Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies.

In recent years, an explosion of neuroimaging studies has examined cognitive reappraisal, an emotion regulation strategy that involves changing the way one thinks about a stimulus in order to change its affective impact. Existing models broadly agree that reappraisal recruits frontal and parietal control regions to modulate emotional responding in the amygdala, but they offer competing visions of how this is accomplished. One view holds that control regions engage ventromedial prefrontal cortex (vmPFC), an area associated with fear extinction, that in turn modulates amygdala responses. An alternative view is that control regions modulate semantic representations in lateral temporal cortex that indirectly influence emotion-related responses in the amygdala. Furthermore, while previous work has emphasized the amygdala, whether reappraisal influences other regions implicated in emotional responding remains unknown. To resolve these questions, we performed a meta-analysis of 48 neuroimaging studies of reappraisal, most involving downregulation of negative affect. Reappraisal consistently 1) activated cognitive control regions and lateral temporal cortex, but not vmPFC, and 2) modulated the bilateral amygdala, but no other brain regions. This suggests that reappraisal involves the use of cognitive control to modulate semantic representations of an emotional stimulus, and these altered representations in turn attenuate activity in the amygdala.

[1]  M. Gazzaniga Handbook of Cognitive Neuroscience , 1984, Springer US.

[2]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[3]  W. Schultz,et al.  Neuronal activity in monkey ventral striatum related to the expectation of reward , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Gross Antecedent- and response-focused emotion regulation: divergent consequences for experience, expression, and physiology. , 1998, Journal of personality and social psychology.

[5]  Michael Davis,et al.  The amygdala , 2000, Current Biology.

[6]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[7]  J. Gabrieli,et al.  Event-Related Activation in the Human Amygdala Associates with Later Memory for Individual Emotional Experience , 2000, The Journal of Neuroscience.

[8]  E. Gordon,et al.  Arousal Dissociates Amygdala and Hippocampal Fear Responses: Evidence from Simultaneous fMRI and Skin Conductance Recording , 2001, NeuroImage.

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

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

[11]  K. Berridge,et al.  Fear and Feeding in the Nucleus Accumbens Shell: Rostrocaudal Segregation of GABA-Elicited Defensive Behavior Versus Eating Behavior , 2001, The Journal of Neuroscience.

[12]  K. Scherer,et al.  Appraisal processes in emotion: Theory, methods, research. , 2001 .

[13]  Richard W Briggs,et al.  Semantic monitoring of words with emotional connotation during fMRI: Contribution of anterior left frontal cortex , 2002, Journal of the International Neuropsychological Society.

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

[15]  K. Berridge,et al.  Positive and Negative Motivation in Nucleus Accumbens Shell: Bivalent Rostrocaudal Gradients for GABA-Elicited Eating, Taste “Liking”/“Disliking” Reactions, Place Preference/Avoidance, and Fear , 2002, The Journal of Neuroscience.

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

[17]  B. Mensour,et al.  Neural circuitry underlying voluntary suppression of sadness , 2003, Biological Psychiatry.

[18]  K. Berridge,et al.  Glutamate motivational ensembles in nucleus accumbens: rostrocaudal shell gradients of fear and feeding , 2003, The European journal of neuroscience.

[19]  J. Price Comparative Aspects of Amygdala Connectivity , 2003, Annals of the New York Academy of Sciences.

[20]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[21]  I. Fischler,et al.  Processing Words with Emotional Connotation: An fMRI Study of Time Course and Laterality in Rostral Frontal and Retrosplenial Cortices , 2004, Journal of Cognitive Neuroscience.

[22]  Jennifer C. Britton,et al.  Neural correlates of individual ratings of emotional salience: a trial-related fMRI study , 2004, NeuroImage.

[23]  William A. Cunningham,et al.  Implicit and Explicit Evaluation: fMRI Correlates of Valence, Emotional Intensity, and Control in the Processing of Attitudes , 2004, Journal of Cognitive Neuroscience.

[24]  H. Damasio,et al.  The Iowa Gambling Task and the somatic marker hypothesis: some questions and answers , 2005, Trends in Cognitive Sciences.

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

[26]  A. Beck The current state of cognitive therapy: a 40-year retrospective. , 2005, Archives of general psychiatry.

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

[28]  Joseph E LeDoux,et al.  Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior , 2005, Neuron.

[29]  M. Roitman,et al.  Nucleus Accumbens Neurons Are Innately Tuned for Rewarding and Aversive Taste Stimuli, Encode Their Predictors, and Are Linked to Motor Output , 2005, Neuron.

[30]  Gregory J. Quirk,et al.  Prefrontal Mechanisms in Extinction of Conditioned Fear , 2006, Biological Psychiatry.

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

[32]  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.

[33]  Atsushi Sato,et al.  Association of neural and physiological responses during voluntary emotion suppression , 2006, NeuroImage.

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

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

[36]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

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

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

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

[40]  S. Rauch,et al.  Recall of Fear Extinction in Humans Activates the Ventromedial Prefrontal Cortex and Hippocampus in Concert , 2007, Biological Psychiatry.

[41]  B. Mesquita,et al.  The experience of emotion. , 2007, Annual review of psychology.

[42]  Lutz Jäncke,et al.  Modulation of anticipatory emotion and perception processing by cognitive control , 2007, NeuroImage.

[43]  T. Robbins Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  R. Andrew Chambers,et al.  Network Modeling of Adult Neurogenesis: Shifting Rates of Neuronal Turnover Optimally Gears Network Learning according to Novelty Gradient , 2007, Journal of Cognitive Neuroscience.

[45]  Heather L. Urry,et al.  Failure to Regulate: Counterproductive Recruitment of Top-Down Prefrontal-Subcortical Circuitry in Major Depression , 2007, The Journal of Neuroscience.

[46]  Claus C. Hilgetag,et al.  Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala , 2007, NeuroImage.

[47]  Kevin N. Ochsner,et al.  The neural architecture of emotion regulation , 2007 .

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

[49]  M. Linehan,et al.  Dialectical behavior therapy for borderline personality disorder. , 2007, Annual review of clinical psychology.

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

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

[52]  Ethan Kross,et al.  Facilitating Adaptive Emotional Analysis: Distinguishing Distanced-Analysis of Depressive Experiences From Immersed-Analysis and Distraction , 2008, Personality & social psychology bulletin.

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

[54]  J. Pekar,et al.  Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent , 2008, Neuropsychologia.

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

[56]  M. Delgado,et al.  Regulating the expectation of reward via cognitive strategies , 2008, Nature Neuroscience.

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

[58]  Joseph E LeDoux,et al.  From Fear to Safety and Back: Reversal of Fear in the Human Brain , 2008, The Journal of Neuroscience.

[59]  K. Ochsner,et al.  The role of social cognition in emotion , 2008, Trends in Cognitive Sciences.

[60]  Derek G. V. Mitchell,et al.  Dissociable roles of medial orbitofrontal cortex in human operant extinction learning , 2008, NeuroImage.

[61]  Matthew L. Davidson,et al.  The neuroimaging of emotion. , 2008 .

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

[63]  M. Hayward Mentalization-based Treatment for Borderline Personality Disorder: A Practical Guide , 2008 .

[64]  Jin Fan,et al.  A Functional Magnetic Resonance Imaging Study of Deliberate Emotion Regulation in Resilience and Posttraumatic Stress Disorder , 2009, Biological Psychiatry.

[65]  Frank Van Overwalle,et al.  Understanding others' actions and goals by mirror and mentalizing systems: A meta-analysis , 2009, NeuroImage.

[66]  Ethan Kross,et al.  Coping with Emotions Past: The Neural Bases of Regulating Affect Associated with Negative Autobiographical Memories , 2009, Biological Psychiatry.

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

[68]  Psychodynamic Techniques: Working with Emotion in the Therapeutic Relationship , 2009 .

[69]  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.

[70]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[71]  Tatia M.C. Lee,et al.  Neural correlates of regulation of positive and negative emotions: An fMRI study , 2009, Neuroscience Letters.

[72]  B. Abler,et al.  Cognitive reappraisal modulates expected value and prediction error encoding in the ventral striatum , 2009, NeuroImage.

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

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

[75]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[76]  Axel Schäfer,et al.  Emotion regulation in spider phobia: role of the medial prefrontal cortex. , 2009, Social cognitive and affective neuroscience.

[77]  Richard J. Davidson,et al.  Individual differences in some (but not all) medial prefrontal regions reflect cognitive demand while regulating unpleasant emotion , 2009, NeuroImage.

[78]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[79]  Jin Fan,et al.  Neural correlates of using distancing to regulate emotional responses to social situations , 2010, Neuropsychologia.

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

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

[82]  Henrik Walter,et al.  Volition diminishes genetically mediated amygdala hyperreactivity , 2010, NeuroImage.

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

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

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

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

[87]  Heather L. Urry,et al.  Seeing, thinking, and feeling: emotion-regulating effects of gaze-directed cognitive reappraisal. , 2010, Emotion.

[88]  Mauricio R. Delgado,et al.  Overlapping neural systems mediating extinction, reversal and regulation of fear , 2010, Trends in Cognitive Sciences.

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

[90]  Hedy Kober,et al.  Meta-analysis of neuroimaging data. , 2010, Wiley interdisciplinary reviews. Cognitive science.

[91]  A. Kring,et al.  Emotion regulation and psychopathology : a transdiagnostic approach to etiology and treatment , 2010 .

[92]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[93]  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.

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

[95]  Danielle Z. Bolling,et al.  How grossed out are you? The neural bases of emotion regulation from childhood to adolescence , 2011, Developmental Cognitive Neuroscience.

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

[97]  M. J. Hannush Psychodynamic Techniques: Working with Emotion in the Therapeutic Relationship , 2011 .

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

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

[100]  H. Walter,et al.  Dorsolateral prefrontal cortex modulates striatal reward encoding during reappraisal of reward anticipation. , 2011, Cerebral cortex.

[101]  P. Vuilleumier,et al.  Effects of emotion regulation strategy on brain responses to the valence and social content of visual scenes , 2011, Neuropsychologia.

[102]  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.

[103]  Joan Y. Chiao,et al.  Look before you regulate: differential perceptual strategies underlying expressive suppression and cognitive reappraisal. , 2011, Emotion.

[104]  J. Gross,et al.  Feeling bad about screwing up: emotion regulation and action monitoring in the anterior cingulate cortex , 2011, Cognitive, affective & behavioral neuroscience.

[105]  Falk Eippert,et al.  Intentional social distance regulation alters affective responses towards victims of violence: An FMRI study , 2012, Human brain mapping.

[106]  Mastering Intensive Short-Term Dynamic Psychotherapy: A Roadmap to the Unconscious , 2012 .

[107]  Joshua Carp,et al.  On the Plurality of (Methodological) Worlds: Estimating the Analytic Flexibility of fMRI Experiments , 2012, Front. Neurosci..

[108]  Heather L. Urry,et al.  Prefrontal mediation of age differences in cognitive reappraisal , 2012, Neurobiology of Aging.

[109]  Michael Erb,et al.  Where in the brain is nonliteral language? A coordinate-based meta-analysis of functional magnetic resonance imaging studies , 2012, NeuroImage.

[110]  James J Gross,et al.  Bottom-up and top-down emotion generation: implications for emotion regulation. , 2012, Social cognitive and affective neuroscience.

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

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

[113]  Martin P Paulus,et al.  Amygdala response and functional connectivity during emotion regulation: a study of 14 depressed adolescents. , 2012, Journal of affective disorders.

[114]  Philipp Kanske,et al.  Neural correlates of emotion regulation deficits in remitted depression: The influence of regulation strategy, habitual regulation use, and emotional valence , 2012, NeuroImage.

[115]  Tobias Brosch,et al.  Motivational Salience , 2012 .

[116]  Nalini Ambady,et al.  How does the brain regulate negative bias to stigma? , 2012, Social cognitive and affective neuroscience.

[117]  J. Gabrieli,et al.  The development of emotion regulation: an fMRI study of cognitive reappraisal in children, adolescents and young adults. , 2012, Social cognitive and affective neuroscience.

[118]  Joshua Carp,et al.  The secret lives of experiments: Methods reporting in the fMRI literature , 2012, NeuroImage.

[119]  Jamil Zaki,et al.  Overlapping activity in anterior insula during interoception and emotional experience , 2012, NeuroImage.

[120]  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.

[121]  A. Villringer,et al.  Neural correlates of the volitional regulation of the desire for food , 2011, International Journal of Obesity.

[122]  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.

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

[124]  Brent L. Hughes,et al.  Common representation of pain and negative emotion in the midbrain periaqueductal gray. , 2013, Social cognitive and affective neuroscience.

[125]  Colin F Camerer,et al.  Emotion regulation reduces loss aversion and decreases amygdala responses to losses. , 2013, Social cognitive and affective neuroscience.

[126]  A. Sanfey,et al.  Reappraising the ultimatum: an fMRI study of emotion regulation and decision making. , 2013, Cerebral cortex.

[127]  A. Sanfey,et al.  Living Emotions, Avoiding Emotions: Behavioral Investigation of the Regulation of Socially Driven Emotions , 2013, Front. Psychology.

[128]  K. Ochsner,et al.  The Neuroscience of Emotion Regulation , 2013 .

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

[130]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[131]  Mastering intensive short-term dynamic psychotherapy, a roadmap to the unconscious , 2014 .

[132]  K. Miyazaki,et al.  Nucleus accumbens , 2018, Radiopaedia.org.