Neural network of cognitive emotion regulation — An ALE meta-analysis and MACM analysis

Cognitive regulation of emotions is a fundamental prerequisite for intact social functioning which impacts on both well being and psychopathology. The neural underpinnings of this process have been studied intensively in recent years, without, however, a general consensus. We here quantitatively summarize the published literature on cognitive emotion regulation using activation likelihood estimation in fMRI and PET (23 studies/479 subjects). In addition, we assessed the particular functional contribution of identified regions and their interactions using quantitative functional inference and meta-analytic connectivity modeling, respectively. In doing so, we developed a model for the core brain network involved in emotion regulation of emotional reactivity. According to this, the superior temporal gyrus, angular gyrus and (pre) supplementary motor area should be involved in execution of regulation initiated by frontal areas. The dorsolateral prefrontal cortex may be related to regulation of cognitive processes such as attention, while the ventrolateral prefrontal cortex may not necessarily reflect the regulatory process per se, but signals salience and therefore the need to regulate. We also identified a cluster in the anterior middle cingulate cortex as a region, which is anatomically and functionally in an ideal position to influence behavior and subcortical structures related to affect generation. Hence this area may play a central, integrative role in emotion regulation. By focusing on regions commonly active across multiple studies, this proposed model should provide important a priori information for the assessment of dysregulated emotion regulation in psychiatric disorders.

[1]  R. Lazarus Psychological stress and the coping process , 1970 .

[2]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[3]  M. Wessa,et al.  How to regulate emotion? Neural networks for reappraisal and distraction. , 2011, Cerebral cortex.

[4]  Jin Fan,et al.  Neural Correlates of the Use of Psychological Distancing to Regulate Responses to Negative Social Cues: A Study of Patients with Borderline Personality Disorder , 2009, Biological Psychiatry.

[5]  P. Niedenthal,et al.  Embodiment of emotion concepts. , 2009, Journal of personality and social psychology.

[6]  J. Gross,et al.  The Neural Bases of Emotion Regulation: Reappraisal and Suppression of Negative Emotion , 2008, Biological Psychiatry.

[7]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[8]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[9]  Thomas E. Nichols,et al.  Image-based vs. Coordinate-based Meta-analysis , 2009, NeuroImage.

[10]  S. Petersen,et al.  Role of the anterior insula in task-level control and focal attention , 2010, Brain Structure and Function.

[11]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

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

[13]  M. Lindquist,et al.  Meta-analysis of functional neuroimaging data: current and future directions. , 2007, Social cognitive and affective neuroscience.

[14]  Simon B. Eickhoff,et al.  Crossmodal Interactions in Audiovisual Emotion Processing Veronika I. Studies of Audiovisual Integration Have Predominantly Assessed the Neural Correlates of Audiovisual Speech Perception (beauchamp Unimodal Emotional Processing in Turn Has Been Extensively Studied, with a High Proportion of Studies , 2022 .

[15]  R. Veit,et al.  Regulation of emotional responses elicited by threat‐related stimuli , 2007, Human brain mapping.

[16]  Joseph E LeDoux,et al.  Neural Circuitry Underlying the Regulation of Conditioned Fear and Its Relation to Extinction , 2008, Neuron.

[17]  K. Zilles,et al.  The "what" and "when" of self-initiated movements. , 2013, Cerebral cortex.

[18]  Angela R. Laird,et al.  Activation likelihood estimation meta-analysis revisited , 2012, NeuroImage.

[19]  Yufeng Zang,et al.  Sustained activity within the default mode network during an implicit memory task , 2010, Cortex.

[20]  M. Seghier,et al.  Functional Subdivisions in the Left Angular Gyrus Where the Semantic System Meets and Diverges from the Default Network , 2010, The Journal of Neuroscience.

[21]  Henrik Walter,et al.  The Temporal Dynamics of Voluntary Emotion Regulation , 2009, PloS one.

[22]  Carsten Spitzer,et al.  Cognitive reappraisal in trauma-exposed women with borderline personality disorder , 2012, NeuroImage.

[23]  J. Gross,et al.  Emotion Regulation and Mental Health , 1995 .

[24]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[25]  R. C. Gur,et al.  Gender differences in the neural correlates of humor processing: Implications for different processing modes , 2011, Neuropsychologia.

[26]  Katiuscia Sacco,et al.  Meta-analytic clustering of the insular cortex Characterizing the meta-analytic connectivity of the insula when involved in active tasks , 2012, NeuroImage.

[27]  A. Laird,et al.  The Neural Basis of Drug Stimulus Processing and Craving: An Activation Likelihood Estimation Meta-Analysis , 2011, Biological Psychiatry.

[28]  S. Schultz Principles of Neural Science, 4th ed. , 2001 .

[29]  Simon B. Eickhoff,et al.  Assignment of functional activations to probabilistic cytoarchitectonic areas revisited , 2007, NeuroImage.

[30]  Angela R. Laird,et al.  Is There “One” DLPFC in Cognitive Action Control? Evidence for Heterogeneity From Co-Activation-Based Parcellation , 2012, Cerebral cortex.

[31]  H. Barbas Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices , 2000, Brain Research Bulletin.

[32]  Jennifer S. Beer,et al.  Prefrontal involvement in the regulation of emotion: convergence of rat and human studies , 2006, Current Opinion in Neurobiology.

[33]  Kristin Prehn,et al.  Neuronal Correlates of Cognitive Reappraisal in Borderline Patients with Affective Instability , 2011, Biological Psychiatry.

[34]  Alan C. Evans,et al.  An MRI-Based Probabilistic Atlas of Neuroanatomy , 1994 .

[35]  A. Aleman,et al.  Individual differences in dispositional mindfulness and brain activity involved in reappraisal of emotion. , 2010, Social cognitive and affective neuroscience.

[36]  Murray B. Stein,et al.  Functioning of neural systems supporting emotion regulation in anxiety-prone individuals , 2011, NeuroImage.

[37]  M. Beauregard,et al.  Neural Correlates of Conscious Self-Regulation of Emotion , 2001, The Journal of Neuroscience.

[38]  Scott T. Grafton,et al.  A distributed left hemisphere network active during planning of everyday tool use skills. , 2004, Cerebral cortex.

[39]  Piotr Winkielman,et al.  Emotional Conception , 2009, Psychological science.

[40]  Christa Neuper,et al.  To retrieve or to calculate? Left angular gyrus mediates the retrieval of arithmetic facts during problem solving , 2009, Neuropsychologia.

[41]  Peter Falkai,et al.  Fear is only as deep as the mind allows A coordinate-based meta-analysis of neuroimaging studies on the regulation of negative affect , 2011, NeuroImage.

[42]  A. Damasio The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[43]  J. Weber,et al.  Prefrontal–striatal pathway underlies cognitive regulation of craving , 2010, Proceedings of the National Academy of Sciences.

[44]  R. Poldrack Inferring Mental States from Neuroimaging Data: From Reverse Inference to Large-Scale Decoding , 2011, Neuron.

[45]  Deanna M. Barch,et al.  When less is more: TPJ and default network deactivation during encoding predicts working memory performance , 2010, NeuroImage.

[46]  M. Phillips,et al.  A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder , 2008, Molecular Psychiatry.

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

[48]  John Duncan,et al.  The role of the right inferior frontal gyrus: inhibition and attentional control , 2010, NeuroImage.

[49]  Angela R. Laird,et al.  Investigating function and connectivity of morphometric findings — Exemplified on cerebellar atrophy in spinocerebellar ataxia 17 (SCA17) , 2012, NeuroImage.

[50]  Simon B Eickhoff,et al.  Brain structure anomalies in autism spectrum disorder—a meta‐analysis of VBM studies using anatomic likelihood estimation , 2012, Human brain mapping.

[51]  R. Lazarus Emotion and Adaptation , 1991 .

[52]  Simon B. Eickhoff,et al.  Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps , 2006, NeuroImage.

[53]  Tatia M.C. Lee,et al.  Sex-related differences in neural activity during emotion regulation , 2009, Neuropsychologia.

[54]  J. Price,et al.  Architectonic subdivision of the human orbital and medial prefrontal cortex , 2003, The Journal of comparative neurology.

[55]  Richard J. Davidson,et al.  Gaze fixations predict brain activation during the voluntary regulation of picture-induced negative affect , 2007, NeuroImage.

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

[57]  Kevin N. Ochsner,et al.  The Neural Bases of Distraction and Reappraisal , 2010, Journal of Cognitive Neuroscience.

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

[59]  J. Gross The Emerging Field of Emotion Regulation: An Integrative Review , 1998 .

[60]  D. Zald,et al.  Neuroscience and Biobehavioral Reviews Anatomical Insights into the Interaction of Emotion and Cognition in the Prefrontal Cortex , 2022 .

[61]  Heather L. Urry,et al.  Amygdala and Ventromedial Prefrontal Cortex Are Inversely Coupled during Regulation of Negative Affect and Predict the Diurnal Pattern of Cortisol Secretion among Older Adults , 2006, The Journal of Neuroscience.

[62]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

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

[64]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[65]  Danilo Bzdok,et al.  The BrainMap strategy for standardization, sharing, and meta-analysis of neuroimaging data , 2011, BMC Research Notes.

[66]  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.

[67]  Karin Ackermann,et al.  The Nature Of Emotion Fundamental Questions , 2016 .

[68]  Roberto Cabeza,et al.  Cognitive and neural contributors to emotion regulation in aging. , 2011, Social cognitive and affective neuroscience.

[69]  S. Rauch,et al.  Neurobiology of emotion perception I: the neural basis of normal emotion perception , 2003, Biological Psychiatry.

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

[71]  Carla L. Harenski,et al.  Neural correlates of regulating negative emotions related to moral violations , 2006, NeuroImage.

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

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

[74]  Brent L. Hughes,et al.  Supplemental Data Prefrontal-Subcortical Pathways Mediating Successful Emotion Regulation , 2008 .

[75]  Angela R. Laird,et al.  Co-activation patterns distinguish cortical modules, their connectivity and functional differentiation , 2011, NeuroImage.

[76]  Eliot R. Smith,et al.  Situated Social Cognition , 2007 .

[77]  Jessica A. Turner,et al.  Neuroinformatics Original Research Article , 2022 .

[78]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[79]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[80]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

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

[82]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[83]  K. Phan,et al.  Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

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

[85]  Markus Heinrichs,et al.  The neural correlates of sex differences in emotional reactivity and emotion regulation , 2009, Human brain mapping.

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

[87]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

[88]  Simon B Eickhoff,et al.  Minimizing within‐experiment and within‐group effects in activation likelihood estimation meta‐analyses , 2012, Human brain mapping.

[89]  L. Barsalou Grounded cognition. , 2008, Annual review of psychology.

[90]  Ross A. Thompson,et al.  Emotion regulation: Conceptual foundations , 2007 .

[91]  R. Kalisch The functional neuroanatomy of reappraisal: Time matters , 2009, Neuroscience & Biobehavioral Reviews.

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

[93]  K. Zilles,et al.  Differentiated parietal connectivity of frontal regions for “what” and “where” memory , 2012, Brain Structure and Function.

[94]  Angela R. Laird,et al.  Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: Validation of the Lancaster transform , 2010, NeuroImage.

[95]  Jessica A. Turner,et al.  The Cognitive Paradigm Ontology: Design and Application , 2011, Neuroinformatics.

[96]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[97]  G. McCarthy,et al.  Staying Cool when Things Get Hot: Emotion Regulation Modulates Neural Mechanisms of Memory Encoding , 2010, Front. Hum. Neurosci..

[98]  R. Davidson,et al.  Suppression and enhancement of emotional responses to unpleasant pictures. , 2000, Psychophysiology.

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

[100]  S. Haber Connectivity of Primate Reward Centers , 2009 .

[101]  J. Singer,et al.  Cognitive, social, and physiological determinants of emotional state. , 1962, Psychological review.

[102]  Joaquin M. Fuster,et al.  Proceedings of the Human Cerebral Cortex: From Gene to Structure and Function , 2000 .

[103]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[104]  P. Young,et al.  Emotion and personality , 1963 .