Neural systems of visual attention responding to emotional gestures

Humans are the only species known to use symbolic gestures for communication. This affords a unique medium for nonverbal emotional communication with a distinct theoretical status compared to facial expressions and other biologically evolved nonverbal emotion signals. While a frown is a frown all around the world, the relation of emotional gestures to their referents is arbitrary and varies from culture to culture. The present studies examined whether such culturally based emotion displays guide visual attention processes. In two experiments, participants passively viewed symbolic hand gestures with positive, negative and neutral emotional meaning. In Experiment 1, functional magnetic resonance imaging (fMRI) measurements showed that gestures of insult and approval enhance activity in selected bilateral visual-associative brain regions devoted to object perception. In Experiment 2, dense sensor event-related brain potential recordings (ERP) revealed that emotional hand gestures are differentially processed already 150 ms poststimulus. Thus, the present studies provide converging neuroscientific evidence that emotional gestures provoke the cardinal signatures of selective visual attention regarding brain structures and temporal dynamics previously shown for emotional face and body expressions. It is concluded that emotionally charged gestures are efficient in shaping selective attention processes already at the level of stimulus perception.

[1]  Dieter Vaitl,et al.  Neuroimaging of emotion: empirical effects of proportional global signal scaling in fMRI data analysis , 2005, NeuroImage.

[2]  K. Vohs,et al.  Case Western Reserve University , 1990 .

[3]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[4]  N. Kanwisher,et al.  A Cortical Area Selective for Visual Processing of the Human Body , 2001, Science.

[5]  Patrik Vuilleumier,et al.  Emotional modulation of body-selective visual areas. , 2007, Social cognitive and affective neuroscience.

[6]  M. Bradley,et al.  Emotional perception: correlation of functional MRI and event-related potentials. , 2006, Cerebral cortex.

[7]  Olaf Hauk,et al.  Keep it simple: a case for using classical minimum norm estimation in the analysis of EEG and MEG data , 2004, NeuroImage.

[8]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[9]  M. Tomasello,et al.  The gestural communication of apes , 2007 .

[10]  J. Kissler,et al.  Event related potentials to emotional adjectives during reading. , 2008, Psychophysiology.

[11]  M. Bradley,et al.  Activation of the visual cortex in motivated attention. , 2003, Behavioral neuroscience.

[12]  Markus Junghöfer,et al.  The categorization of natural scenes: Brain attention networks revealed by dense sensor ERPs , 2006, NeuroImage.

[13]  R. Veit,et al.  Differential cerebral activation during observation of expressive gestures and motor acts , 2006, Neuropsychologia.

[14]  P. Boesiger,et al.  SENSE: Sensitivity encoding for fast MRI , 1999, Magnetic resonance in medicine.

[15]  Markus Junghöfer,et al.  Fleeting images: rapid affect discrimination in the visual cortex , 2006, Neuroreport.

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

[17]  R. Buck,et al.  Verbal and Nonverbal Communication: Distinguishing Symbolic, Spontaneous, and Pseudo-Spontaneous Nonverbal Behavior , 2002 .

[18]  S. Mineka,et al.  Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. , 2001, Psychological review.

[19]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[20]  Shelley E. Taylor,et al.  Asymmetrical effects of positive and negative events: the mobilization-minimization hypothesis. , 1991, Psychological bulletin.

[21]  Peter J. Lang,et al.  Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance , 2005, NeuroImage.

[22]  D. Tucker,et al.  Frontal evaluation and posterior representation in target detection. , 2001, Brain research. Cognitive brain research.

[23]  Angela D. Friederici,et al.  Cooperation of different neuronal systems during hand sign recognition , 2004, NeuroImage.

[24]  Harald T. Schupp,et al.  Emotional Facilitation of Sensory Processing in the Visual Cortex , 2003, Psychological science.

[25]  R. Adolphs.  Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[26]  M. Bradley,et al.  Emotion and motivation II: sex differences in picture processing. , 2001, Emotion.

[27]  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.

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

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

[30]  J. Kissler,et al.  Emotion and attention in visual word processing—An ERP study , 2009, Biological Psychology.

[31]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[32]  Sakiko Yoshikawa,et al.  Emotional expression boosts early visual processing of the face: ERP recording and its decomposition by independent component analysis , 2001, Neuroreport.

[33]  N. Hadjikhani,et al.  Seeing Fearful Body Expressions Activates the Fusiform Cortex and Amygdala , 2003, Current Biology.

[34]  B. Rockstroh,et al.  Statistical control of artifacts in dense array EEG/MEG studies. , 2000, Psychophysiology.

[35]  L. Nadel,et al.  Cognitive neuroscience of emotion , 2000 .

[36]  Michèle Fabre-Thorpe,et al.  Interaction of top-down and bottom-up processing in the fast visual analysis of natural scenes. , 2004, Brain research. Cognitive brain research.

[37]  J. Decety,et al.  The effects of learning and intention on the neural network involved in the perception of meaningless actions. , 1999, Brain : a journal of neurology.

[38]  Dean Sabatinelli,et al.  Affective picture perception: gender differences in visual cortex? , 2004, Neuroreport.

[39]  D. Lundqvist,et al.  Unconscious emotion : Evolutionary perspectives, psychophysiological data, and neuropsychological mechanisms , 2000 .

[40]  Dane Archer,et al.  Unspoken Diversity: Cultural Differences in Gestures , 1997 .

[41]  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.

[42]  Wendy Heller,et al.  Visual processing of facial affect , 2003, Neuroreport.

[43]  C. Frith,et al.  Dissociable neural pathways for the perception and recognition of expressive and instrumental gestures , 2004, Neuropsychologia.

[44]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[45]  Markus Junghöfer,et al.  Selective Visual Attention to Emotion , 2007, The Journal of Neuroscience.

[46]  M. Bradley,et al.  Motivated attention: Affect, activation, and action. , 1997 .

[47]  D. Morris.  Gestures, Their Origins and Distribution. , 1979 .

[48]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[49]  K. Grill-Spector,et al.  The human visual cortex. , 2004, Annual review of neuroscience.

[50]  M. Bradley,et al.  Fleeting images: a new look at early emotion discrimination. , 2001, Psychophysiology.

[51]  Markus Junghöfer,et al.  Stimulus novelty and emotion perception: the near absence of habituation in the visual cortex , 2006, Neuroreport.

[52]  Jari K. Hietanen,et al.  Differential electrocortical responses to increasing intensities of fearful and happy emotional expressions , 2007, Brain Research.

[53]  J. Kissler,et al.  Buzzwords , 2007, Psychological science.

[54]  Markus Junghöfer,et al.  Rapid picture processing: affective primes and targets. , 2007, Psychophysiology.