Converging Evidence for the Advantage of Dynamic Facial Expressions

Neuroimaging evidence suggests that dynamic facial expressions elicit greater activity than static face stimuli in brain structures associated with social cognition, interpreted as greater ecological validity. However, a quantitative meta-analysis of brain activity associated with dynamic facial expressions is lacking. The current study investigated, using three fMRI experiments, activity elicited by (a) dynamic and static happy faces, (b) dynamic and static happy and angry faces, and (c) dynamic faces and dynamic flowers. In addition, using activation likelihood estimate (ALE) meta-analysis, we determined areas concordant across published studies that (a) used dynamic faces and (b) specifically compared dynamic and static emotional faces. The middle temporal gyri (Experiment 1) and superior temporal sulci (STS; Experiment 1 and 2) were more active for dynamic than static faces. In contrasts with the baseline the amygdalae were more active for dynamic faces (Experiment 1 and 2) and the fusiform gyri were active for all conditions (all Experiments). The ALE meta-analyses revealed concordant activation in all of these regions as well as in areas associated with cognitive manipulations (inferior frontal gyri). Converging data from the experiments and the meta-analyses suggest that dynamic facial stimuli elicit increased activity in regions associated with interpretation of social signals and emotional processing.

[1]  Beatriz Luna,et al.  Methodological approaches in developmental neuroimaging studies , 2010, Human brain mapping.

[2]  S. Baron-Cohen,et al.  Reading the Mind in the Voice: A Study with Normal Adults and Adults with Asperger Syndrome and High Functioning Autism , 2002, Journal of autism and developmental disorders.

[3]  E. Naito,et al.  Enhanced neural activity in response to dynamic facial expressions of emotion: an fMRI study. , 2004, Brain research. Cognitive brain research.

[4]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R. Adolphs.  Cognitive neuroscience: Cognitive neuroscience of human social behaviour , 2003, Nature Reviews Neuroscience.

[6]  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.

[7]  Nico H. Frijda,et al.  The understanding of facial expression of emotion. , 1953 .

[8]  K. Pelphrey,et al.  Friend or foe? Brain systems involved in the perception of dynamic signals of menacing and friendly social approaches , 2008, Social neuroscience.

[9]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[10]  G. Rhodes,et al.  Are you always on my mind? A review of how face perception and attention interact , 2007, Neuropsychologia.

[11]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[12]  Leslie G. Ungerleider.  Two cortical visual systems , 1982 .

[13]  Angela R. Laird,et al.  Lost in localization? The focus is meta-analysis , 2009, NeuroImage.

[14]  C. Deruelle,et al.  Motion and Emotion: A Novel Approach to the Study of Face Processing by Young Autistic Children , 2001, Journal of autism and developmental disorders.

[15]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[16]  Sakiko Yoshikawa,et al.  Enhanced perceptual, emotional, and motor processing in response to dynamic facial expressions of emotion1 , 2006 .

[17]  A. Gitter,et al.  Perception of Emotion: Differences in Mode of Presentation, Sex of Perceiver, and Race of Expressor. , 1968 .

[18]  William Davis Gaillard,et al.  Developmental Aspects of Pediatric fMRI: Considerations for Image Acquisition, Analysis, and Interpretation , 2001, NeuroImage.

[19]  Michael Petrides,et al.  Lateral frontal cortical contribution to memory , 1996 .

[20]  Jennifer C. Britton,et al.  Neural correlates of social and nonsocial emotions: An fMRI study , 2006, NeuroImage.

[21]  K. Scherer,et al.  Studying the dynamics of emotional expression using synthesized facial muscle movements. , 2000, Journal of personality and social psychology.

[22]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[24]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

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

[26]  J. Gabrieli,et al.  The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex , 2000, Psychobiology.

[27]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[28]  Margot J. Taylor,et al.  Neural correlates of personally familiar faces: Parents, partner and own faces , 2009, Human brain mapping.

[29]  D. V. van Essen,et al.  The contributions of prefrontal cortex and executive control to deception: evidence from activation likelihood estimate meta-analyses. , 2009, Cerebral cortex.

[30]  Lisa Feldman Barrett,et al.  Functional grouping and cortical–subcortical interactions in emotion: A meta-analysis of neuroimaging studies , 2008, NeuroImage.

[31]  Cezary Biele,et al.  Sex differences in perception of emotion intensity in dynamic and static facial expressions , 2006, Experimental Brain Research.

[32]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[33]  M. Herrmann,et al.  Emotions in motion: Dynamic compared to static facial expressions of disgust and happiness reveal more widespread emotion-specific activations , 2009, Brain Research.

[34]  R. Schultz,et al.  Superior temporal activation in response to dynamic audio-visual emotional cues , 2009, Brain and Cognition.

[35]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[36]  R. Adolphs.  Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[37]  Leslie G. Ungerleider,et al.  Visual Imagery of Famous Faces: Effects of Memory and Attention Revealed by fMRI , 2002, NeuroImage.

[38]  D. Maurer,et al.  Expert face processing requires visual input to the right hemisphere during infancy , 2003, Nature Neuroscience.

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

[40]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[41]  Frank E. Ritter,et al.  The Rise of Cognitive Architectures , 2007, Integrated Models of Cognitive Systems.

[42]  G. Rhodes,et al.  Configural Coding, Expertise, and the Right Hemisphere Advantage for Face Recognition , 1993, Brain and Cognition.

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

[44]  L. Uddin,et al.  Functional Brain Correlates of Social and Nonsocial Processes in Autism Spectrum Disorders: An Activation Likelihood Estimation Meta-Analysis , 2009, Biological Psychiatry.

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

[46]  G. McCarthy,et al.  Perception of dynamic changes in facial affect and identity in autism. , 2007, Social cognitive and affective neuroscience.

[47]  Deborah Giaschi,et al.  Combined Functional MRI and Diffusion Tensor Imaging Analysis of Visual Motion Pathways , 2009, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[48]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[49]  W. Sato,et al.  Brief Report: Representational Momentum for Dynamic Facial Expressions in Pervasive Developmental Disorder , 2010, Journal of autism and developmental disorders.

[50]  Zixiang Xiong,et al.  Lossy-to-lossless compression of medical volumetric data using three-dimensional integer wavelet transforms , 2003, IEEE Transactions on Medical Imaging.

[51]  J. Piven,et al.  Visual Scanning of Faces in Autism , 2002, Journal of autism and developmental disorders.

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

[53]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[54]  E. Adelson,et al.  The analysis of moving visual patterns , 1985 .

[55]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[56]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[57]  T. Paus,et al.  Brain networks involved in viewing angry hands or faces. , 2006, Cerebral cortex.

[58]  René Hurlemann,et al.  Segregating intra-amygdalar responses to dynamic facial emotion with cytoarchitectonic maximum probability maps , 2008, Journal of Neuroscience Methods.

[59]  Clinton D. Kilts,et al.  Dissociable Neural Pathways Are Involved in the Recognition of Emotion in Static and Dynamic Facial Expressions , 2003, NeuroImage.

[60]  Timothy J. Andrews,et al.  Neural responses to rigidly moving faces displaying shifts in social attention investigated with fMRI and MEG , 2010, Neuropsychologia.

[61]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[62]  E. Leibenluft,et al.  Mothers' neural activation in response to pictures of their children and other children , 2004, Biological Psychiatry.

[63]  Patrik Vuilleumier,et al.  Emotional facial expressions capture attention , 2001, Neurology.

[64]  T. Allison,et al.  Face-sensitive regions in human extrastriate cortex studied by functional MRI. , 1995, Journal of neurophysiology.

[65]  Jeremy M. Wolfe,et al.  Guided Search 4.0: Current Progress With a Model of Visual Search , 2007, Integrated Models of Cognitive Systems.

[66]  E. Bullmore,et al.  The anatomy of first-episode and chronic schizophrenia: an anatomical likelihood estimation meta-analysis. , 2008, The American journal of psychiatry.

[67]  A J Shinkfield,et al.  Recognition of facial emotional expressions from moving and static displays by individuals with mental retardation. , 1999, American journal of mental retardation : AJMR.

[68]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[69]  P. Ekman.  Pictures of Facial Affect , 1976 .

[70]  Danielle Ropar,et al.  Do the eyes have it? Inferring mental states from animated faces in autism. , 2007, Child development.