A causal role of the right superior temporal sulcus in emotion recognition from biological motion

Understanding the emotions of others through nonverbal cues is critical for successful social interactions. The right posterior superior temporal sulcus (rpSTS) is one brain region thought to be key in the recognition of the mental states of others based on body language and facial expression. In the present study, we temporarily disrupted functional activity of the rpSTS by using continuous, theta-burst transcranial magnetic stimulation (cTBS) to test the hypothesis that the rpSTS plays a causal role in emotion recognition from body movements. Participants (N=23) received cTBS of the rpSTS, which was individually localized using fMRI, and a vertex control site. Before and after cTBS, we tested the ability of participants to identify emotions from point-light biological motion stimuli and a non-biological global motion identification task. Results revealed that the ability of participants to accurately identify emotional states from biological motion was reduced following cTBS stimulation to the rpSTS, but was unimpaired following vertex stimulation. Accuracy on the global motion tasks was unaffected by cTBS to either site. These results support the causal role of the rpSTS in decoding information about other’s emotional state from their body movements and gestures.

[1]  L. Janusik.  Profile of Nonverbal Sensitivity (PONS) , 2017 .

[2]  Malin Björnsdotter,et al.  Evaluation of Quantified Social Perception Circuit Activity as a Neurobiological Marker of Autism Spectrum Disorder. , 2016, JAMA psychiatry.

[3]  T. Flash,et al.  Brain activity correlates with emotional perception induced by dynamic avatars , 2015, NeuroImage.

[4]  M. Shadlen,et al.  Choice Certainty Is Informed by Both Evidence and Decision Time , 2014, Neuron.

[5]  James C. Thompson,et al.  Social-Network Complexity in Humans Is Associated With the Neural Response to Social Information , 2014, Psychological science.

[6]  Vincent Walsh,et al.  Combined TMS and fMRI Reveal Dissociable Cortical Pathways for Dynamic and Static Face Perception , 2014, Current Biology.

[7]  Joris Vangeneugden,et al.  Distinct Neural Mechanisms for Body Form and Body Motion Discriminations , 2014, The Journal of Neuroscience.

[8]  D. Ongur,et al.  Deficient biological motion perception in schizophrenia: results from a motion noise paradigm , 2013, Front. Psychol..

[9]  Andrew D. Engell,et al.  Probabilistic atlases for face and biological motion perception: An analysis of their reliability and overlap , 2013, NeuroImage.

[10]  M. Pavlova.  Biological motion processing as a hallmark of social cognition. , 2012, Cerebral cortex.

[11]  V. Walsh,et al.  Effects of TMS over Premotor and Superior Temporal Cortices on Biological Motion Perception , 2012, Journal of Cognitive Neuroscience.

[12]  H. Lau,et al.  Direct injection of noise to the visual cortex decreases accuracy but increases decision confidence. , 2012, Journal of neurophysiology.

[13]  Simon B Eickhoff,et al.  Brain regions involved in human movement perception: A quantitative voxel‐based meta‐analysis , 2012, Human brain mapping.

[14]  H. Lau,et al.  Attention induces conservative subjective biases in visual perception , 2011, Nature Neuroscience.

[15]  David Whitney,et al.  Neural correlates of coherent and biological motion perception in autism. , 2011, Developmental science.

[16]  Ralph-Axel Müller,et al.  Functional Differentiation of Posterior Superior Temporal Sulcus in Autism: A Functional Connectivity Magnetic Resonance Imaging Study , 2011, Biological Psychiatry.

[17]  Daniel D. Dilks,et al.  Differential selectivity for dynamic versus static information in face-selective cortical regions , 2011, NeuroImage.

[18]  R. Baayen,et al.  Mixed-effects modeling with crossed random effects for subjects and items , 2008 .

[19]  D. Pitcher,et al.  Transcranial Magnetic Stimulation Disrupts the Perception and Embodiment of Facial Expressions , 2008, The Journal of Neuroscience.

[20]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[21]  S. Reeves,et al.  Significant analgesic effects of one session of postoperative left prefrontal cortex repetitive transcranial magnetic stimulation: A replication study , 2008, Brain Stimulation.

[22]  A. Saygin.  Superior temporal and premotor brain areas necessary for biological motion perception. , 2007, Brain : a journal of neurology.

[23]  Y. Samson,et al.  Autism, the superior temporal sulcus and social perception , 2006, Trends in Neurosciences.

[24]  Á. Pascual-Leone,et al.  Repetitive TMS over posterior STS disrupts perception of biological motion , 2005, Vision Research.

[25]  Aina Puce,et al.  Configural Processing of Biological Motion in Human Superior Temporal Sulcus , 2005, The Journal of Neuroscience.

[26]  Randolph Blake,et al.  Impaired visual recognition of biological motion in schizophrenia , 2005, Schizophrenia Research.

[27]  J. Rothwell,et al.  Theta Burst Stimulation of the Human Motor Cortex , 2005, Neuron.

[28]  D. Perrett,et al.  A region of right posterior superior temporal sulcus responds to observed intentional actions , 2004, Neuropsychologia.

[29]  Kevin A. Pelphrey,et al.  Grasping the Intentions of Others: The Perceived Intentionality of an Action Influences Activity in the Superior Temporal Sulcus during Social Perception , 2004, Journal of Cognitive Neuroscience.

[30]  Tali Sharot,et al.  How emotion enhances the feeling of remembering , 2004, Nature Neuroscience.

[31]  A. Young,et al.  Emotion Perception from Dynamic and Static Body Expressions in Point-Light and Full-Light Displays , 2004, Perception.

[32]  N. Birbaumer,et al.  Dissociable cortical processing of recognizable and non-recognizable biological movement: analysing gamma MEG activity. , 2004, Cerebral cortex.

[33]  J. Haxby,et al.  fMRI Responses to Video and Point-Light Displays of Moving Humans and Manipulable Objects , 2003, Journal of Cognitive Neuroscience.

[34]  Hillary Anger Elfenbein,et al.  When familiarity breeds accuracy: cultural exposure and facial emotion recognition. , 2003, Journal of personality and social psychology.

[35]  Aina Puce,et al.  Electrophysiology and brain imaging of biological motion. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[36]  R. Blake,et al.  Brain Areas Active during Visual Perception of Biological Motion , 2002, Neuron.

[37]  A. O'Toole,et al.  Recognizing moving faces: a psychological and neural synthesis , 2002, Trends in Cognitive Sciences.

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

[39]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

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

[41]  T. Allison,et al.  Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. , 1999, Cerebral cortex.

[42]  T. Allison,et al.  Electrophysiological studies of human face perception. II: Response properties of face-specific potentials generated in occipitotemporal cortex. , 1999, Cerebral cortex.

[43]  T. Allison,et al.  Temporal Cortex Activation in Humans Viewing Eye and Mouth Movements , 1998, The Journal of Neuroscience.

[44]  Alan C. Evans,et al.  Specific Involvement of Human Parietal Systems and the Amygdala in the Perception of Biological Motion , 1996, The Journal of Neuroscience.

[45]  D Vickers,et al.  Effects of alternating set for speed or accuracy on response time, accuracy and confidence in a unidimensional discrimination task. , 1982, Acta psychologica.

[46]  Wayne A. Wickelgren,et al.  Speed-accuracy tradeoff and information processing dynamics , 1977 .

[47]  A. Mehrabian,et al.  Inference of attitudes from nonverbal communication in two channels. , 1967, Journal of consulting psychology.

[48]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[49]  R. Rosenthal.  MEASURING SENSITIVITY TO NONVERBAL COMMUNICATION: THE PONS TEST* , 1979 .