Decoding the difference between explicit and implicit body expression representation in high level visual, prefrontal and inferior parietal cortex

Recent studies provide an increasing understanding of how visual objects categories like faces or bodies are represented in the brain and also raised the question whether a category based or more dynamic network inspired models are more powerful. Two important and so far sidestepped issues in this debate are, first, how major category attributes like the emotional expression directly influence category representation and second, whether category and attribute representation are sensitive to task demands. This study investigated the impact of a crucial category attribute like emotional expression on category area activity and whether this varies with the participants’ task. Using (fMRI) we measured BOLD responses while participants viewed whole body expressions and performed either an explicit (emotion) or an implicit (shape) recognition task. Our results based on multivariate methods show that the type of task is the strongest determinant of brain activity and can be decoded in EBA, VLPFC and IPL. Brain activity was higher for the explicit task condition in VLPFC and was not emotion specific. This pattern suggests that during explicit recognition of the body expression, body category representation may be strengthened, and emotion and action related activity suppressed. Taken together these results stress the importance of the task and of the role of category attributes for understanding the functional organization of high level visual cortex.

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

[2]  B. de Gelder,et al.  Looking at the face and seeing the whole body. Neural basis of combined face and body expressions , 2017, Social cognitive and affective neuroscience.

[3]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[4]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

[5]  J. S. Guntupalli,et al.  Decoding neural representational spaces using multivariate pattern analysis. , 2014, Annual review of neuroscience.

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

[7]  B. de Gelder,et al.  The perception of emotion in body expressions. , 2015, Wiley interdisciplinary reviews. Cognitive science.

[8]  Yaroslav O. Halchenko,et al.  The Animacy Continuum in the Human Ventral Vision Pathway , 2015, Journal of Cognitive Neuroscience.

[9]  Marco Tamietto,et al.  Attention and awareness each influence amygdala activity for dynamic bodily expressions—a short review , 2012, Front. Integr. Neurosci..

[10]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[11]  Tom Michael Mitchell,et al.  Predicting Human Brain Activity Associated with the Meanings of Nouns , 2008, Science.

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

[13]  A. Sack,et al.  Dynamic Interactions between Emotion Perception and Action Preparation for Reacting to Social Threat: A Combined cTBS-fMRI Study , 2018, eNeuro.

[14]  N. Kanwisher Domain specificity in face perception , 2000, Nature Neuroscience.

[15]  Subjective understanding of actions and emotions requires interaction of the semantic and action observation networks , 2021 .

[16]  Steven P. Tipper,et al.  Implicitly Evoked Actions Modulate Visual Selection: Evidence from Parietal Extinction , 2005, Current Biology.

[17]  Radoslaw Martin Cichy,et al.  The representational dynamics of task and object processing in humans , 2018, eLife.

[18]  Alison J. Wiggett,et al.  Functional MRI analysis of body and body part representations in the extrastriate and fusiform body areas. , 2007, Journal of neurophysiology.

[19]  J. Tanji,et al.  Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties , 2007, Current Opinion in Neurobiology.

[20]  David J. Freedman,et al.  Task Dependence of Visual and Category Representations in Prefrontal and Inferior Temporal Cortices , 2014, The Journal of Neuroscience.

[21]  Ben M. Crittenden,et al.  Task Difficulty Manipulation Reveals Multiple Demand Activity but no Frontal Lobe Hierarchy , 2012, Cerebral cortex.

[22]  Dan J Stein,et al.  The Basolateral Amygdalae and Frontotemporal Network Functions for Threat Perception , 2017, eNeuro.

[23]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[24]  Talia Konkle,et al.  Large-scale dissociations between views of objects, scenes, and reachable-scale environments in visual cortex , 2020, Proceedings of the National Academy of Sciences.

[25]  B. de Gelder,et al.  Computation-Based Feature Representation of Body Expressions in the Human Brain. , 2020, Cerebral cortex.

[26]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  B. de Gelder,et al.  The role of computational and subjective features in emotional body expressions , 2020, Scientific Reports.

[28]  L. Carretié Exogenous (automatic) attention to emotional stimuli: a review , 2014, Cognitive, Affective, & Behavioral Neuroscience.

[29]  P. Downing,et al.  The neural basis of visual body perception , 2007, Nature Reviews Neuroscience.

[30]  Giancarlo Valente,et al.  The effect of spatial resolution on decoding accuracy in fMRI multivariate pattern analysis , 2016, NeuroImage.

[31]  Beatrice de Gelder,et al.  Emotional Voice and Emotional Body Postures Influence Each Other Independently of Visual Awareness , 2011, PloS one.

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

[33]  C. Cavina-Pratesi,et al.  Dissociable neural responses to hands and non-hand body parts in human left extrastriate visual cortex. , 2010, Journal of neurophysiology.

[34]  D. Javitt,et al.  Implicit emotion perception in schizophrenia. , 2015, Journal of psychiatric research.

[35]  Hervé Abdi,et al.  How the Human Brain Represents Perceived Dangerousness or “Predacity” of Animals , 2016, The Journal of Neuroscience.

[36]  Paddy Ross Body form and body motion processing are dissociable in the visual pathways , 2014, Front. Psychol..

[37]  Ivan Toni,et al.  The Extrastriate Body Area Computes Desired Goal States during Action Planning123 , 2016, eNeuro.

[38]  Alexander G. Huth,et al.  Attention During Natural Vision Warps Semantic Representation Across the Human Brain , 2013, Nature Neuroscience.

[39]  Lindsey J. Powell,et al.  My body or yours? The effect of visual perspective on cortical body representations. , 2006, Cerebral cortex.

[40]  A. Pinkham,et al.  Implicit and explicit processing of bodily emotions in schizophrenia , 2019, Cognitive neuropsychiatry.

[41]  Rainer Goebel,et al.  Personality traits predict brain activation and connectivity when witnessing a violent conflict , 2015, Scientific Reports.

[42]  John H. R. Maunsell,et al.  Hierarchical organization and functional streams in the visual cortex , 1983, Trends in Neurosciences.

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

[44]  Gian Luca Romani,et al.  Neural systems underlying observation of humanly impossible movements: an FMRI study. , 2005, Cerebral cortex.

[45]  D. Pandya,et al.  Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. , 2005, Cerebral cortex.

[46]  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.

[47]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[48]  Rainer Goebel,et al.  Fast Gaussian Naïve Bayes for searchlight classification analysis , 2017, NeuroImage.

[49]  Susan J. Lederman,et al.  Brain networks involved in haptic and visual identification of facial expressions of emotion: An fMRI study , 2010, NeuroImage.

[50]  Yaoda Xu,et al.  Task modulation of the 2-pathway characterization of occipitotemporal and posterior parietal visual object representations , 2019, Neuropsychologia.

[51]  Rainer Goebel,et al.  Ventral and Dorsal Pathways Relate Differently to Visual Awareness of Body Postures under Continuous Flash Suppression , 2018, eNeuro.

[52]  Thomas E. Nichols,et al.  A Bayesian Model of Category-Specific Emotional Brain Responses , 2015, PLoS Comput. Biol..

[53]  B. de Gelder,et al.  How white and black bodies are perceived depends on what emotion is expressed , 2017, Scientific Reports.

[54]  Daniel M Wegner,et al.  The neural substrates of action identification. , 2010, Social cognitive and affective neuroscience.

[55]  J. Duncan The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[56]  Nadim Joni Shah,et al.  Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques , 2011, NeuroImage.

[57]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[58]  D. Herr,et al.  Role of the Prefrontal Cortex in Pain Processing , 2018, Molecular Neurobiology.

[59]  B. de Gelder,et al.  Islamic Headdress Influences How Emotion is Recognized from the Eyes , 2012, Front. Psychology.

[60]  R. Goebel,et al.  The Constructive Nature of Affective Vision: Seeing Fearful Scenes Activates Extrastriate Body Area , 2012, PloS one.

[61]  Ewald Moser,et al.  Amygdala activation and facial expressions: Explicit emotion discrimination versus implicit emotion processing , 2007, Neuropsychologia.

[62]  Matthew D. Lieberman,et al.  Putting Feelings Into Words , 2007, Psychological science.

[63]  R. Goebel,et al.  Emotion unfolded by motion: a role for parietal lobe in decoding dynamic facial expressions. , 2013, Social cognitive and affective neuroscience.

[64]  B. Gelder,et al.  Unconscious fearful body perception enhances discrimination of conscious anger expressions under continuous flash suppression , 2019, Neuropsychologia.

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

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

[67]  Samuel A. Nastase,et al.  Attention Selectively Reshapes the Geometry of Distributed Semantic Representation , 2016, bioRxiv.

[68]  P. Downing,et al.  Category selectivity in human visual cortex: Beyond visual object recognition , 2017, Neuropsychologia.

[69]  Kalanit Grill-Spector,et al.  Not one extrastriate body area: Using anatomical landmarks, hMT+, and visual field maps to parcellate limb-selective activations in human lateral occipitotemporal cortex , 2011, NeuroImage.

[70]  Alison J. Wiggett,et al.  Surface-Based Information Mapping Reveals Crossmodal Vision–Action Representations in Human Parietal and Occipitotemporal Cortex , 2010, Journal of neurophysiology.

[71]  Tolga Çukur,et al.  Biased competition in semantic representation during natural visual search , 2019, NeuroImage.

[72]  Brittany G Travers,et al.  Neural substrates of interpreting actions and emotions from body postures. , 2012, Social cognitive and affective neuroscience.

[73]  R. Knight,et al.  Insights into Human Behavior from Lesions to the Prefrontal Cortex , 2014, Neuron.

[74]  Tessa R. Flack,et al.  Removing Hand Form Information Specifically Impairs Emotion Recognition for Fearful and Angry Body Stimuli , 2019, Perception.

[75]  Catherine R. G. Jones,et al.  Using Time Perception to Explore Implicit Sensitivity to Emotional Stimuli in Autism Spectrum Disorder , 2017, Journal of Autism and Developmental Disorders.

[76]  K. Roelofs,et al.  From face to hand: Attentional bias towards expressive hands in social anxiety , 2017, Biological Psychology.

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

[78]  Ivan Toni,et al.  Is the extrastriate body area part of the dorsal visuomotor stream? , 2017, Brain Structure and Function.

[79]  Richard J. Brown Neuropsychology Mental Structure , 1989 .

[80]  Nancy Kanwisher,et al.  The Quest for the FFA and Where It Led , 2017, The Journal of Neuroscience.

[81]  Beatrice de Gelder,et al.  The Bodily Expressive Action Stimulus Test (BEAST). Construction and Validation of a Stimulus Basis for Measuring Perception of Whole Body Expression of Emotions , 2011, Front. Psychology.

[82]  Patrik Vuilleumier,et al.  Effects of perceived mutual gaze and gender on face processing and recognition memory , 2005 .

[83]  M. Peelen,et al.  Supramodal Representations of Perceived Emotions in the Human Brain , 2010, The Journal of Neuroscience.

[84]  C. Freitag,et al.  Neural Correlates of Explicit Versus Implicit Facial Emotion Processing in ASD , 2017, Journal of autism and developmental disorders.

[85]  B. Gelder,et al.  A computational neuroethology perspective on body and expression perception , 2021, Trends in Cognitive Sciences.

[86]  Kalanit Grill-Spector,et al.  The improbable simplicity of the fusiform face area , 2012, Trends in Cognitive Sciences.

[87]  Richard F. Betzel,et al.  Network neuroscience and the connectomics revolution , 2020, Connectomic Deep Brain Stimulation.

[88]  Joseph E LeDoux,et al.  Viewpoints: Approaches to defining and investigating fear , 2019, Nature Neuroscience.

[89]  P. Downing,et al.  The role of occipitotemporal body-selective regions in person perception , 2011, Cognitive neuroscience.

[90]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[91]  Kalanit Grill-Spector,et al.  Task alters category representations in prefrontal but not high-level visual cortex , 2017, NeuroImage.

[92]  Li Fei-Fei,et al.  Neural mechanisms of rapid natural scene categorization in human visual cortex , 2009, Nature.

[93]  O. Blanke,et al.  The Insula Mediates Access to Awareness of Visual Stimuli Presented Synchronously to the Heartbeat , 2016, The Journal of Neuroscience.

[94]  Michael S. A. Graziano,et al.  The inferior parietal lobule and temporoparietal junction: A network perspective , 2017, Neuropsychologia.

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

[96]  N. Kanwisher,et al.  The fusiform face area: a cortical region specialized for the perception of faces , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[97]  J. S. Guntupalli,et al.  The Representation of Biological Classes in the Human Brain , 2012, The Journal of Neuroscience.

[98]  Christina F. Chick,et al.  Transcranial magnetic stimulation demonstrates a role for the ventrolateral prefrontal cortex in emotion perception , 2019, Psychiatry Research.

[99]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[100]  C. Urgesi,et al.  The Neural Basis of Body Form and Body Action Agnosia , 2008, Neuron.

[101]  Jack L. Gallant,et al.  A Continuous Semantic Space Describes the Representation of Thousands of Object and Action Categories across the Human Brain , 2012, Neuron.

[102]  Katiuscia Sacco,et al.  Once you feel it, you see it: Insula and sensory-motor contribution to visual awareness for fearful bodies in parietal neglect , 2015, Cortex.

[103]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Parietal Cortex and Comparison with Human and Macaque Resting-State Functional Connectivity , 2011, The Journal of Neuroscience.

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

[105]  B. de Gelder,et al.  Orienting to threat: faster localization of fearful facial expressions and body postures revealed by saccadic eye movements , 2009, Proceedings of the Royal Society B: Biological Sciences.

[106]  Swann Pichon,et al.  Threat prompts defensive brain responses independently of attentional control. , 2012, Cerebral cortex.

[107]  J. Duncan An adaptive coding model of neural function in prefrontal cortex , 2001 .

[108]  H. P. Op de Beeck,et al.  Task Context Overrules Object- and Category-Related Representational Content in the Human Parietal Cortex , 2017, Cerebral cortex.

[109]  P. Haggard,et al.  Constructing Visual Perception of Body Movement with the Motor Cortex , 2015, Cerebral cortex.

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

[111]  B. de Gelder,et al.  Perceiving emotions from bodily expressions and multisensory integration of emotion cues in schizophrenia , 2011, Social neuroscience.

[112]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.