Increased Global Interaction Across Functional Brain Modules During Cognitive Emotion Regulation

Cognitive emotion regulation (CER) enables humans to flexibly modulate their emotions. While local theories of CER neurobiology suggest interactions between specialized local brain circuits underlying CER, e.g., in subparts of amygdala and medial prefrontal cortices (mPFC), global theories hypothesize global interaction increases among larger functional brain modules comprising local circuits. We tested the global CER hypothesis using graph-based whole-brain network analysis of functional MRI data during aversive emotional processing with and without CER. During CER, global between-module interaction across stable functional network modules increased. Global interaction increase was particularly driven by subregions of amygdala and cuneus-nodes of highest nodal participation-that overlapped with CER-specific local activations, and by mPFC and posterior cingulate as relevant connector hubs. Results provide evidence for the global nature of human CER, complementing functional specialization of embedded local brain circuits during successful CER.

[1]  Justin L. Vincent,et al.  Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[2]  Ludmila I. Kuncheva,et al.  Using diversity in cluster ensembles , 2004, 2004 IEEE International Conference on Systems, Man and Cybernetics (IEEE Cat. No.04CH37583).

[3]  Wenhai Zhang,et al.  Positive and negative affective processing exhibit dissociable functional hubs during the viewing of affective pictures , 2015, Human brain mapping.

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

[5]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[6]  Marie T Banich,et al.  Flexible brain network reconfiguration supporting inhibitory control , 2015, Proceedings of the National Academy of Sciences.

[7]  Lisa Feldman Barrett,et al.  The Future of Psychology Connecting Mind to Brain , 2009 .

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

[9]  S.,et al.  An Efficient Heuristic Procedure for Partitioning Graphs , 2022 .

[10]  James J. Gross,et al.  Handbook of emotion regulation , 2007 .

[11]  Karthik Ramakrishnan Sreenivasan,et al.  Threat-related learning relies on distinct dorsal prefrontal cortex network connectivity , 2014, NeuroImage.

[12]  Daniella J. Furman,et al.  Functional neuroimaging of major depressive disorder: a meta-analysis and new integration of base line activation and neural response data. , 2012, The American journal of psychiatry.

[13]  N. Meiran,et al.  Divergent cognitive costs for online forms of reappraisal and distraction. , 2008, Emotion.

[14]  H. Mayberg Limbic-cortical dysregulation: a proposed model of depression. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[15]  J. P. Hamilton,et al.  Amygdala volume in major depressive disorder: a meta-analysis of magnetic resonance imaging studies , 2008, Molecular Psychiatry.

[16]  E. Bullmore,et al.  Behavioral / Systems / Cognitive Functional Connectivity and Brain Networks in Schizophrenia , 2010 .

[17]  T. Yarkoni Big Correlations in Little Studies: Inflated fMRI Correlations Reflect Low Statistical Power—Commentary on Vul et al. (2009) , 2009, Perspectives on psychological science : a journal of the Association for Psychological Science.

[18]  P. Fox,et al.  Metaanalytic connectivity modeling: Delineating the functional connectivity of the human amygdala , 2009, Human brain mapping.

[19]  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.

[20]  H. Walter,et al.  Acute and Sustained Effects of Cognitive Emotion Regulation in Major Depression , 2010, The Journal of Neuroscience.

[21]  Noah D. Brenowitz,et al.  Whole-brain, time-locked activation with simple tasks revealed using massive averaging and model-free analysis , 2012, Proceedings of the National Academy of Sciences.

[22]  Valentin Riedl,et al.  Cognitive emotion regulation enhances aversive prediction error activity while reducing emotional responses , 2015, NeuroImage.

[23]  J. Gabrieli,et al.  Gender Differences in Emotion Regulation: An fMRI Study of Cognitive Reappraisal , 2008, Group processes & intergroup relations : GPIR.

[24]  Sterling C. Johnson,et al.  A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches , 2012, NeuroImage.

[25]  Chenwang Jin,et al.  A preliminary study of the dysregulation of the resting networks in first-episode medication-naive adolescent depression , 2011, Neuroscience Letters.

[26]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

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

[28]  M E J Newman,et al.  Community structure in social and biological networks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Brent L. Hughes,et al.  Prefrontal-Subcortical Pathways Mediating Successful Emotion Regulation , 2008, Neuron.

[30]  M. Mintun,et al.  The default mode network and self-referential processes in depression , 2009, Proceedings of the National Academy of Sciences.

[31]  David W. Frank,et al.  Emotion regulation: Quantitative meta-analysis of functional activation and deactivation , 2014, Neuroscience & Biobehavioral Reviews.

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

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

[34]  M E J Newman,et al.  Fast algorithm for detecting community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[35]  N. Canteras,et al.  The many paths to fear , 2012, Nature Reviews Neuroscience.

[36]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

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

[38]  R. Guimerà,et al.  The worldwide air transportation network: Anomalous centrality, community structure, and cities' global roles , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[40]  Barry Horwitz,et al.  The Functional Connectome of Speech Control , 2015, PLoS biology.

[41]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[42]  Christine D. Wilson-Mendenhall,et al.  A psychological construction account of emotion regulation and dysregulation: the role of situated conceptualizations , 2013 .

[43]  P. Lang International Affective Picture System (IAPS) : Technical Manual and Affective Ratings , 1995 .

[44]  M. Cabanac What is emotion? , 2002, Behavioural Processes.

[45]  R. Adolphs Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1997 .

[46]  M E J Newman,et al.  Modularity and community structure in networks. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[47]  J. Fodor The Modularity of mind. An essay on faculty psychology , 1986 .

[48]  M. Thase,et al.  Can’t shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals , 2002, Biological Psychiatry.

[49]  J. Fodor The Modularity of mind. An essay on faculty psychology , 1986 .

[50]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

[51]  Keith Bush,et al.  A comparison of statistical methods for detecting context-modulated functional connectivity in fMRI , 2014, NeuroImage.

[52]  J. P. Hamilton,et al.  Anomalous Gray Matter Structural Networks in Major Depressive Disorder , 2013, Biological Psychiatry.

[53]  Robert L. Barry,et al.  Breakdown of the brain’s functional network modularity with awareness , 2015, Proceedings of the National Academy of Sciences.

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

[55]  Junming Shao,et al.  Aberrant topology of striatum's connectivity is associated with the number of episodes in depression. , 2014, Brain : a journal of neurology.

[56]  H. Pollard,et al.  Network science and the human brain: Using graph theory to understand the brain and one of its hubs, the amygdala, in health and disease , 2016, Journal of neuroscience research.

[57]  James J. Gross,et al.  Emotion Generation and Emotion Regulation: One or Two Depends on Your Point of View , 2011, Emotion review : journal of the International Society for Research on Emotion.

[58]  Danielle S Bassett,et al.  Brain graphs: graphical models of the human brain connectome. , 2011, Annual review of clinical psychology.

[59]  Michael Angstadt,et al.  Volitional regulation of emotions produces distributed alterations in connectivity between visual, attention control, and default networks , 2014, NeuroImage.

[60]  John H Krystal,et al.  Subtype-specific alterations of gamma-aminobutyric acid and glutamate in patients with major depression. , 2004, Archives of general psychiatry.

[61]  L. Swanson,et al.  What is the amygdala? , 1998, Trends in Neurosciences.

[62]  Stefan Koelsch,et al.  Functional centrality of amygdala, striatum and hypothalamus in a “small‐world” network underlying joy: An fMRI study with music , 2014, Human brain mapping.

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

[64]  P. Koolschijn,et al.  Brain volume abnormalities in major depressive disorder: a Meta-analysis of magnetic resonance imaging studies , 2009, NeuroImage.

[65]  B. Biswal,et al.  Functional connectivity of human striatum: a resting state FMRI study. , 2008, Cerebral cortex.

[66]  L. Pessoa,et al.  Network Analysis Reveals Increased Integration during Emotional and Motivational Processing , 2012, The Journal of Neuroscience.

[67]  N. Sadato,et al.  Brain regions involved in verbal or non‐verbal aspects of facial emotion recognition , 2000, Neuroreport.

[68]  Danilo Bzdok,et al.  Medial Prefrontal Aberrations in Major Depressive Disorder Revealed by Cytoarchitectonically Informed Voxel-Based Morphometry. , 2016, The American journal of psychiatry.

[69]  A. McDonald Cortical pathways to the mammalian amygdala , 1998, Progress in Neurobiology.

[70]  R. Guimerà,et al.  Functional cartography of complex metabolic networks , 2005, Nature.

[71]  Jennifer A. Silvers,et al.  Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. , 2014, Cerebral cortex.

[72]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[73]  Q. Gong,et al.  Depression, Neuroimaging and Connectomics: A Selective Overview , 2015, Biological Psychiatry.

[74]  J. Fodor,et al.  The Modularity of Mind: An Essay on Faculty Psychology , 1984 .

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

[76]  M. Weissman,et al.  Cortical thinning in persons at increased familial risk for major depression , 2009, Proceedings of the National Academy of Sciences.

[77]  Edward T. Bullmore,et al.  Neuroinformatics Original Research Article , 2022 .

[78]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

[79]  T. Prescott,et al.  The brainstem reticular formation is a small-world, not scale-free, network , 2006, Proceedings of the Royal Society B: Biological Sciences.

[80]  Roger Guimerà,et al.  Cartography of complex networks: modules and universal roles , 2005, Journal of statistical mechanics.

[81]  Peter Kirsch,et al.  Analyzing task‐dependent brain network changes by whole‐brain psychophysiological interactions: A comparison to conventional analysis , 2014, Human brain mapping.

[82]  Brian A. Nosek,et al.  Power failure: why small sample size undermines the reliability of neuroscience , 2013, Nature Reviews Neuroscience.