Modulation of Perception and Brain Activity by Predictable Trajectories of Facial Expressions

People track facial expression dynamics with ease to accurately perceive distinct emotions. Although the superior temporal sulcus (STS) appears to possess mechanisms for perceiving changeable facial attributes such as expressions, the nature of the underlying neural computations is not known. Motivated by novel theoretical accounts, we hypothesized that visual and motor areas represent expressions as anticipated motion trajectories. Using magnetoencephalography, we show predictable transitions between fearful and neutral expressions (compared with scrambled and static presentations) heighten activity in visual cortex as quickly as 165 ms poststimulus onset and later (237 ms) engage fusiform gyrus, STS and premotor areas. Consistent with proposed models of biological motion representation, we suggest that visual areas predictively represent coherent facial trajectories. We show that such representations bias emotion perception of subsequent static faces, suggesting that facial movements elicit predictions that bias perception. Our findings reveal critical processes evoked in the perception of dynamic stimuli such as facial expressions, which can endow perception with temporal continuity.

[1]  Claus Bundesen,et al.  Images of Illusory Motion in Primary Visual Cortex , 2006, Journal of Cognitive Neuroscience.

[2]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

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

[4]  T. Hubbard Representational momentum and related displacements in spatial memory: A review of the findings , 2005, Psychonomic bulletin & review.

[5]  Lars Muckli,et al.  Primary Visual Cortex Activity along the Apparent-Motion Trace Reflects Illusory Perception , 2005, PLoS biology.

[6]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

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

[8]  N. Kanwisher,et al.  Stages of processing in face perception: an MEG study , 2002, Nature Neuroscience.

[9]  Geraint Rees,et al.  Primary visual cortex activation on the path of apparent motion is mediated by feedback from hMT+/V5 , 2006, NeuroImage.

[10]  D. Heeger,et al.  A Hierarchy of Temporal Receptive Windows in Human Cortex , 2008, The Journal of Neuroscience.

[11]  Karl J. Friston,et al.  DEM: A variational treatment of dynamic systems , 2008, NeuroImage.

[12]  T. Poggio,et al.  Cognitive neuroscience: Neural mechanisms for the recognition of biological movements , 2003, Nature Reviews Neuroscience.

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

[14]  J. Bharucha,et al.  Judged displacement in apparent vertical and horizontal motion , 1988, Perception & psychophysics.

[15]  Karl J. Friston,et al.  Canonical Source Reconstruction for MEG , 2007, Comput. Intell. Neurosci..

[16]  Martin A. Giese,et al.  Predicting point-light actions in real-time , 2010 .

[17]  V. S. Ramachandran,et al.  Extrapolation of motion path in human visual perception , 1983, Vision Research.

[18]  W. Sato,et al.  Dynamic facial expressions of emotion induce representational momentum , 2008, Cognitive, affective & behavioral neuroscience.

[19]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[20]  Karl J. Friston,et al.  Population-level inferences for distributed MEG source localization under multiple constraints: Application to face-evoked fields , 2007, NeuroImage.

[21]  Timothy J. Andrews,et al.  Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe , 2004, NeuroImage.

[22]  Pierre Rainville,et al.  Brain responses to dynamic facial expressions of pain , 2006, Pain.

[23]  M. Jeannerod Neural Simulation of Action: A Unifying Mechanism for Motor Cognition , 2001, NeuroImage.

[24]  M. Webster,et al.  Adaptation to natural facial categories , 2002 .

[25]  C. Keysers,et al.  Towards a unifying neural theory of social cognition. , 2006, Progress in brain research.

[26]  Paul Schrater,et al.  Shape perception reduces activity in human primary visual cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[27]  G. Aschersleben,et al.  The Theory of Event Coding (TEC): a framework for perception and action planning. , 2001, The Behavioral and brain sciences.

[28]  Ian M. Thornton,et al.  Representational momentum: New findings, new directions , 2002 .

[29]  S. Hurley The shared circuits model (SCM): how control, mirroring, and simulation can enable imitation, deliberation, and mindreading. , 2008, The Behavioral and brain sciences.

[30]  A. Young,et al.  Understanding the recognition of facial identity and facial expression , 2005, Nature Reviews Neuroscience.

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

[32]  Karl J. Friston,et al.  MEG source localization under multiple constraints: An extended Bayesian framework , 2006, NeuroImage.

[33]  Karl Verfaillie,et al.  Representing and anticipating human actions in vision , 2002 .

[34]  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.

[35]  Talma Hendler,et al.  Neural representations of kinematic laws of motion: Evidence for action-perception coupling , 2007, Proceedings of the National Academy of Sciences.

[36]  A. Treves Computational constraints between retrieving the past and predicting the future, and the CA3‐CA1 differentiation , 2004, Hippocampus.

[37]  V. Gallese Before and below ‘theory of mind’: embodied simulation and the neural correlates of social cognition , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[38]  Karl J. Friston,et al.  A Hierarchy of Time-Scales and the Brain , 2008, PLoS Comput. Biol..

[39]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

[40]  Karl J. Friston,et al.  Predictive coding: an account of the mirror neuron system , 2007, Cognitive Processing.

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

[42]  Karl J. Friston,et al.  Experience-dependent coding of facial expression in superior temporal sulcus , 2007, Proceedings of the National Academy of Sciences.

[43]  James V. Haxby,et al.  Mirror Neuron System Differentially Activated by Facial Expressions and Social Hand Gestures: A Functional Magnetic Resonance Imaging Study , 2008, Journal of Cognitive Neuroscience.

[44]  Karl J. Friston,et al.  Bayesian inversion of EEG models , 2007 .

[45]  Michael J. Constantino,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008 .

[46]  C. Keysers,et al.  Facial expressions: What the mirror neuron system can and cannot tell us , 2007, Social neuroscience.

[47]  Dana H. Ballard,et al.  Learning receptive fields using predictive feedback , 2006, Journal of Physiology-Paris.

[48]  Caspar M. Schwiedrzik,et al.  A spatio-temporal interaction on the apparent motion trace , 2007, Vision Research.

[49]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  Jennifer A. Mangels,et al.  Predictive Codes for Forthcoming Perception in the Frontal Cortex , 2006, Science.

[51]  Karl J. Friston,et al.  Bayesian decoding of brain images , 2008, NeuroImage.

[52]  M. Meister,et al.  Dynamic predictive coding by the retina , 2005, Nature.

[53]  R. Passingham,et al.  Seeing or Doing? Influence of Visual and Motor Familiarity in Action Observation , 2006, Current Biology.

[54]  Aina Puce,et al.  Common and distinct brain activation to viewing dynamic sequences of face and hand movements , 2007, NeuroImage.

[55]  Klaas E. Stephan,et al.  Yearning to yawn: the neural basis of contagious yawning , 2005, NeuroImage.

[56]  A. Treves,et al.  Converging Neuronal Activity in Inferior Temporal Cortex during the Classification of Morphed Stimuli , 2008, Cerebral cortex.

[57]  C. Summerfield,et al.  A Neural Representation of Prior Information during Perceptual Inference , 2008, Neuron.

[58]  Karl J. Friston,et al.  Electromagnetic source reconstruction for group studies , 2008, NeuroImage.

[59]  Karl J. Friston,et al.  Applications of random field theory to electrophysiology , 2005, Neuroscience Letters.