Brain networks for engaging oneself in positive-social emotion regulation

ABSTRACT Positive emotions facilitate cognitive performance, and their absence is associated with burdening psychiatric disorders. However, the brain networks regulating positive emotions are not well understood, especially with regard to engaging oneself in positive‐social situations. Here we report convergent evidence from a multimodal approach that includes functional magnetic resonance imaging (fMRI) brain activations, meta‐analytic functional characterization, Bayesian model‐driven analysis of effective brain connectivity, and personality questionnaires to identify the brain networks mediating the cognitive up‐regulation of positive‐social emotions. Our comprehensive approach revealed that engaging in positive‐social emotion regulation with a self‐referential first‐person perspective is characterized by dynamic interactions between functionally specialized prefrontal cortex (PFC) areas, the temporoparietal junction (TPJ) and the amygdala. Increased top‐down connectivity from the superior frontal gyrus (SFG) controls affective valuation in the ventromedial and dorsomedial PFC, self‐referential processes in the TPJ, and modulate emotional responses in the amygdala via the ventromedial PFC. Understanding the brain networks engaged in the regulation of positive‐social emotions that involve a first‐person perspective is important as they are known to constitute an effective strategy in therapeutic settings. HIGHLIGHTSBrain networks for engaging in first‐person positive‐social emotion regulation revealed.Positive‐social emotion regulation modulates prefrontal‐TPJ‐subcortical interactions.Cognitive control processes originate in interacting prefrontal cortex regions.Brain networks associated with regulating positive and negative emotions overlap.

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

[2]  Karl J. Friston,et al.  Ten simple rules for dynamic causal modeling , 2010, NeuroImage.

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

[4]  M. Bradley,et al.  Looking at pictures: affective, facial, visceral, and behavioral reactions. , 1993, Psychophysiology.

[5]  Stéphane Lehéricy,et al.  In search of the depressive self: extended medial prefrontal network during self-referential processing in major depression. , 2009, Social cognitive and affective neuroscience.

[6]  A. Grabowska,et al.  The Nencki Affective Picture System (NAPS): Introduction to a novel, standardized, wide-range, high-quality, realistic picture database , 2013, Behavior research methods.

[7]  Karl J. Friston,et al.  Post-hoc selection of dynamic causal models , 2012, Journal of Neuroscience Methods.

[8]  Sang Hee Kim,et al.  Neural Correlates of Positive and Negative Emotion Regulation , 2007, Journal of Cognitive Neuroscience.

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

[10]  C. Crane,et al.  A systematic review of mechanisms of change in mindfulness-based cognitive therapy in the treatment of recurrent major depressive disorder. , 2015, Clinical psychology review.

[11]  Angela R Laird,et al.  Brainmap taxonomy of experimental design: Description and evaluation , 2005, Human brain mapping.

[12]  J. P. Minda,et al.  Better Mood and Better Performance , 2010, Psychological science.

[13]  Mark Jenkinson,et al.  Fast, automated, N‐dimensional phase‐unwrapping algorithm , 2003, Magnetic resonance in medicine.

[14]  Dimitri Van De Ville,et al.  Real-time fMRI data for testing OpenNFT functionality , 2017, Data in brief.

[15]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[16]  K. Davis,et al.  Lateralization in intrinsic functional connectivity of the temporoparietal junction with salience- and attention-related brain networks. , 2012, Journal of neurophysiology.

[17]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[18]  Jamil Zaki,et al.  Neural substrates of empathic accuracy in people with schizophrenia. , 2013, Schizophrenia bulletin.

[19]  R. Adolphs,et al.  The social brain: neural basis of social knowledge. , 2009, Annual review of psychology.

[20]  Dimitri Van De Ville,et al.  Data-driven tensor independent component analysis for model-based connectivity neurofeedback , 2019, NeuroImage.

[21]  John D E Gabrieli,et al.  Bottom-Up and Top-Down Processes in Emotion Generation , 2009, Psychological science.

[22]  Naama Mayseless,et al.  Unleashing creativity: The role of left temporoparietal regions in evaluating and inhibiting the generation of creative ideas , 2014, Neuropsychologia.

[23]  Adeel Razi,et al.  Bayesian model reduction and empirical Bayes for group (DCM) studies , 2016, NeuroImage.

[24]  E. Fehr,et al.  Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice , 2011, Nature Neuroscience.

[25]  Patrik Vuilleumier,et al.  Lateralized interactive social content and valence processing within the human amygdala , 2013, Front. Hum. Neurosci..

[26]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[28]  K. Ochsner,et al.  The neuroscience of empathy: progress, pitfalls and promise , 2012, Nature Neuroscience.

[29]  J. Gross,et al.  Explicit and implicit emotion regulation: a multi-level framework , 2017, Social cognitive and affective neuroscience.

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

[31]  Olaf Blanke,et al.  The brain network reflecting bodily self-consciousness: a functional connectivity study. , 2014, Social cognitive and affective neuroscience.

[32]  Karl J. Friston,et al.  A critique of functional localisers , 2006, NeuroImage.

[33]  V. Ramachandran,et al.  The simulating social mind: the role of the mirror neuron system and simulation in the social and communicative deficits of autism spectrum disorders. , 2007, Psychological bulletin.

[34]  Klaus Mathiak,et al.  Signal quality and Bayesian signal processing in neurofeedback based on real-time fMRI , 2012, NeuroImage.

[35]  R. Kana,et al.  Differential role of temporoparietal junction and medial prefrontal cortex in causal inference in autism: An independent component analysis , 2014, Neuroscience Letters.

[36]  Simon B Eickhoff,et al.  Meta-analysis in human neuroimaging: computational modeling of large-scale databases. , 2014, Annual review of neuroscience.

[37]  K. Scherer,et al.  The Geneva affective picture database (GAPED): a new 730-picture database focusing on valence and normative significance , 2011, Behavior research methods.

[38]  P. Fox,et al.  Segregation of the human medial prefrontal cortex in social cognition , 2013, Front. Hum. Neurosci..

[39]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[40]  S. W. Rieger,et al.  Learning Control Over Emotion Networks Through Connectivity‐Based Neurofeedback , 2015, Cerebral cortex.

[41]  Lawrence L. Wald,et al.  Physiological noise and signal-to-noise ratio in fMRI with multi-channel array coils , 2011, NeuroImage.

[42]  Francesco Fera,et al.  The Amygdala Response to Emotional Stimuli: A Comparison of Faces and Scenes , 2002, NeuroImage.

[43]  Robin I. M. Dunbar Social Brain Hypothesis , 1998, Encyclopedia of Evolutionary Psychological Science.

[44]  E. Holmes,et al.  Looking at or through rose-tinted glasses? Imagery perspective and positive mood. , 2008, Emotion.

[45]  Karl J. Friston,et al.  Comparing Families of Dynamic Causal Models , 2010, PLoS Comput. Biol..

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

[47]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[48]  P. Fletcher,et al.  Seeing other minds: attributed mental states influence perception , 2010, Trends in Cognitive Sciences.

[49]  Daniel Västfjäll,et al.  Positive feelings facilitate working memory and complex decision making among older adults , 2013, Cognition & emotion.

[50]  Dimitri Van De Ville,et al.  Connectivity-based neurofeedback: Dynamic causal modeling for real-time fMRI☆ , 2013, Neuroimage.

[51]  Dimitri Van De Ville,et al.  OpenNFT: An open-source Python/Matlab framework for real-time fMRI neurofeedback training based on activity, connectivity and multivariate pattern analysis , 2017, NeuroImage.

[52]  Daniel P. Kennedy,et al.  The social brain in psychiatric and neurological disorders , 2012, Trends in Cognitive Sciences.

[53]  R. Deichmann,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex: compensation of susceptibility-induced gradients in the readout direction , 2007, Magnetic Resonance Materials in Physics, Biology and Medicine.

[54]  Gerd Wagner,et al.  Fronto-cingulate effective connectivity in major depression: A study with fMRI and dynamic causal modeling , 2008, NeuroImage.

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

[56]  Kamryn T. Eddy,et al.  Amygdala-frontal connectivity during emotion regulation. , 2007, Social cognitive and affective neuroscience.

[57]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[58]  Jennifer A. Silvers,et al.  Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion , 2012, Annals of the New York Academy of Sciences.

[59]  Ingrid R. Olson,et al.  Converging evidence from fMRI and aphasia that the left temporoparietal cortex has an essential role in representing abstract semantic knowledge , 2015, Cortex.

[60]  D. Zald,et al.  Reconsidering anhedonia in depression: Lessons from translational neuroscience , 2011, Neuroscience & Biobehavioral Reviews.

[61]  Dana Samson,et al.  Left temporoparietal junction is necessary for representing someone else's belief , 2004, Nature Neuroscience.

[62]  D. Pizzagalli,et al.  Corticostriatal pathways contribute to the natural time course of positive mood , 2015, Nature Communications.

[63]  Karl-Jürgen Bär,et al.  The neural basis of the abnormal self‐referential processing and its impact on cognitive control in depressed patients , 2015, Human brain mapping.

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

[65]  O. John,et al.  Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. , 2003, Journal of personality and social psychology.

[66]  J. Gross,et al.  Cognitive Emotion Regulation , 2008, Current directions in psychological science.

[67]  Jarrod A. Lewis-Peacock,et al.  Closed-loop brain training: the science of neurofeedback , 2017, Nature Reviews Neuroscience.

[68]  A. Beck,et al.  An inventory for measuring depression. , 1961, Archives of general psychiatry.

[69]  J. Gross Emotion regulation: affective, cognitive, and social consequences. , 2002, Psychophysiology.

[70]  R. Malach,et al.  When the Brain Loses Its Self: Prefrontal Inactivation during Sensorimotor Processing , 2006, Neuron.

[71]  Karl J. Friston,et al.  Empirical Bayes for Group (DCM) Studies: A Reproducibility Study , 2015, Front. Hum. Neurosci..

[72]  Kevin N. Ochsner,et al.  The Social Regulation of Emotion: An Integrative, Cross-Disciplinary Model , 2016, Trends in Cognitive Sciences.

[73]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[74]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[75]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[76]  Klaus R. Scherer,et al.  Emotion as a process: Function, origin and regulation , 1982 .

[77]  Karl J. Friston,et al.  Network discovery with DCM , 2011, NeuroImage.

[78]  Ritesh Mistry,et al.  Relation between Emotion Regulation and Mental Health: A Meta-Analysis Review , 2014, Psychological reports.

[79]  C. Beevers,et al.  Neural mechanisms of the cognitive model of depression , 2011, Nature Reviews Neuroscience.

[80]  Karl J. Friston,et al.  Network discovery with large DCMs , 2013, NeuroImage.

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