perception: evidence across multiple channels. , 1998, Neuropsychology.

[37]  S. Luck,et al.  The role of attention in feature detection and conjunction discrimination: an electrophysiological analysis. , 1995, The International journal of neuroscience.

[38]  Carlo J. De Luca,et al.  The Use of Surface Electromyography in Biomechanics , 1997 .

[39]  P. Ellsworth,et al.  The role of facial response in the experience of emotion. , 1979, Journal of personality and social psychology.

[40]  K. Scherer,et al.  Studying the dynamics of emotional expression using synthesized facial muscle movements. , 2000, Journal of personality and social psychology.

[41]  Clara D. Martin,et al.  Controlling for interstimulus perceptual variance abolishes N170 face selectivity , 2007, Nature Neuroscience.

[42]  Peter Jönsson,et al.  Dismissing-avoidant pattern of attachment and mimicry reactions at different levels of information processing. , 2004, Scandinavian journal of psychology.

[43]  L. Parr,et al.  Emotional communication in primates: implications for neurobiology , 2005, Current Opinion in Neurobiology.

[44]  C. Brunia,et al.  Anticipatory EMG responses of pericranial muscles in relation to heart rate during a warned simple reaction time task. , 1996, Psychophysiology.

[45]  Ruud Zaalberg,et al.  Facial EMG responses to dynamic emotional facial expressions in boys with disruptive behavior disorders. , 2006, Journal of psychiatric research.

[46]  Margot J. Taylor,et al.  Early processing of the six basic facial emotional expressions. , 2003, Brain research. Cognitive brain research.

[47]  R. L. Hagen,et al.  Empathy: review of available measures , 1985 .

[48]  James L. Herrick,et al.  Cortical innervation of the facial nucleus in the non-human primate: a new interpretation of the effects of stroke and related subtotal brain trauma on the muscles of facial expression. , 2001, Brain : a journal of neurology.

[49]  A. Mehrabian,et al.  Emotional empathy and associated individual differences , 1988 .

[50]  Pierre Philippot,et al.  Facial Reactions to Emotional Facial Expressions: Affect or Cognition? , 1998 .

[51]  R. Soussignan,et al.  Facial and Autonomic Responses to Biological and Artificial Olfactory Stimuli in Human Neonates Re-Examining Early Hedonic Discrimination of Odors , 1997, Physiology & Behavior.

[52]  Klaus R. Scherer,et al.  Studying the dynamics of emotional expression using synthesized facial muscle movements. , 2000 .

[53]  A. van Boxtel,et al.  Amplitude and bilateral coherency of facial and jaw-elevator EMG activity as an index of effort during a two-choice serial reaction task. , 1993, Psychophysiology.

[54]  Joseph E LeDoux.  Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[55]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

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

[57]  U. Dimberg,et al.  Facial reactions to emotional stimuli: Automatically controlled emotional responses , 2002 .

[58]  P. Ekman.  Pictures of Facial Affect , 1976 .

[59]  R. Morecraft,et al.  The Motor Cortex and Facial Expression:: New Insights From Neuroscience , 2004, The neurologist.

[60]  P. Jönsson,et al.  Emotional Empathy as Related to Mimicry Reactions at Different Levels of Information Processing , 2003 .

[61]  S. Campanella,et al.  Categorical Perception of Happiness and Fear Facial Expressions: An ERP Study , 2002, Journal of Cognitive Neuroscience.

[62]  U. Hess,et al.  Facial mimicry and emotional contagion to dynamic emotional facial expressions and their influence on decoding accuracy. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.