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 (pSTS) 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 right pSTS by using continuous, theta-burst transcranial magnetic stimulation (cTBS) to test the hypothesis that the right pSTS plays a causal role in emotion recognition from body movements. Participants (N = 23) received cTBS to the right pSTS, which was individually localized using fMRI, and a vertex control site. Before and after cTBS, we tested participants’ ability to identify emotions from point-light displays (PLDs) of biological motion stimuli and a nonbiological global motion identification task. Results revealed that accurate identification of emotional states from biological motion was reduced following cTBS to the right pSTS, but accuracy was not impaired following vertex stimulation. Accuracy on the global motion task was unaffected by cTBS to either site. These results support the causal role of the right pSTS in decoding information about others’ emotional state from their body movements and gestures.

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

[2]  Neil G. Muggleton,et al.  Effects of TMS over Premotor and Superior Temporal Cortices on Biological Motion Perception , 2012, Journal of Cognitive Neuroscience.

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

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

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

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

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

[8]  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.

[9]  Á. Pascual-Leone,et al.  A Review of Combined TMS-EEG Studies to Characterize Lasting Effects of Repetitive TMS and Assess Their Usefulness in Cognitive and Clinical Neuroscience , 2009, Brain Topography.

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

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

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

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

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

[15]  B. Bahrami,et al.  Neuroanatomical correlates of biological motion detection , 2013, Neuropsychologia.

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

[17]  Mikko Sams,et al.  Naturalistic fMRI Mapping Reveals Superior Temporal Sulcus as the Hub for the Distributed Brain Network for Social Perception , 2012, Front. Hum. Neurosci..

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

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

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

[21]  S. Swinnen,et al.  Underconnectivity of the superior temporal sulcus predicts emotion recognition deficits in autism. , 2014, Social cognitive and affective neuroscience.

[22]  B. Bahrami,et al.  Online social network size is reflected in human brain structure , 2011, Proceedings of the Royal Society B: Biological Sciences.

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

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

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

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

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

[28]  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.

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

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

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

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

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

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

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

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