Emotionotopy in the human right temporo-parietal cortex

Humans use emotions to decipher complex cascades of internal events. However, which mechanisms link descriptions of affective states to brain activity is unclear, with evidence supporting either local or distributed processing. A biologically favorable alternative is provided by the notion of gradient, which postulates the isomorphism between functional representations of stimulus features and cortical distance. Here, we use fMRI activity evoked by an emotionally charged movie and continuous ratings of the perceived emotion intensity to reveal the topographic organization of affective states. Results show that three orthogonal and spatially overlapping gradients encode the polarity, complexity and intensity of emotional experiences in right temporo-parietal territories. The spatial arrangement of these gradients allows the brain to map a variety of affective states within a single patch of cortex. As this organization resembles how sensory regions represent psychophysical properties (e.g., retinotopy), we propose emotionotopy as a principle of emotion coding. People can experience a wide variety of emotions, and how the brain represents these varying affective states is a matter of debate. Here the authors show that coding mechanisms of emotions in right temporo-parietal cortex resemble those of low-level stimulus features in primary sensory regions.

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

[2]  M. Sams,et al.  Distributed affective space represents multiple emotion categories across the human brain , 2018, Social cognitive and affective neuroscience.

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

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

[5]  Diana I Tamir,et al.  Mental models accurately predict emotion transitions , 2017, Proceedings of the National Academy of Sciences.

[6]  Andrew Ortony,et al.  The Cognitive Structure of Emotions , 1988 .

[7]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

[8]  Thomas E. Nichols,et al.  A Bayesian Model of Category-Specific Emotional Brain Responses , 2015, PLoS Comput. Biol..

[9]  R Walker,et al.  Cultural differences in emotions: a context for interpreting emotional experiences. , 2003, Behaviour research and therapy.

[10]  Geoffrey E. Hinton,et al.  Visualizing Data using t-SNE , 2008 .

[11]  B. P. Klein,et al.  Topographic Representation of Numerosity in the Human Parietal Cortex , 2013, Science.

[12]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[13]  Emiliano Ricciardi,et al.  Modality-independent encoding of individual concepts in the left parietal cortex , 2017, Neuropsychologia.

[14]  Forrest Gump Portrayed emotions in the movie " , 2017 .

[15]  Matthew D. Lieberman,et al.  The neural components of empathy: predicting daily prosocial behavior. , 2014, Social cognitive and affective neuroscience.

[16]  Michael Hanke,et al.  A studyforrest extension, simultaneous fMRI and eye gaze recordings during prolonged natural stimulation , 2016, Scientific Data.

[17]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[18]  Ajay B. Satpute,et al.  The Brain Basis of Positive and Negative Affect: Evidence from a Meta-Analysis of the Human Neuroimaging Literature. , 2016, Cerebral cortex.

[19]  Michael Hanke,et al.  Portrayed emotions in the movie "Forrest Gump" , 2015, F1000Research.

[20]  Murray Smith Engaging Characters: Fiction, Emotion, and the Cinema , 1995 .

[21]  Janaina Mourão Miranda,et al.  Contributions of stimulus valence and arousal to visual activation during emotional perception , 2003, NeuroImage.

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

[23]  J. Diedrichsen,et al.  Hand use predicts the structure of representations in sensorimotor cortex , 2015, Nature Neuroscience.

[24]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[25]  Stefanie Seiler,et al.  Finding Groups In Data , 2016 .

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

[27]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

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

[29]  Koen V. Haak,et al.  Connectopic mapping with resting-state fMRI , 2016, NeuroImage.

[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]  Schreiber,et al.  Improved Surrogate Data for Nonlinearity Tests. , 1996, Physical review letters.

[32]  Matteo Bianchi,et al.  A synergy-based hand control is encoded in human motor cortical areas , 2016, eLife.

[33]  Philip A. Kragel,et al.  Multivariate neural biomarkers of emotional states are categorically distinct. , 2015, Social cognitive and affective neuroscience.

[34]  Jack L. Gallant,et al.  Pyrcca: Regularized Kernel Canonical Correlation Analysis in Python and Its Applications to Neuroimaging , 2015, Front. Neuroinform..

[35]  J. Gross,et al.  Emotion elicitation using films , 1995 .

[36]  Sylvia D. Kreibig,et al.  Autonomic nervous system activity in emotion: A review , 2010, Biological Psychology.

[37]  Ralph Adolphs,et al.  The Biology of Fear , 2013, Current Biology.

[38]  Sarah-Jayne Blakemore,et al.  Functional connectivity during a social emotion task in adolescents and in adults , 2009, The European journal of neuroscience.

[39]  R. Hari,et al.  Discrete Neural Signatures of Basic Emotions. , 2016, Cerebral cortex.

[40]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.

[41]  F. Overwalle Social cognition and the brain: a meta-analysis. , 2009 .

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

[43]  Philip A. Kragel,et al.  Decoding the Nature of Emotion in the Brain , 2016, Trends in Cognitive Sciences.

[44]  M. Taquet,et al.  Emotions in Everyday Life , 2015, PloS one.

[45]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[46]  Julia M. Huntenburg,et al.  Large-Scale Gradients in Human Cortical Organization , 2018, Trends in Cognitive Sciences.

[47]  Craig A. Smith,et al.  Patterns of cognitive appraisal in emotion. , 1985, Journal of personality and social psychology.

[48]  N. Rinehart,et al.  Noninvasive stimulation of the temporoparietal junction: A systematic review , 2015, Neuroscience & Biobehavioral Reviews.

[49]  Mara Mather,et al.  Emotional Arousal Can Impair Feature Binding in Working Memory , 2006, Journal of Cognitive Neuroscience.

[50]  Lisa Feldman Barrett,et al.  The Structure of Emotion , 2006 .

[51]  C. Almli,et al.  Unbiased nonlinear average age-appropriate brain templates from birth to adulthood , 2009, NeuroImage.

[52]  L. F. Barrett,et al.  Multivoxel Pattern Analysis Does Not Provide Evidence to Support the Existence of Basic Emotions. , 2016, Cerebral cortex.

[53]  Karl J. Friston Imaging cognitive anatomy , 1997, Trends in Cognitive Sciences.

[54]  Elizabeth Jefferies,et al.  Situating the default-mode network along a principal gradient of macroscale cortical organization , 2016, Proceedings of the National Academy of Sciences.

[55]  D. Schacter,et al.  Processing emotional pictures and words: Effects of valence and arousal , 2006, Cognitive, affective & behavioral neuroscience.

[56]  P. Philippot Inducing and assessing differentiated emotion-feeling states in the laboratory. , 1993, Cognition & emotion.

[57]  Alan S. Cowen,et al.  Self-report captures 27 distinct categories of emotion bridged by continuous gradients , 2017, Proceedings of the National Academy of Sciences.

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

[59]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[60]  Aaron R. Seitz,et al.  Detecting and Quantifying Topography in Neural Maps , 2014, PloS one.

[61]  John Suckling,et al.  Shared Neural Circuits for Mentalizing about the Self and Others , 2010, Journal of Cognitive Neuroscience.

[62]  A. Schaefer,et al.  Please Scroll down for Article Cognition & Emotion Assessing the Effectiveness of a Large Database of Emotion-eliciting Films: a New Tool for Emotion Researchers , 2022 .

[63]  Timothy S. Coalson,et al.  Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. , 2012, Cerebral cortex.

[64]  R. Hari,et al.  Emotions promote social interaction by synchronizing brain activity across individuals , 2012, Proceedings of the National Academy of Sciences.

[65]  P. Ekman An argument for basic emotions , 1992 .

[66]  James A. Russell,et al.  Mixed Emotions Viewed from the Psychological Constructionist Perspective , 2017 .

[67]  L. Phillips,et al.  The overlapping relationship between emotion perception and theory of mind , 2015, Neuropsychologia.

[68]  T. Shallice,et al.  Impact of brain tumour location on emotion and personality: a voxel-based lesion-symptom mapping study on mentalization processes. , 2014, Brain : a journal of neurology.

[69]  K. Scherer,et al.  The World of Emotions is not Two-Dimensional , 2007, Psychological science.

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

[71]  Yaroslav O. Halchenko,et al.  The Animacy Continuum in the Human Ventral Vision Pathway , 2015, Journal of Cognitive Neuroscience.

[72]  Jack L. Gallant,et al.  Encoding and decoding in fMRI , 2011, NeuroImage.

[73]  Jeff T. Larsen,et al.  Can people feel happy and sad at the same time? , 2001, Journal of personality and social psychology.

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

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

[76]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[77]  Jaak Panksepp,et al.  Toward a general psychobiological theory of emotions , 1982, Behavioral and Brain Sciences.

[78]  Peter Totterdell,et al.  Eliciting mixed emotions: a meta-analysis comparing models, types, and measures , 2015, Front. Psychol..

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

[80]  K. Luan Phan,et al.  Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging , 2003, NeuroImage.

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

[82]  Rebecca Saxe,et al.  Neural Representations of Emotion Are Organized around Abstract Event Features , 2015, Current Biology.

[83]  Talma Hendler,et al.  Cry for her or cry with her: context-dependent dissociation of two modes of cinematic empathy reflected in network cohesion dynamics. , 2014, Social cognitive and affective neuroscience.

[84]  J. Russell,et al.  An approach to environmental psychology , 1974 .

[85]  Thomas L. Griffiths,et al.  Supplementary Information for Natural Speech Reveals the Semantic Maps That Tile Human Cerebral Cortex , 2022 .

[86]  T. Redman The Impact of , 1998 .

[87]  Matthew D. Lieberman,et al.  The role of automaticity and attention in neural processes underlying empathy for happiness, sadness, and anxiety , 2013, Front. Hum. Neurosci..