A Bayesian Model of Category-Specific Emotional Brain Responses

Understanding emotion is critical for a science of healthy and disordered brain function, but the neurophysiological basis of emotional experience is still poorly understood. We analyzed human brain activity patterns from 148 studies of emotion categories (2159 total participants) using a novel hierarchical Bayesian model. The model allowed us to classify which of five categories—fear, anger, disgust, sadness, or happiness—is engaged by a study with 66% accuracy (43-86% across categories). Analyses of the activity patterns encoded in the model revealed that each emotion category is associated with unique, prototypical patterns of activity across multiple brain systems including the cortex, thalamus, amygdala, and other structures. The results indicate that emotion categories are not contained within any one region or system, but are represented as configurations across multiple brain networks. The model provides a precise summary of the prototypical patterns for each emotion category, and demonstrates that a sufficient characterization of emotion categories relies on (a) differential patterns of involvement in neocortical systems that differ between humans and other species, and (b) distinctive patterns of cortical-subcortical interactions. Thus, these findings are incompatible with several contemporary theories of emotion, including those that emphasize emotion-dedicated brain systems and those that propose emotion is localized primarily in subcortical activity. They are consistent with componential and constructionist views, which propose that emotions are differentiated by a combination of perceptual, mnemonic, prospective, and motivational elements. Such brain-based models of emotion provide a foundation for new translational and clinical approaches.

[1]  G. Berntson,et al.  The decerebrate human: Associative learning , 1983, Experimental Neurology.

[2]  Philip A Kragel,et al.  Multivariate pattern classification reveals autonomic and experiential representations of discrete emotions. , 2013, Emotion.

[3]  M. Delgado,et al.  Extending animal models of fear conditioning to humans , 2006, Biological Psychology.

[4]  Dewen Hu,et al.  Altered cerebellar–cerebral resting-state functional connectivity reliably identifies major depressive disorder , 2013, Brain Research.

[5]  Joseph E LeDoux Rethinking the Emotional Brain , 2012, Neuron.

[6]  Ethan Kross,et al.  Discriminating Neural Representations of Physical and Social Pains: How Multivariate Statistics Challenge the 'shared Representation' Theory of Pain Rogachov a Hanna Jr, and Wager Td. Separate Neural Representations for Physical Pain and Social Rejection , 2022 .

[7]  E. E. Smith,et al.  Brain Mechanisms of Social Threat Effects on Working Memory. , 2014, Cerebral cortex.

[8]  Martin A. Lindquist,et al.  Brain mediators of cardiovascular responses to social threat, Part II: Prefrontal-subcortical pathways and relationship with anxiety , 2009, NeuroImage.

[9]  J. Grau Learning from the spinal cord: How the study of spinal cord plasticity informs our view of learning , 2014, Neurobiology of Learning and Memory.

[10]  Lars Kai Hansen,et al.  Mining for associations between text and brain activation in a functional neuroimaging database , 2007, Neuroinformatics.

[11]  Lisa Feldman Barrett,et al.  Emotions are real. , 2012, Emotion.

[12]  P. Ekman,et al.  What is Meant by Calling Emotions Basic , 2011 .

[13]  J. W. Aldridge,et al.  Dissecting components of reward: 'liking', 'wanting', and learning. , 2009, Current opinion in pharmacology.

[14]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[15]  M. Corbetta,et al.  Evolutionarily Novel Functional Networks in the Human Brain? , 2013, The Journal of Neuroscience.

[16]  Amit Etkin,et al.  Hippocampal Network Connectivity and Activation Differentiates Post-Traumatic Stress Disorder From Generalized Anxiety Disorder , 2013, Neuropsychopharmacology.

[17]  Larry W Swanson,et al.  Dissecting the brain's fear system reveals the hypothalamus is critical for responding in subordinate conspecific intruders , 2009, Proceedings of the National Academy of Sciences.

[18]  Martin A. Lindquist,et al.  Brain mediators of cardiovascular responses to social threat Part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity , 2009, NeuroImage.

[19]  Lisa Feldman Barrett,et al.  Considering PTSD from the perspective of brain processes: a psychological construction approach. , 2011, Journal of traumatic stress.

[20]  Ajay B. Satpute,et al.  Large-scale brain networks in affective and social neuroscience: towards an integrative functional architecture of the brain , 2013, Current Opinion in Neurobiology.

[21]  Huafu Chen,et al.  Characterization of Post-traumatic Stress Disorder Using Resting-State fMRI with a Multi-level Parametric Classification Approach , 2014, Brain Topography.

[22]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[23]  K. Scherer Studying the emotion-antecedent appraisal process: An expert system approach , 1993 .

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

[25]  K. Amunts,et al.  Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps , 2005, Anatomy and Embryology.

[26]  L. F. Barrett Solving the Emotion Paradox: Categorization and the Experience of Emotion , 2006, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[27]  R Cameron Craddock,et al.  Disease state prediction from resting state functional connectivity , 2009, Magnetic resonance in medicine.

[28]  Lisa Feldman Barrett,et al.  Feeling Blue or Turquoise? Emotional Differentiation in Major Depressive Disorder , 2012, Psychological science.

[29]  Lisa Feldman Barrett,et al.  Psychological Construction: The Darwinian Approach to the Science of Emotion , 2013 .

[30]  Jessica L. Tracy,et al.  Four Models of Basic Emotions: A Review of Ekman and Cordaro, Izard, Levenson, and Panksepp and Watt , 2011 .

[31]  J L McGaugh,et al.  Basolateral Amygdala Is Involved in Modulating Consolidation of Memory for Classical Fear Conditioning , 1999, The Journal of Neuroscience.

[32]  Daniella J. Furman,et al.  Default-Mode and Task-Positive Network Activity in Major Depressive Disorder: Implications for Adaptive and Maladaptive Rumination , 2011, Biological Psychiatry.

[33]  Christopher L. Asplund,et al.  The organization of the human cerebellum estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[34]  Charles J. Lynch,et al.  Default Mode Network in Childhood Autism: Posteromedial Cortex Heterogeneity and Relationship with Social Deficits , 2013, Biological Psychiatry.

[35]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[36]  Ulf Toelch,et al.  Cross-modal effects of value on perceptual acuity and stimulus encoding , 2014, Proceedings of the National Academy of Sciences.

[37]  W. James,et al.  What Is an Emotion , 1977 .

[38]  A. Lozano,et al.  Deep Brain Stimulation for Treatment-Resistant Depression , 2005, Neuron.

[39]  W. James II.—WHAT IS AN EMOTION ? , 1884 .

[40]  Cynthia G. Wible,et al.  Investigation of spectrally coherent resting‐state networks using non‐negative matrix factorization for functional MRI data , 2011, Int. J. Imaging Syst. Technol..

[41]  Kristen A. Lindquist,et al.  A functional architecture of the human brain: emerging insights from the science of emotion , 2012, Trends in Cognitive Sciences.

[42]  Thomas E. Nichols,et al.  Meta Analysis of Functional Neuroimaging Data via Bayesian Spatial Point Processes , 2011, Journal of the American Statistical Association.

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

[44]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[45]  L. Garriga-Grimau,et al.  [Cerebellar cognitive affective syndrome]. , 2015, Archivos argentinos de pediatria.

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

[47]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[48]  S. Dickerson,et al.  Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. , 2004, Psychological bulletin.

[49]  Lisa Feldman Barrett,et al.  Neural Evidence That Human Emotions Share Core Affective Properties , 2013, Psychological science.

[50]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[51]  J. Fuster Prefrontal Cortex , 2018 .

[52]  M. Just,et al.  Identifying Emotions on the Basis of Neural Activation , 2013, PloS one.

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

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

[55]  R. Buckner,et al.  The organization of the human striatum estimated by intrinsic functional connectivity. , 2012, Journal of neurophysiology.

[56]  D. Shohamy,et al.  Ventromedial prefrontal-subcortical systems and the generation of affective meaning , 2012, Trends in Cognitive Sciences.

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

[58]  Shannon Fogh,et al.  Localized therapy for male breast cancer: functional advantages with comparable outcomes using breast conservation. , 2013, Clinical breast cancer.

[59]  Daphna Shohamy,et al.  Representation of aversive prediction errors in the human periaqueductal gray , 2014, Nature Neuroscience.

[60]  J. Price Prefrontal Cortical Networks Related to Visceral Function and Mood , 1999, Annals of the New York Academy of Sciences.

[61]  P. Strick,et al.  Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. , 1994, Science.

[62]  Hans Colonius,et al.  Behavioral Measures of Multisensory Integration: Bounds on Bimodal Detection Probability , 2014, Brain Topography.

[63]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[64]  Richard J Davidson,et al.  Emotion as Motion , 2007, Psychological science.

[65]  김정란 The Real , 2020, The Palm at the End of the Mind.

[66]  P. Maclean Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). , 1952, Electroencephalography and clinical neurophysiology.

[67]  Chad L. Stephens,et al.  Autonomic specificity of basic emotions: Evidence from pattern classification and cluster analysis , 2010, Biological Psychology.

[68]  Rutvik H. Desai,et al.  The neurobiology of semantic memory , 2011, Trends in Cognitive Sciences.

[69]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.

[70]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[71]  K. Deisseroth,et al.  Optogenetic investigation of neural circuits underlying brain disease in animal models , 2012, Nature Reviews Neuroscience.

[72]  M. Brammer,et al.  Pattern Classification of Sad Facial Processing: Toward the Development of Neurobiological Markers in Depression , 2008, Biological Psychiatry.

[73]  Michael R. Irwin,et al.  Reciprocal regulation of the neural and innate immune systems , 2011, Nature Reviews Immunology.

[74]  J. Schmahmann,et al.  Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. , 2004, The Journal of neuropsychiatry and clinical neurosciences.

[75]  J. Thayer,et al.  eview meta-analysis of heart rate variability and neuroimaging studies : Implications or heart rate variability as a marker of stress and health , 2012 .

[76]  Lisa Feldman Barrett,et al.  The psychological construction of emotion , 2014 .

[77]  P. Lang The emotion probe. Studies of motivation and attention. , 1995, The American psychologist.

[78]  T. Dalgleish,et al.  Handbook of cognition and emotion , 1999 .

[79]  L. F. Barrett,et al.  Knowing what you're feeling and knowing what to do about it: Mapping the relation between emotion differentiation and emotion regulation , 2001 .

[80]  R. Davidson,et al.  Right hemisphere lateralization for emotion in the human brain: interactions with cognition , 1975, Science.

[81]  Joseph J Paton,et al.  Functional Circuits and Anatomical Distribution of Response Properties in the Primate Amygdala , 2013, The Journal of Neuroscience.

[82]  Kevin N. Ochsner,et al.  A Meta-analysis of Functional Neuroimaging Studies of Self- and Other Judgments Reveals a Spatial Gradient for Mentalizing in Medial Prefrontal Cortex , 2012, Journal of Cognitive Neuroscience.

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

[84]  Ajay B. Satpute,et al.  The Functional Neural Architecture of Self-Reports of Affective Experience , 2013, Biological Psychiatry.

[85]  Kristen A. Lindquist,et al.  Intrinsic connectivity in the human brain does not reveal networks for 'basic' emotions. , 2015, Social cognitive and affective neuroscience.

[86]  S. Gilbert Decoding the Content of Delayed Intentions , 2011, The Journal of Neuroscience.

[87]  Gary G. Berntson,et al.  Organization of brainstem behavioral systems , 1976, Brain Research Bulletin.

[88]  Lisa Feldman Barrett,et al.  States of mind: Emotions, body feelings, and thoughts share distributed neural networks , 2012, NeuroImage.

[89]  E. Rolls,et al.  Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. , 2003, Brain : a journal of neurology.

[90]  E. Silberman,et al.  Hemispheric lateralization of functions related to emotion , 1986, Brain and Cognition.

[91]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[92]  William A. Cunningham,et al.  Emotional States from Affective Dynamics , 2013 .

[93]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[94]  Jian Kang,et al.  Some Novel Spatial Stochastic Models for Functional Neuroimaging Analysis. , 2011 .

[95]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

[96]  Lisa Feldman Barrett,et al.  Grounding emotion in situated conceptualization , 2011, Neuropsychologia.

[97]  R. Lane,et al.  Levels of emotional awareness: a cognitive-developmental theory and its application to psychopathology. , 1987, The American journal of psychiatry.

[98]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

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

[100]  D. Dutton,et al.  Some evidence for heightened sexual attraction under conditions of high anxiety. , 1974, Journal of personality and social psychology.

[101]  J. Hietanen,et al.  Bodily maps of emotions , 2013, Proceedings of the National Academy of Sciences.

[102]  Leonard M. Freeman,et al.  A set of measures of centrality based upon betweenness , 1977 .

[103]  S. Lui,et al.  Prediction of post-earthquake depressive and anxiety symptoms: a longitudinal resting-state fMRI study , 2014, Scientific reports.

[104]  J. Panksepp Affective Neuroscience: The Foundations of Human and Animal Emotions , 1998 .

[105]  W. Mehling,et al.  Are difficulties perceiving and expressing emotions associated with low-back pain? The relationship between lack of emotional awareness (alexithymia) and 12-month prevalence of low-back pain in 1180 urban public transit operators. , 2005, Journal of psychosomatic research.

[106]  C. Neil Macrae,et al.  The Link between Social Cognition and Self-referential Thought in the Medial Prefrontal Cortex , 2005, Journal of Cognitive Neuroscience.

[107]  H. Sebastian Seung,et al.  Learning the parts of objects by non-negative matrix factorization , 1999, Nature.

[108]  Eshkol Rafaeli,et al.  Emotion differentiation as a protective factor against nonsuicidal self-injury in borderline personality disorder. , 2013, Behavior therapy.

[109]  D. Hu,et al.  Identifying major depression using whole-brain functional connectivity: a multivariate pattern analysis. , 2012, Brain : a journal of neurology.

[110]  R. Goebel,et al.  Pattern classification of valence in depression☆ , 2013, NeuroImage: Clinical.

[111]  A. Kring Emotion disturbances as transdiagnostic processes in psychopathology. , 2008 .

[112]  R W Guillery,et al.  The role of the thalamus in the flow of information to the cortex. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.