Early Preferential Responses to Fear Stimuli in Human Right Dorsal Visual Stream - A Meg Study

Emotional expressions of others are salient biological stimuli that automatically capture attention and prepare us for action. We investigated the early cortical dynamics of automatic visual discrimination of fearful body expressions by monitoring cortical activity using magnetoencephalography. We show that right parietal cortex distinguishes between fearful and neutral bodies as early as 80-ms after stimulus onset, providing the first evidence for a fast emotion-attention-action link through human dorsal visual stream.

[1]  Nouchine Hadjikhani,et al.  Non-conscious recognition of emotional body language , 2006, Neuroreport.

[2]  A. Milner,et al.  Is visual processing in the dorsal stream accessible to consciousness? , 2012, Proceedings of the Royal Society B: Biological Sciences.

[3]  Dottie M. Clower,et al.  The Inferior Parietal Lobule Is the Target of Output from the Superior Colliculus, Hippocampus, and Cerebellum , 2001, The Journal of Neuroscience.

[4]  Scott H. Johnson-Frey The neural bases of complex tool use in humans , 2004, Trends in Cognitive Sciences.

[5]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[6]  Jumpei Matsumoto,et al.  Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes , 2013, Proceedings of the National Academy of Sciences.

[7]  A. Sack,et al.  A causal role for inferior parietal lobule in emotion body perception , 2015, Cortex.

[8]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[9]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[10]  C. Gilbert,et al.  Cortical dynamics , 1997, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[11]  C. Darwin The Expression of the Emotions in Man and Animals , .

[12]  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.

[13]  A. Avenanti,et al.  Early changes in corticospinal excitability when seeing fearful body expressions , 2015, Scientific Reports.

[14]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[15]  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.

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

[17]  Swann Pichon,et al.  Two different faces of threat. Comparing the neural systems for recognizing fear and anger in dynamic body expressions , 2009, NeuroImage.

[18]  Quan Le Van Neurophysiological study for pulvinar role in rapid detection of snakes in monkeys , 2014 .

[19]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[20]  Martin A. Giese,et al.  Brain activity correlates with emotional perception induced by dynamic avatars , 2015, NeuroImage.

[21]  V. Gazzola,et al.  Seeing fearful body language rapidly freezes the observer's motor cortex , 2015, Cortex.

[22]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[23]  S. Sherlock,et al.  Anatomy and Function , 2001 .

[24]  Anders M. Dale,et al.  Dynamic Statistical Parametric Neurotechnique Mapping: Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000 .

[25]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[26]  V. Gallese The "Conscious" Dorsal Stream: Embodied Simulation and its Role in Space and Action Conscious Awareness , 2007 .

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

[28]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

[29]  Swann Pichon,et al.  Perceiving fear in dynamic body expressions , 2007, NeuroImage.

[30]  Christopher K. Kovach,et al.  Rapid Interactions between the Ventral Visual Stream and Emotion-Related Structures Rely on a Two-Pathway Architecture , 2008, The Journal of Neuroscience.

[31]  Fabricio Baglivo,et al.  Early detection of intentional harm in the human amygdala. , 2016, Brain : a journal of neurology.

[32]  R. Hari,et al.  Viewing Lip Forms Cortical Dynamics , 2002, Neuron.

[33]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[34]  Beatrice de Gelder,et al.  The Body as a Tool for Anger Awareness—Differential Effects of Angry Facial and Bodily Expressions on Suppression from Awareness , 2015, PloS one.

[35]  C. Darwin,et al.  The Expression of the Emotions in Man and Animals , 1956 .

[36]  M. Hämäläinen,et al.  Realistic conductivity geometry model of the human head for interpretation of neuromagnetic data , 1989, IEEE Transactions on Biomedical Engineering.

[37]  J. Mattingley,et al.  Fast and slow parietal pathways mediate spatial attention , 2004, Nature Neuroscience.

[38]  J. Culham,et al.  The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? , 2006, Neuropsychologia.

[39]  Martin E. Maier,et al.  Emotional and movement-related body postures modulate visual processing. , 2015, Social cognitive and affective neuroscience.

[40]  A. Dale,et al.  Distributed current estimates using cortical orientation constraints , 2006, Human brain mapping.

[41]  Rafael Malach,et al.  The emotion–action link? Naturalistic emotional stimuli preferentially activate the human dorsal visual stream , 2014, NeuroImage.

[42]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[43]  E. Làdavas,et al.  The effect of alexithymia on early visual processing of emotional body postures , 2016, Biological Psychology.

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

[45]  Elisabeth Pacherie,et al.  The Sense of Control and the Sense of Agency , 2007 .

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

[47]  B. de Gelder,et al.  Rapid detection of fear in body expressions, an ERP study , 2007, Brain Research.

[48]  Swann Pichon,et al.  Cortico-subcortical visual, somatosensory, and motor activations for perceiving dynamic whole-body emotional expressions with and without striate cortex (V1) , 2011, Proceedings of the National Academy of Sciences.