Modulation of the face- and body-selective visual regions by the motion and emotion of point-light face and body stimuli

Neural regions selective for facial or bodily form also respond to facial or bodily motion in highly form-degraded point-light displays. Yet it is unknown whether these face-selective and body-selective regions are sensitive to human motion regardless of stimulus type (faces and bodies) or to the specific motion-related cues characteristic of their proprietary stimulus categories. Using fMRI, we show that facial and bodily motions activate selectively those populations of neurons that code for the static structure of faces and bodies. Bodily (vs. facial) motion activated body-selective EBA bilaterally and right but not left FBA, irrespective of whether observers judged the emotion or color-change in point-light angry, happy and neutral stimuli. Facial (vs. bodily) motion activated face-selective right and left FFA, but only during emotion judgments for right FFA. Moreover, the strength of responses to point-light bodies vs. faces positively correlated with voxelwise selectivity for static bodies but not faces, whereas the strength of responses to point-light faces positively correlated with voxelwise selectivity for static faces but not bodies. Emotional content carried by point-light form-from-motion cues was sufficient to enhance the activity of several regions, including bilateral EBA and right FFA and FBA. However, although the strength of emotional modulation in right and left EBA by point-light body movements was related to the degree of voxelwise selectivity to static bodies but not static faces, there was no evidence that emotional modulation in fusiform cortex occurred in a similarly stimulus category-selective manner. This latter finding strongly constrains the claim that emotionally expressive movements modulate precisely those neuronal populations that code for the viewed stimulus category.

[1]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[2]  Christopher J. Fox,et al.  Defining the face processing network: Optimization of the functional localizer in fMRI , 2009, Human brain mapping.

[3]  A. Atkinson,et al.  Evidence for distinct contributions of form and motion information to the recognition of emotions from body gestures , 2007, Cognition.

[4]  Shigeru Akamatsu,et al.  Dynamic Properties Influence the Perception of Facial Expressions , 2001, Perception.

[5]  P. Downing,et al.  Within‐subject reproducibility of category‐specific visual activation with functional MRI , 2005, Human brain mapping.

[6]  H. Critchley,et al.  Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study , 2000, Human brain mapping.

[7]  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.

[8]  Hirokazu Doi,et al.  Role of Biological-Motion Information in Recognition of Facial Expressions by Young Children , 2008, Perception.

[9]  R. Blake,et al.  Perception of coherent motion, biological motion and form-from-motion under dim-light conditions , 1999, Vision Research.

[10]  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.

[11]  Alvaro Pascual-Leone,et al.  Growing up blind does not change the neural bases of Theory of Mind , 2009, Proceedings of the National Academy of Sciences.

[12]  G. Orban,et al.  Human Functional Magnetic Resonance Imaging Reveals Separation and Integration of Shape and Motion Cues in Biological Motion Processing , 2009, The Journal of Neuroscience.

[13]  Umberto Castiello,et al.  The human temporal lobe integrates facial form and motion: evidence from fMRI and ERP studies , 2003, NeuroImage.

[14]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

[15]  Sheng He,et al.  Cortical Responses to Invisible Faces: Dissociating Subsystems for Facial-Information Processing , 2006, Current Biology.

[16]  Swann Pichon,et al.  Similarities and differences in perceiving threat from dynamic faces and bodies. An fMRI study , 2011, NeuroImage.

[17]  F. Pollick,et al.  Recognising Facial Expression from Spatially and Temporally Modified Movements , 2003, Perception.

[18]  Jim M. Monti,et al.  Expectation and Surprise Determine Neural Population Responses in the Ventral Visual Stream , 2010, The Journal of Neuroscience.

[19]  R. J Dolan,et al.  Common and distinct neural responses during direct and incidental processing of multiple facial emotions , 2003, NeuroImage.

[20]  Alison J. Wiggett,et al.  Patterns of fMRI Activity Dissociate Overlapping Functional Brain Areas that Respond to Biological Motion , 2006, Neuron.

[21]  G. McCarthy,et al.  Dynamic perception of facial affect and identity in the human brain. , 2003, Cerebral Cortex.

[22]  J. Driver,et al.  Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[23]  Beatrice de Gelder,et al.  Neural Correlates of Perceiving Emotional Faces and Bodies in Developmental Prosopagnosia: An Event-Related fMRI-Study , 2008, PloS one.

[24]  J. N. Bassili Emotion recognition: the role of facial movement and the relative importance of upper and lower areas of the face. , 1979, Journal of personality and social psychology.

[25]  P. McGuire,et al.  Cortical substrates for the perception of face actions: an fMRI study of the specificity of activation for seen speech and for meaningless lower-face acts (gurning). , 2001, Brain research. Cognitive brain research.

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

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

[28]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[29]  Alison J. Wiggett,et al.  Behavioral / Systems / Cognitive Functional Magnetic Resonance Imaging Investigation of Overlapping Lateral Occipitotemporal Activations Using Multi-Voxel Pattern Analysis , 2006 .

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

[31]  Marc G. Berman,et al.  Evaluating functional localizers: The case of the FFA , 2010, NeuroImage.

[32]  G. Pourtois,et al.  Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging , 2007, Neuropsychologia.

[33]  G. Orban,et al.  Specificity of regions processing biological motion , 2005, The European journal of neuroscience.

[34]  M. Sereno,et al.  Point-Light Biological Motion Perception Activates Human Premotor Cortex , 2004, The Journal of Neuroscience.

[35]  Kenneth F. Valyear,et al.  The involvement of the “fusiform face area” in processing facial expression , 2005, Neuropsychologia.

[36]  Richard N. Henson,et al.  CHAPTER 15 – Efficient Experimental Design for fMRI , 2007 .

[37]  N. Sadato,et al.  Attention to emotion modulates fMRI activity in human right superior temporal sulcus. , 2001, Brain research. Cognitive brain research.

[38]  Leila Reddy,et al.  Top–down biases win against focal attention in the fusiform face area , 2007, NeuroImage.

[39]  G. Johansson Visual perception of biological motion and a model for its analysis , 1973 .

[40]  Béatrice de Gelder,et al.  Tease or threat? Judging social interactions from bodily expressions , 2010, NeuroImage.

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

[42]  Kenji Kawano,et al.  Global and fine information coded by single neurons in the temporal visual cortex , 1999, Nature.

[43]  N. Kanwisher,et al.  The Human Body , 2001 .

[44]  H. Wallbott Bodily expression of emotion , 1998 .

[45]  M. Lappe,et al.  Visual areas involved in the perception of human movement from dynamic form analysis , 2005, Neuroreport.

[46]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[47]  A. Johnston,et al.  Comparing Solid-Body with Point-Light Animations , 2003, Perception.

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

[49]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

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

[51]  Michael J. Brammer,et al.  A preferential increase in the extrastriate response to signals of danger , 2003, NeuroImage.

[52]  Raja Parasuraman,et al.  Object-Based Attentional Modulation of Biological Motion Processing: Spatiotemporal Dynamics Using Functional Magnetic Resonance Imaging and Electroencephalography , 2010, The Journal of Neuroscience.

[53]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[54]  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.

[55]  E. Vatikiotis-Bateson,et al.  Perceiving Biological Motion: Dissociating Visible Speech from Walking , 2003, Journal of Cognitive Neuroscience.

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

[57]  Randolph Blake,et al.  Learning to See Biological Motion: Brain Activity Parallels Behavior , 2004, Journal of Cognitive Neuroscience.

[58]  J. N. Bassili Facial motion in the perception of faces and of emotional expression. , 1978, Journal of experimental psychology. Human perception and performance.

[59]  J. A. Johnson,et al.  Point-light facial displays enhance comprehension of speech in noise. , 1996, Journal of speech and hearing research.

[60]  R. Blake,et al.  Perception of human motion. , 2007, Annual review of psychology.

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

[62]  Charan Ranganath,et al.  Category expectation modulates baseline and stimulus-evoked activity in human inferotemporal cortex , 2009, Brain Research.

[63]  R. Blake,et al.  Brain Areas Involved in Perception of Biological Motion , 2000, Journal of Cognitive Neuroscience.

[64]  P. Downing,et al.  Selectivity for the human body in the fusiform gyrus. , 2005, Journal of neurophysiology.

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

[66]  J. Schultz,et al.  Natural facial motion enhances cortical responses to faces , 2009, Experimental Brain Research.

[67]  Rebecca Saxe,et al.  Dissociation between emotion and personality judgments: Convergent evidence from functional neuroimaging , 2005, NeuroImage.

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

[69]  Rebecca F. Schwarzlose,et al.  Separate Face and Body Selectivity on the Fusiform Gyrus , 2005, The Journal of Neuroscience.

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