Undifferentiated facial electromyography responses to dynamic, audio-visual emotion displays in individuals with autism spectrum disorders.

We examined facial electromyography (fEMG) activity to dynamic, audio-visual emotional displays in individuals with autism spectrum disorders (ASD) and typically developing (TD) individuals. Participants viewed clips of happy, angry, and fearful displays that contained both facial expression and affective prosody while surface electrodes measured corrugator supercilli and zygomaticus major facial muscle activity. Across measures of average and peak activity, the TD group demonstrated emotion-selective fEMG responding, with greater relative activation of the zygomatic to happy stimuli and greater relative activation of the corrugator to fearful stimuli. In contrast, the ASD group largely showed no significant differences between zygomatic and corrugator activity across these emotions. There were no group differences in the magnitude and timing of fEMG response in the muscle congruent to the stimuli. This evidence that fEMG responses in ASD are undifferentiated with respect to the valence of the stimulus is discussed in light of potential underlying neurobiological mechanisms.

[1]  Ralph Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  D. McIntosh,et al.  Mimicry of Dynamic Emotional and Motor-Only Stimuli , 2011 .

[3]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[4]  J. Piven,et al.  Visual Scanning of Faces in Autism , 2002, Journal of autism and developmental disorders.

[5]  K. Loveland,et al.  Judgments of Auditory—Visual Affective Congruence in Adolescents with and without Autism: A Pilot Study of a New Task Using fMRI , 2008, Perceptual and motor skills.

[6]  R. Schultz,et al.  Superior temporal activation in response to dynamic audio-visual emotional cues , 2009, Brain and Cognition.

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

[8]  Jeff T. Larsen,et al.  Effects of positive and negative affect on electromyographic activity over zygomaticus major and corrugator supercilii. , 2003, Psychophysiology.

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

[10]  Á. Pascual-Leone,et al.  Impaired motor facilitation during action observation in individuals with autism spectrum disorder , 2005, Current Biology.

[11]  R. Adolphs,et al.  Visual emotion perception : mechanisms and processes , 2005 .

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

[13]  N. Minshew,et al.  A fine-grained analysis of facial expression processing in high-functioning adults with autism , 2007, Neuropsychologia.

[14]  D. McIntosh,et al.  Sponteous facial mimicry, liking and emotional contagion , 2006 .

[15]  A. Couteur,et al.  Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders , 1994, Journal of autism and developmental disorders.

[16]  B. Leventhal,et al.  The Autism Diagnostic Observation Schedule—Generic: A Standard Measure of Social and Communication Deficits Associated with the Spectrum of Autism , 2000, Journal of autism and developmental disorders.

[17]  P. Niedenthal,et al.  When did her smile drop? Facial mimicry and the influences of emotional state on the detection of change in emotional expression , 2001 .

[18]  T. Q. Irigaray,et al.  Intellectual abilities in Alzheimer's disease patients: Contributions from the Wechsler Abbreviated Scale of Intelligence (WASI) , 2010 .

[19]  F. Volkmar,et al.  Verbal bias in recognition of facial emotions in children with Asperger syndrome. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[20]  S Z Rapcsak,et al.  Fear recognition deficits after focal brain damage: a cautionary note. , 2000, Neurology.

[21]  D. McIntosh,et al.  More than mere mimicry? The influence of emotion on rapid facial reactions to faces. , 2007, Emotion.

[22]  M. Sigman,et al.  Understanding of simple and complex emotions in non-retarded children with autism. , 1992, Journal of child psychology and psychiatry, and allied disciplines.

[23]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[24]  G. McCarthy,et al.  Dynamic perception of facial affect and identity in the human brain. , 2003, Cerebral Cortex.

[25]  S. Folstein,et al.  Recognition and expression of emotional cues by autistic and normal adults. , 1989, Journal of child psychology and psychiatry, and allied disciplines.

[26]  D. McIntosh,et al.  Mimicry and Autism: Bases and Consequences of Rapid, Automatic Matching Behavior. , 2006 .

[27]  R. Hari,et al.  Abnormal imitation‐related cortical activation sequences in Asperger's syndrome , 2004, Annals of neurology.

[28]  Charles A. Nelson,et al.  Eye-Tracking, Autonomic, and Electrophysiological Correlates of Emotional Face Processing in Adolescents with Autism Spectrum Disorder , 2013, Journal of autism and developmental disorders.

[29]  Daniel N. McIntosh,et al.  Facial feedback hypotheses: Evidence, implications, and directions , 1996 .

[30]  W. Sato,et al.  The specific impairment of fearful expression recognition and its atypical development in pervasive developmental disorder , 2011, Social neuroscience.

[31]  L. Brosgole,et al.  Visual and auditory affect recognition in singly diagnosed mentally retarded patients, mentally retarded patients with autism and normal young children. , 1988, The International journal of neuroscience.

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

[33]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[34]  F. Volkmar,et al.  Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. , 2002, Archives of general psychiatry.

[35]  L. Wing,et al.  Severe impairments of social interaction and associated abnormalities in children: Epidemiology and classification , 1979, Journal of autism and developmental disorders.

[36]  L. Kanner Autistic disturbances of affective contact. , 1968, Acta paedopsychiatrica.

[37]  U. Dimberg,et al.  Facial electromyography and the experience of emotion. , 1988 .

[38]  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.

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

[40]  J. Cacioppo,et al.  Electromyographic activity over facial muscle regions can differentiate the valence and intensity of affective reactions. , 1986, Journal of personality and social psychology.

[41]  Kevin S LaBar,et al.  Development of emotional facial recognition in late childhood and adolescence. , 2007, Developmental science.

[42]  B. Scassellati,et al.  Limited activity monitoring in toddlers with autism spectrum disorder , 2011, Brain Research.

[43]  P. Bertelson,et al.  Multisensory integration, perception and ecological validity , 2003, Trends in Cognitive Sciences.

[44]  E. Bullmore,et al.  Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger Syndrome , 2007, Neuropsychologia.

[45]  F. Volkmar,et al.  Handbook of Autism and Pervasive Developmental Disorders , 1987 .

[46]  U. Dimberg,et al.  Facial reactions: Rapidly evoked emotional responses , 1997 .

[47]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[48]  E. Bullmore,et al.  Social intelligence in the normal and autistic brain: an fMRI study , 1999, The European journal of neuroscience.

[49]  D. Druckman,et al.  Socially induced affect , 1994 .

[50]  B. de Gelder,et al.  Facial electromyographic responses to emotional information from faces and voices in individuals with pervasive developmental disorder. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[51]  A. Lee,et al.  What's in a face? The case of autism. , 1988, British journal of psychology.

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

[53]  Livia Colle,et al.  Impaired recognition of negative basic emotions in autism: A test of the amygdala theory , 2006, Social neuroscience.

[54]  M. Hoffman,et al.  Interaction of affect and cognition in empathy. , 1985 .

[55]  Geraldine Dawson,et al.  Young children with autism show atypical brain responses to fearful versus neutral facial expressions of emotion. , 2004, Developmental science.

[56]  B. de Gelder,et al.  Atypical processing of fearful face-voice pairs in Pervasive Developmental Disorder: an ERP study. , 2008, Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology.

[57]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

[58]  Daniel Brandeis,et al.  Tuning of the visual word processing system: Distinct developmental ERP and fMRI effects , 2009, Human brain mapping.

[59]  P. Mundy,et al.  Facial expressions of affect in autistic, mentally retarded and normal children. , 1989, Journal of child psychology and psychiatry, and allied disciplines.

[60]  P. Niedenthal Embodying Emotion , 2007, Science.

[61]  H. Critchley,et al.  The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. , 2000, Brain : a journal of neurology.

[62]  C. Frith,et al.  Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. , 2002, Brain : a journal of neurology.

[63]  Catherine Lord,et al.  The Social Communication Questionnaire Manual , 2003 .

[64]  David Hartman Learning, Remembering, Believing: Enhancing Human Performance , 2010 .

[65]  G. Hall,et al.  Enhanced salience and emotion recognition in Autism: a PET study. , 2003, The American journal of psychiatry.

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

[67]  M. Bradley,et al.  Affective reactions to acoustic stimuli. , 2000, Psychophysiology.

[68]  A. Mayes,et al.  Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism , 2000, Neuroreport.

[69]  M. Bradley,et al.  Emotion and motivation. , 2007 .

[70]  E. Naito,et al.  Enhanced neural activity in response to dynamic facial expressions of emotion: an fMRI study. , 2004, Brain research. Cognitive brain research.

[71]  D. McIntosh,et al.  Rapid facial reactions to emotional facial expressions in typically developing children and children with autism spectrum disorder. , 2008, Journal of experimental child psychology.

[72]  Jennifer H. Pfeifer,et al.  Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders , 2006, Nature Neuroscience.

[73]  M. Bradley,et al.  Emotion and motivation I: defensive and appetitive reactions in picture processing. , 2001, Emotion.

[74]  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.

[75]  P. Putman,et al.  Reduced spontaneous facial mimicry in women with autistic traits , 2009, Biological Psychology.

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

[77]  Bruno Rossion,et al.  Developmental changes in face recognition during childhood : evidence from upright and inverted faces , 2012 .

[78]  J. Cacioppo,et al.  Emotional Contagion , 1993 .

[79]  U. Dimberg Facial reactions to facial expressions. , 1982, Psychophysiology.

[80]  K. Burton Habitual Emotion Regulation and the Facial Grimace , 2011, Psychological reports.

[81]  Gilles Pourtois,et al.  Simultaneous recording of EEG and facial muscle reactions during spontaneous emotional mimicry , 2008, Neuropsychologia.

[82]  Tristram H. Smith,et al.  A Review of Subtyping in Autism and Proposed Dimensional Classification Model , 2001, Journal of autism and developmental disorders.

[83]  R. Peter Hobson Autism and Emotion , 2005 .

[84]  A. Hamilton Emulation and Mimicry for Social Interaction: A Theoretical Approach to Imitation in Autism , 2008, Quarterly journal of experimental psychology.

[85]  G. McCarthy,et al.  Perception of dynamic changes in facial affect and identity in autism. , 2007, Social cognitive and affective neuroscience.

[86]  B. de Gelder,et al.  Similar facial electromyographic responses to faces, voices, and body expressions , 2007, Neuroreport.

[87]  D. Massaro,et al.  Perceiving affect from the voice and the face , 1996, Psychonomic bulletin & review.

[88]  T. Chartrand,et al.  The chameleon effect: the perception-behavior link and social interaction. , 1999, Journal of personality and social psychology.

[89]  V. Ramachandran,et al.  Face to face: Blocking facial mimicry can selectively impair recognition of emotional expressions , 2007, Social neuroscience.

[90]  J. Hietanen,et al.  Facial electromyographic responses to vocal affect expressions. , 1998, Psychophysiology.

[91]  J. Cacioppo,et al.  Specific forms of facial EMG response index emotions during an interview: from Darwin to the continuous flow hypothesis affect-laden information processing. , 1988, Journal of personality and social psychology.

[92]  A. Hamilton Goals, intentions and mental states: challenges for theories of autism. , 2009, Journal of child psychology and psychiatry, and allied disciplines.

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

[94]  Kim M. Dalton,et al.  Gaze fixation and the neural circuitry of face processing in autism , 2005, Nature Neuroscience.

[95]  J. Cacioppo,et al.  Mind at ease puts a smile on the face: psychophysiological evidence that processing facilitation elicits positive affect. , 2001, Journal of personality and social psychology.

[96]  R. Poldrack,et al.  Pediatric Functional Magnetic Resonance Imaging: Progress and Challenges , 2002, Topics in magnetic resonance imaging : TMRI.

[97]  V. Ramachandran,et al.  Paper Slow Echo: Facial Emg Evidence for the Delay of Spontaneous, but Not Voluntary, Emotional Mimicry in Children with Autism Spectrum Disorders , 2022 .

[98]  L. Rosén,et al.  Decoding of Emotion through Facial Expression, Prosody and Verbal Content in Children and Adolescents with Asperger’s Syndrome , 2006, Journal of autism and developmental disorders.