“Embodied Body Language”: an electrical neuroimaging study with emotional faces and bodies

To date, most investigations in the field of affective neuroscience mainly focused on the processing of facial expressions, overlooking the exploration of emotional body language (EBL), its capability to express our emotions notwithstanding. Few electrophysiological studies investigated the time course and the neural correlates of EBL and the integration of face and body emotion-related information. The aim of the present study was to investigate both the time course and the neural correlates underlying the integration of affective information conveyed by faces and bodies. We analysed EEG activities evoked during an expression matching task, requiring the judgment of emotional congruence between sequentially presented pairs of stimuli belonging to the same category (face-face or body-body), and between stimuli belonging to different categories (face-body or body-face). We focused on N400 time window and results showed that incongruent stimuli elicited a modulation of the N400 in all comparisons except for body-face condition. This modulation was mainly detected in the Middle Temporal Gyrus and within regions related to the mirror mechanism. More specifically, while the perception of incongruent facial expressions activates somatosensory-related representations, incongruent emotional body postures also require the activation of motor and premotor representations, suggesting a strict link between emotion and action.

[1]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. I. Method Descriptions and Simulations , 2004, Brain Topography.

[2]  Yue-jia Luo,et al.  Do Bodily Expressions Compete with Facial Expressions? Time Course of Integration of Emotional Signals from the Face and the Body , 2013, PloS one.

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

[4]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

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

[6]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[7]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. II. Demonstration of Sublobar Accuracy in Patients with Simultaneous Surface and Depth Recordings , 2004, Brain Topography.

[8]  V. Gallese.  The manifold nature of interpersonal relations: the quest for a common mechanism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

[10]  Phillip J Holcomb,et al.  Semantic integration in videos of real-world events: an electrophysiological investigation. , 2003, Psychophysiology.

[11]  R. Adolphs,et al.  A Role for Somatosensory Cortices in the Visual Recognition of Emotion as Revealed by Three-Dimensional Lesion Mapping , 2000, The Journal of Neuroscience.

[12]  Le Song,et al.  The ‘when’ and ‘where’ of perceiving signals of threat versus non-threat , 2006, NeuroImage.

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

[14]  Vincent M. Reid,et al.  N400 involvement in the processing of action sequences , 2008, Neuroscience Letters.

[15]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[16]  C. Keysers,et al.  Primary somatosensory contribution to action observation brain activity—combining fMRI and cTBS , 2016, Social cognitive and affective neuroscience.

[17]  M. Rugg,et al.  Event-related potentials and the semantic matching of faces , 1989, Neuropsychologia.

[18]  V. Gallese,et al.  Embodied Simulation: Beyond the Expression/Experience Dualism of Emotions , 2016, Trends in Cognitive Sciences.

[19]  Sönke Johannes,et al.  Brain potentials reveal the timing of face identity and expression judgments , 1998, Neuroscience Research.

[20]  J. Stekelenburg,et al.  The neural correlates of perceiving human bodies: an ERP study on the body-inversion effect , 2004, Neuroreport.

[21]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[22]  N. Hadjikhani,et al.  Fear fosters flight: a mechanism for fear contagion when perceiving emotion expressed by a whole body. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Proverbio,et al.  Comprehending Body Language and Mimics: An ERP and Neuroimaging Study on Italian Actors and Viewers , 2014, PloS one.

[24]  P. Downing,et al.  The neural basis of visual body perception , 2007, Nature Reviews Neuroscience.

[25]  R. Adorni,et al.  Who needs a referee? How incorrect basketball actions are automatically detected by basketball players' brain , 2012, Scientific Reports.

[26]  H. Meeren,et al.  Rapid perceptual integration of facial expression and emotional body language. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[27]  M. Rugg,et al.  Event-related potentials and the semantic matching of pictures , 1990, Brain and Cognition.

[28]  M. Iacoboni.  Neural mechanisms of imitation , 2005, Current Opinion in Neurobiology.

[29]  Ralph Adolphs,et al.  The neuropsychology of face perception: beyond simple dissociations and functional selectivity , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[30]  David I. Perrett,et al.  Event-related potentials and the matching of familiar and unfamiliar faces , 1988, Neuropsychologia.

[31]  A. Proverbio,et al.  When neurons do not mirror the agent's intentions: Sex differences in neural coding of goal-directed actions , 2010, Neuropsychologia.

[32]  Ellen F. Lau,et al.  A cortical network for semantics: (de)constructing the N400 , 2008, Nature Reviews Neuroscience.

[33]  M A Bobes,et al.  Different scalp topography of brain potentials related to expression and identity matching of faces. , 2000, Brain research. Cognitive brain research.

[34]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

[35]  N. Kanwisher,et al.  The Human Body , 2001 .

[36]  Alice Mado Proverbio,et al.  RP and N400 ERP components reflect semantic violations in visual processing of human actions , 2009, Neuroscience Letters.

[37]  B. Gelder,et al.  Clear signals or mixed messages: inter-individual emotion congruency modulates brain activity underlying affective body perception , 2016 .

[38]  Alison J. Wiggett,et al.  Functional MRI analysis of body and body part representations in the extrastriate and fusiform body areas. , 2007, Journal of neurophysiology.

[39]  Christian Keysers,et al.  Somatosensation in social perception , 2010, Nature Reviews Neuroscience.

[40]  J. Gentle,et al.  Randomization and Monte Carlo Methods in Biology. , 1990 .

[41]  Marco Tamietto,et al.  Standing up for the body. Recent progress in uncovering the networks involved in the perception of bodies and bodily expressions , 2010, Neuroscience & Biobehavioral Reviews.

[42]  G. Rizzolatti,et al.  A unifying view of the basis of social cognition , 2004, Trends in Cognitive Sciences.

[43]  B. Gelder,et al.  Why bodies? Twelve reasons for including bodily expressions in affective neuroscience , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  Alumit Ishai,et al.  Let’s face it: It’s a cortical network , 2008, NeuroImage.

[45]  S Sutton,et al.  ERP components in picture matching in children and adults. , 1988, Psychophysiology.

[46]  Alejandra Sel,et al.  The Emotional Homunculus: ERP Evidence for Independent Somatosensory Responses during Facial Emotional Processing , 2014, The Journal of Neuroscience.

[47]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[48]  P. Downing,et al.  Selectivity for the human body in the fusiform gyrus. , 2005, Journal of neurophysiology.

[49]  M. Gentilucci,et al.  Interaction Between Words and Symbolic Gestures as Revealed By N400 , 2014, Brain Topography.

[50]  Kara D. Federmeier,et al.  Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). , 2011, Annual review of psychology.

[51]  Michela Balconi,et al.  Face-selective processing and the effect of pleasant and unpleasant emotional expressions on ERP correlates. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[52]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

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

[54]  M. Kutas,et al.  Reading senseless sentences: brain potentials reflect semantic incongruity. , 1980, Science.

[55]  Martin Eimer,et al.  Facial identity and facial expression are initially integrated at visual perceptual stages of face processing , 2016, Neuropsychologia.

[56]  A. Ishai,et al.  Effective connectivity within the distributed cortical network for face perception. , 2007, Cerebral cortex.

[57]  B. Gelder.  Towards the neurobiology of emotional body language , 2006, Nature Reviews Neuroscience.

[58]  J. Haxby,et al.  Human neural systems for face recognition and social communication , 2002, Biological Psychiatry.

[59]  Christoph M. Michel,et al.  Spatiotemporal Analysis of Multichannel EEG: CARTOOL , 2011, Comput. Intell. Neurosci..