A Common Neural Code for Perceived and Inferred Emotion

Although the emotions of other people can often be perceived from overt reactions (e.g., facial or vocal expressions), they can also be inferred from situational information in the absence of observable expressions. How does the human brain make use of these diverse forms of evidence to generate a common representation of a target's emotional state? In the present research, we identify neural patterns that correspond to emotions inferred from contextual information and find that these patterns generalize across different cues from which an emotion can be attributed. Specifically, we use functional neuroimaging to measure neural responses to dynamic facial expressions with positive and negative valence and to short animations in which the valence of a character's emotion could be identified only from the situation. Using multivoxel pattern analysis, we test for regions that contain information about the target's emotional state, identifying representations specific to a single stimulus type and representations that generalize across stimulus types. In regions of medial prefrontal cortex (MPFC), a classifier trained to discriminate emotional valence for one stimulus (e.g., animated situations) could successfully discriminate valence for the remaining stimulus (e.g., facial expressions), indicating a representation of valence that abstracts away from perceptual features and generalizes across different forms of evidence. Moreover, in a subregion of MPFC, this neural representation generalized to trials involving subjectively experienced emotional events, suggesting partial overlap in neural responses to attributed and experienced emotions. These data provide a step toward understanding how the brain transforms stimulus-bound inputs into abstract representations of emotion.

[1]  Jamil Zaki,et al.  Unpacking the informational bases of empathic accuracy. , 2009, Emotion.

[2]  H Sompolinsky,et al.  Simple models for reading neuronal population codes. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Scott T. Grafton,et al.  Differential role of the orbital frontal lobe in emotional versus cognitive perspective-taking , 2006, Neuropsychologia.

[4]  J. O'Doherty,et al.  Evidence for a Common Representation of Decision Values for Dissimilar Goods in Human Ventromedial Prefrontal Cortex , 2009, The Journal of Neuroscience.

[5]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[6]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[7]  J. Rothwell,et al.  Mapping causal interregional influences with concurrent TMS–fMRI , 2008, Experimental Brain Research.

[8]  A. Caramazza,et al.  Decoding representations of face identity that are tolerant to rotation. , 2014, Cerebral cortex.

[9]  Tomaso Poggio,et al.  Fast Readout of Object Identity from Macaque Inferior Temporal Cortex , 2005, Science.

[10]  E. Fehr,et al.  The neurobiology of rewards and values in social decision making , 2014, Nature Reviews Neuroscience.

[11]  Michael Erb,et al.  Cerebral pathways in processing of affective prosody: A dynamic causal modeling study , 2006, NeuroImage.

[12]  A. Tversky,et al.  Loss Aversion in Riskless Choice: A Reference-Dependent Model , 1991 .

[13]  Wolfgang Grodd,et al.  Cerebral representation of non-verbal emotional perception: fMRI reveals audiovisual integration area between voice- and face-sensitive regions in the superior temporal sulcus , 2009, Neuropsychologia.

[14]  Winrich A. Freiwald Faculty Opinions recommendation of Dynamic and static facial expressions decoded from motion-sensitive areas in the macaque monkey. , 2013 .

[15]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

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

[17]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[18]  K M Gothard,et al.  Neural responses to facial expression and face identity in the monkey amygdala. , 2007, Journal of neurophysiology.

[19]  Daniel D. Dilks,et al.  Differential selectivity for dynamic versus static information in face-selective cortical regions , 2011, NeuroImage.

[20]  Joseph W. Kable,et al.  The valuation system: A coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value , 2013, NeuroImage.

[21]  K Tanaka,et al.  Neuronal mechanisms of object recognition. , 1993, Science.

[22]  Ning Liu,et al.  Dynamic and Static Facial Expressions Decoded from Motion-Sensitive Areas in the Macaque Monkey , 2012, The Journal of Neuroscience.

[23]  David D. Cox,et al.  Untangling invariant object recognition , 2007, Trends in Cognitive Sciences.

[24]  T. Allison,et al.  Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. , 2005, Cerebral cortex.

[25]  Rebecca Saxe,et al.  Similar Brain Activation during False Belief Tasks in a Large Sample of Adults with and without Autism , 2013, PloS one.

[26]  N. Kriegeskorte,et al.  Author ' s personal copy Representational geometry : integrating cognition , computation , and the brain , 2013 .

[27]  K. Ochsner,et al.  The Need for a Cognitive Neuroscience of Naturalistic Social Cognition , 2009, Annals of the New York Academy of Sciences.

[28]  J. C. Rothwell,et al.  Transcranial magnetic stimulation of medial–frontal cortex impairs the processing of angry facial expressions , 2001, Nature Neuroscience.

[29]  Nancy Kanwisher,et al.  An algorithmic method for functionally defining regions of interest in the ventral visual pathway , 2012, NeuroImage.

[30]  Jason P. Mitchell Inferences about mental states , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[31]  Jeremy Freeman,et al.  Orientation Decoding Depends on Maps, Not Columns , 2011, The Journal of Neuroscience.

[32]  N. Bolger,et al.  The neural bases of empathic accuracy , 2009, Proceedings of the National Academy of Sciences.

[33]  Tom M. Mitchell,et al.  Machine learning classifiers and fMRI: A tutorial overview , 2009, NeuroImage.

[34]  Yi Chen,et al.  Statistical inference and multiple testing correction in classification-based multi-voxel pattern analysis (MVPA): Random permutations and cluster size control , 2011, NeuroImage.

[35]  Rebecca Elliott,et al.  Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task , 2006, NeuroImage.

[36]  J. Weber,et al.  Journal Section: Behavioral/systems/cognitive Social Cognitive Conflict Resolution: Contributions of Domain General and Domain Specific Neural Systems , 2022 .

[37]  Melissa L. Allen,et al.  Kaufman Brief Intelligence Test , 2021, Encyclopedia of Autism Spectrum Disorders.

[38]  P. Niedenthal Embodying Emotion , 2007, Science.

[39]  James J. DiCarlo,et al.  How Does the Brain Solve Visual Object Recognition? , 2012, Neuron.

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

[41]  S. Carey Conceptual Change in Childhood , 1985 .

[42]  Jeesun Kim,et al.  Emotional expressions evoke a differential response in the fusiform face area , 2013, Front. Hum. Neurosci..

[43]  Amy A. Winecoff,et al.  Ventromedial Prefrontal Cortex Encodes Emotional Value , 2013, The Journal of Neuroscience.

[44]  Haim Sompolinsky,et al.  Implications of Neuronal Diversity on Population Coding , 2006, Neural Computation.

[45]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[46]  David Pitcher,et al.  Facial Expression Recognition Takes Longer in the Posterior Superior Temporal Sulcus than in the Occipital Face Area , 2014, The Journal of Neuroscience.

[47]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

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

[49]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[50]  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.

[51]  Wen-Ming Luh,et al.  Amygdala lesions disrupt modulation of functional MRI activity evoked by facial expression in the monkey inferior temporal cortex , 2012, Proceedings of the National Academy of Sciences.

[52]  Johan D. Carlin,et al.  A Head View-Invariant Representation of Gaze Direction in Anterior Superior Temporal Sulcus , 2011, Current Biology.

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

[54]  A. Caramazza,et al.  Brain Regions That Represent Amodal Conceptual Knowledge , 2013, The Journal of Neuroscience.

[55]  R. Dolan,et al.  Separate Coding of Different Gaze Directions in the Superior Temporal Sulcus and Inferior Parietal Lobule , 2007, Current Biology.

[56]  J. O'Doherty,et al.  Orbitofrontal Cortex Encodes Willingness to Pay in Everyday Economic Transactions , 2007, The Journal of Neuroscience.

[57]  S. Baron-Cohen,et al.  The Autism-Spectrum Quotient (AQ): Evidence from Asperger Syndrome/High-Functioning Autism, Malesand Females, Scientists and Mathematicians , 2001, Journal of autism and developmental disorders.

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

[59]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

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

[61]  Matthew D. Lieberman,et al.  An integrative model of the neural systems supporting the comprehension of observed emotional behavior , 2012, NeuroImage.

[62]  Rainer Goebel,et al.  Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns , 2008, NeuroImage.

[63]  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.

[64]  A. Rangel,et al.  Informatic parcellation of the network involved in the computation of subjective value. , 2014, Social cognitive and affective neuroscience.

[65]  Ryan A. Stevenson,et al.  Audiovisual integration in human superior temporal sulcus: Inverse effectiveness and the neural processing of speech and object recognition , 2009, NeuroImage.

[66]  Rebecca Saxe,et al.  fMRI item analysis in a theory of mind task , 2011, NeuroImage.

[67]  Mark H. Davis Measuring individual differences in empathy: Evidence for a multidimensional approach. , 1983 .

[68]  R. Adolphs,et al.  Social and monetary reward learning engage overlapping neural substrates. , 2012, Social cognitive and affective neuroscience.

[69]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[70]  Z. Cattaneo,et al.  Transcranial magnetic stimulation of medial prefrontal cortex modulates face expressions processing in a priming task , 2011, Neuropsychologia.

[71]  B. Berger,et al.  Characterization of Empathy Deficits following Prefrontal Brain Damage: The Role of the Right Ventromedial Prefrontal Cortex , 2003, Journal of Cognitive Neuroscience.

[72]  J. Aharon-Peretz,et al.  Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. , 2009, Brain : a journal of neurology.

[73]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[74]  L. Tyler,et al.  Representational Similarity Analysis Reveals Commonalities and Differences in the Semantic Processing of Words and Objects , 2013, The Journal of Neuroscience.

[75]  K. Scherer,et al.  Human Emotion Experiences Can Be Predicted on Theoretical Grounds: Evidence from Verbal Labeling , 2013, PloS one.

[76]  Tom M. Mitchell,et al.  Learning to Decode Cognitive States from Brain Images , 2004, Machine Learning.

[77]  S. Ullman Three-dimensional object recognition based on the combination of views , 1998, Cognition.

[78]  Kenneth A. Norman,et al.  Graded Representations of Emotional Expressions in the Left Superior Temporal Sulcus , 2010, Front. Syst. Neurosci..

[79]  I. Biederman,et al.  Loci of the release from fMRI adaptation for changes in facial expression, identity, and viewpoint. , 2010, Journal of vision.

[80]  Emile G. Bruneau,et al.  Distinct roles of the ‘Shared Pain’ and ‘Theory of Mind’ networks in processing others’ emotional suffering , 2012, Neuropsychologia.

[81]  P. Ekman,et al.  What the face reveals : basic and applied studies of spontaneous expression using the facial action coding system (FACS) , 2005 .

[82]  Adam K. Anderson,et al.  Population coding of affect across stimuli, modalities and individuals , 2014, Nature Neuroscience.

[83]  A. Goldman,et al.  Simulationist models of face-based emotion recognition , 2005, Cognition.

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

[85]  P. Glimcher,et al.  The neural correlates of subjective value during intertemporal choice , 2007, Nature Neuroscience.

[86]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[87]  Leif D. Nelson,et al.  Data from Paper “False-Positive Psychology: Undisclosed Flexibility in Data Collection and Analysis Allows Presenting Anything as Significant” , 2014 .

[88]  Hans P. Op de Beeck,et al.  Against hyperacuity in brain reading: Spatial smoothing does not hurt multivariate fMRI analyses? , 2010, NeuroImage.

[89]  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.

[90]  A. Gopnik,et al.  Why the Child's Theory of Mind Really Is a Theory , 1992 .