Unseen facial and bodily expressions trigger fast emotional reactions

The spontaneous tendency to synchronize our facial expressions with those of others is often termed emotional contagion. It is unclear, however, whether emotional contagion depends on visual awareness of the eliciting stimulus and which processes underlie the unfolding of expressive reactions in the observer. It has been suggested either that emotional contagion is driven by motor imitation (i.e., mimicry), or that it is one observable aspect of the emotional state arising when we see the corresponding emotion in others. Emotional contagion reactions to different classes of consciously seen and “unseen” stimuli were compared by presenting pictures of facial or bodily expressions either to the intact or blind visual field of two patients with unilateral destruction of the visual cortex and ensuing phenomenal blindness. Facial reactions were recorded using electromyography, and arousal responses were measured with pupil dilatation. Passive exposure to unseen expressions evoked faster facial reactions and higher arousal compared with seen stimuli, therefore indicating that emotional contagion occurs also when the triggering stimulus cannot be consciously perceived because of cortical blindness. Furthermore, stimuli that are very different in their visual characteristics, such as facial and bodily gestures, induced highly similar expressive responses. This shows that the patients did not simply imitate the motor pattern observed in the stimuli, but resonated to their affective meaning. Emotional contagion thus represents an instance of truly affective reactions that may be mediated by visual pathways of old evolutionary origin bypassing cortical vision while still providing a cornerstone for emotion communication and affect sharing.

[1]  Gilles Pourtois,et al.  Affective blindsight: are we blindly led by emotions? Response to Heywood and Kentridge (2000) , 2000, Trends in Cognitive Sciences.

[2]  N. Frijda The laws of emotion. , 1988, The American psychologist.

[3]  Asaid Khateb,et al.  Discriminating emotional faces without primary visual cortices involves the right amygdala , 2005, Nature Neuroscience.

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

[5]  Béatrice de Gelder,et al.  Collicular Vision Guides Nonconscious Behavior , 2010, Journal of Cognitive Neuroscience.

[6]  L Weiskrantz,et al.  Non-conscious recognition of affect in the absence of striate cortex. , 1999, Neuroreport.

[7]  A. Meltzoff,et al.  Newborn infants imitate adult facial gestures. , 1983, Child development.

[8]  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.

[9]  L. Weiskrantz,et al.  Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. , 2001, Brain : a journal of neurology.

[10]  Gilles Pourtois,et al.  Fear recognition in the voice is modulated by unconsciously recognized facial expressions but not by unconsciously recognized affective pictures , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[11]  A. Damasio Descartes’ Error. Emotion, Reason and the Human Brain. New York (Grosset/Putnam) 1994. , 1994 .

[12]  Marco Tamietto,et al.  Affective blindsight in the intact brain: Neural interhemispheric summation for unseen fearful expressions , 2008, Neuropsychologia.

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

[14]  Martin Davies,et al.  Frontiers of Consciousness , 2008 .

[15]  H. Critchley,et al.  Pupillary contagion: central mechanisms engaged in sadness processing. , 2006, Social cognitive and affective neuroscience.

[16]  Béatrice de Gelder,et al.  Affective blindsight , 2007, Scholarpedia.

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

[18]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[20]  C. Frith,et al.  Modulation of the mirror system by social relevance. , 2006, Social cognitive and affective neuroscience.

[21]  Leslie G. Ungerleider,et al.  Visual awareness and the detection of fearful faces. , 2005, Emotion.

[22]  Arash Sahraie,et al.  Form discrimination in a case of blindsight , 2007, Neuropsychologia.

[23]  K. Berridge,et al.  Unconscious Emotion , 2004 .

[24]  Thomas E. Myers,et al.  Contagious yawning: the role of self-awareness and mental state attribution. , 2003, Brain research. Cognitive brain research.

[25]  J. Mattingley,et al.  The role of selective attention in matching observed and executed actions , 2009, Neuropsychologia.

[26]  J. Eccles The emotional brain. , 1980, Bulletin et memoires de l'Academie royale de medecine de Belgique.

[27]  Michela Romani,et al.  Motor facilitation during action observation: topographic mapping of the target muscle and influence of the onlooker's posture , 2006, The European journal of neuroscience.

[28]  M. Goodale,et al.  The use of visuomotor cues as a strategy for making perceptual judgments in a patient with visual form agnosia. , 1996 .

[29]  Béatrice de Gelder,et al.  Seeing Fearful Body Language Overcomes Attentional Deficits in Patients with Neglect , 2007, Journal of Cognitive Neuroscience.

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

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

[32]  A. Damasio Descartes' error: emotion, reason, and the human brain. avon books , 1994 .

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

[34]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  A. Cowey,et al.  Prime-sight in a blindsight subject , 2002, Nature Neuroscience.

[36]  M. Hyyppä Descartes' error. Emotion, reason and the human brain , 1996 .

[37]  R. Levenson Blood, Sweat, and Fears , 2003, Annals of the New York Academy of Sciences.

[38]  U. Dimberg Facial reactions to fear-relevant and fear-irrelevant stimuli , 1986, Biological Psychology.