A Neural Basis of Facial Action Recognition in Humans

By combining different facial muscle actions, called action units, humans can produce an extraordinarily large number of facial expressions. Computational models and studies in cognitive science and social psychology have long hypothesized that the brain needs to visually interpret these action units to understand other people's actions and intentions. Surprisingly, no studies have identified the neural basis of the visual recognition of these action units. Here, using functional magnetic resonance imaging and an innovative machine learning analysis approach, we identify a consistent and differential coding of action units in the brain. Crucially, in a brain region thought to be responsible for the processing of changeable aspects of the face, multivoxel pattern analysis could decode the presence of specific action units in an image. This coding was found to be consistent across people, facilitating the estimation of the perceived action units on participants not used to train the multivoxel decoder. Furthermore, this coding of action units was identified when participants attended to the emotion category of the facial expression, suggesting an interaction between the visual analysis of action units and emotion categorization as predicted by the computational models mentioned above. These results provide the first evidence for a representation of action units in the brain and suggest a mechanism for the analysis of large numbers of facial actions and a loss of this capacity in psychopathologies. SIGNIFICANCE STATEMENT Computational models and studies in cognitive and social psychology propound that visual recognition of facial expressions requires an intermediate step to identify visible facial changes caused by the movement of specific facial muscles. Because facial expressions are indeed created by moving one's facial muscles, it is logical to assume that our visual system solves this inverse problem. Here, using an innovative machine learning method and neuroimaging data, we identify for the first time a brain region responsible for the recognition of actions associated with specific facial muscles. Furthermore, this representation is preserved across subjects. Our machine learning analysis does not require mapping the data to a standard brain and may serve as an alternative to hyperalignment.

[1]  C. Darwin The Expression of the Emotions in Man and Animals , .

[2]  R. Fisher THE STATISTICAL UTILIZATION OF MULTIPLE MEASUREMENTS , 1938 .

[3]  R. Thouless Experimental Psychology , 1939, Nature.

[4]  P. Ekman,et al.  Pan-Cultural Elements in Facial Displays of Emotion , 1969, Science.

[5]  P. Ekman,et al.  Facial action coding system: a technique for the measurement of facial movement , 1978 .

[6]  J. Russell A circumplex model of affect. , 1980 .

[7]  G. Boulogne,et al.  The Mechanism of Human Facial Expression , 1990 .

[8]  L. Rubin The Mechanism of Human Facial Expression , 1992 .

[9]  J. Russell,et al.  The psychology of facial expression: Frontmatter , 1997 .

[10]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

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

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

[13]  Cecile McKee The Signs of Language Revisited: An Anthology to Honor Ursula Bellugi and Edward Klima (review) , 2001 .

[14]  Avinash C. Kak,et al.  PCA versus LDA , 2001, IEEE Trans. Pattern Anal. Mach. Intell..

[15]  G. Cottrell,et al.  EMPATH: A Neural Network that Categorizes Facial Expressions , 2002, Journal of Cognitive Neuroscience.

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

[17]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

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

[19]  Alice J. O'Toole,et al.  Partially Distributed Representations of Objects and Faces in Ventral Temporal Cortex , 2005, Journal of Cognitive Neuroscience.

[20]  Aleix M. Martínez,et al.  Where are linear feature extraction methods applicable? , 2005, IEEE Transactions on Pattern Analysis and Machine Intelligence.

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

[22]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[23]  Thomas Serre,et al.  Robust Object Recognition with Cortex-Like Mechanisms , 2007, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[24]  Aleix M. Martínez,et al.  Bayes Optimality in Linear Discriminant Analysis , 2008, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[25]  Joseph Krummenacher,et al.  A (fascinating) litmus test for human retino- vs. non-retinotopic processing. , 2009, Journal of vision.

[26]  Donald I. A. MacLeod,et al.  Hemispheric Differences in the Kinetic Depth Effect , 2009 .

[27]  Heng Tao Shen,et al.  Principal Component Analysis , 2009, Encyclopedia of Biometrics.

[28]  Giuseppe Iaria,et al.  The correlates of subjective perception of identity and expression in the face network: An fMRI adaptation study , 2009, NeuroImage.

[29]  Donald Neth,et al.  Emotion perception in emotionless face images suggests a norm-based representation. , 2009, Journal of vision.

[30]  C. Darwin,et al.  The Expression of the Emotions in Man and Animals , 1956 .

[31]  A. Todorov,et al.  Shared perceptual basis of emotional expressions and trustworthiness impressions from faces. , 2009, Emotion.

[32]  Nikolaus Kriegeskorte,et al.  Comparison of multivariate classifiers and response normalizations for pattern-information fMRI , 2010, NeuroImage.

[33]  Andrew D. Engell,et al.  Distributed representations of dynamic facial expressions in the superior temporal sulcus. , 2010, Journal of vision.

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

[35]  J. Kuhtz-Buschbeck,et al.  The Müller-Lyer illusion: investigation of a center of gravity effect on the amplitudes of saccades. , 2011, Journal of vision.

[36]  S. Hamann,et al.  Neuroimaging Support for Discrete Neural Correlates of Basic Emotions: A Voxel-based Meta-analysis , 2010, Journal of Cognitive Neuroscience.

[37]  Alex Martin,et al.  Facial Emotion Recognition in Autism Spectrum Disorders: A Review of Behavioral and Neuroimaging Studies , 2010, Neuropsychology Review.

[38]  Marlene Behrmann,et al.  Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis , 2011, Proceedings of the National Academy of Sciences.

[39]  Bryan R. Conroy,et al.  A Common, High-Dimensional Model of the Representational Space in Human Ventral Temporal Cortex , 2011, Neuron.

[40]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[41]  Sharon L. Thompson-Schill,et al.  The advantage of brief fMRI acquisition runs for multi-voxel pattern detection across runs , 2012, NeuroImage.

[42]  Aleix M. Martínez,et al.  A Model of the Perception of Facial Expressions of Emotion by Humans: Research Overview and Perspectives , 2012, J. Mach. Learn. Res..

[43]  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.

[44]  Richard J. Harris,et al.  Morphing between expressions dissociates continuous from categorical representations of facial expression in the human brain , 2012, Proceedings of the National Academy of Sciences.

[45]  Penelope L. Mavros,et al.  Atypical brain activation patterns during a face‐to‐face joint attention game in adults with autism spectrum disorder , 2013, Human brain mapping.

[46]  A. Young,et al.  Brain networks subserving the evaluation of static and dynamic facial expressions , 2013, Cortex.

[47]  Yong Tao,et al.  Compound facial expressions of emotion , 2014, Proceedings of the National Academy of Sciences.

[48]  M. Bartlett,et al.  Automatic Decoding of Facial Movements Reveals Deceptive Pain Expressions , 2014, Current Biology.

[49]  Rebecca Saxe,et al.  A Common Neural Code for Perceived and Inferred Emotion , 2014, The Journal of Neuroscience.

[50]  K. Grill-Spector,et al.  The functional architecture of the ventral temporal cortex and its role in categorization , 2014, Nature Reviews Neuroscience.

[51]  Stefan Pollmann,et al.  Investigating the brain basis of facial expression perception using multi-voxel pattern analysis , 2015, Cortex.

[52]  E. Růžička,et al.  Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus , 2015, Proceedings of the National Academy of Sciences.