The conscious processing of emotion in depression disorder: a meta-analysis of neuroimaging studies

Background Depression is generally accompanied by a disturbed conscious processing of emotion, which manifests as a negative bias to facial/voice emotion information and a decreased accuracy in emotion recognition tasks. Several studies have proved that abnormal brain activation was responsible for the deficit function of conscious emotion recognition in depression. However, the altered brain activation related to the conscious processing of emotion in depression was incongruent among studies. Therefore, we conducted an activation likelihood estimation (ALE) analysis to better understand the underlying neurophysiological mechanism of conscious processing of emotion in depression. Method Electronic databases were searched using the search terms “depression,” “emotion recognition,” and “neuroimaging” from inceptions to April 10th, 2023. We retrieved trials which explored the neuro-responses of depressive patients to explicit emotion recognition tasks. Two investigators independently performed literature selection, data extraction, and risk of bias assessment. The spatial consistency of brain activation in conscious facial expressions recognition was calculated using ALE. The robustness of the results was examined by Jackknife sensitivity analysis. Results We retrieved 11,365 articles in total, 28 of which were included. In the overall analysis, we found increased activity in the middle temporal gyrus, superior temporal gyrus, parahippocampal gyrus, and cuneus, and decreased activity in the superior temporal gyrus, inferior parietal lobule, insula, and superior frontal gyrus. In response to positive stimuli, depressive patients showed hyperactivity in the medial frontal gyrus, middle temporal gyrus, and insula (uncorrected p < 0.001). When receiving negative stimuli, a higher activation was found in the precentral gyrus, middle frontal gyrus, precuneus, and superior temporal gyrus (uncorrected p < 0.001). Conclusion Among depressive patients, a broad spectrum of brain areas was involved in a deficit of conscious emotion processing. The activation of brain regions was different in response to positive or negative stimuli. Due to potential clinical heterogeneity, the findings should be treated with caution. Systematic review registration https://inplasy.com/inplasy-2022-11-0057/, identifier: 2022110057.

[1]  Katia M. Harlé,et al.  How Obstructed Action Efficacy Impacts Reward-based Decision-making in Adolescent Depression: An fMRI Study. , 2023, Journal of the American Academy of Child and Adolescent Psychiatry.

[2]  G. Juckel,et al.  Daring to feel: Emotion-focused psychotherapy increases amygdala activation and connectivity in euthymic bipolar disorder. A randomized controlled trial. , 2023, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[3]  E. Forbes,et al.  Splitting the reward: Differences in inflammatory marker associations with neural connectivity between reward anticipation and reward outcome in adolescents at high risk for depression. , 2023, Journal of affective disorders.

[4]  Wenbin Guo,et al.  Associations between abnormal spontaneous neural activity and clinical variables, eye movements, and event-related potential indicators in major depressive disorder , 2023, Frontiers in Neuroscience.

[5]  X. Lei,et al.  Functional connectivity between dorsal attention and default mode networks mediates subjective sleep duration and depression in young females. , 2023, Journal of affective disorders.

[6]  Q. Gong,et al.  Neural correlates of neuroticism: A coordinate-based meta-analysis of resting-state functional brain imaging studies , 2023, Neuroscience & Biobehavioral Reviews.

[7]  Katherine S. F. Damme,et al.  Association between reward-related functional connectivity and tri-level mood and anxiety symptoms , 2023, NeuroImage: Clinical.

[8]  Luoyu Wang,et al.  Alteration of whole-brain amplitude of low-frequency fluctuation and degree centrality in patients with mild to moderate depression: A resting-state functional magnetic resonance imaging study , 2022, Frontiers in Psychiatry.

[9]  Shaojia Lu,et al.  Aberrant interhemispheric functional connectivity in major depressive disorder with and without anhedonia , 2022, BMC Psychiatry.

[10]  Zenas C. Chao,et al.  Altered coordination between frontal delta and parietal alpha networks underlies anhedonia and depressive rumination in major depressive disorder , 2022, Journal of psychiatry & neuroscience : JPN.

[11]  A. Sattar,et al.  Effects of Parental Internalizing and Externalizing Behavior Problems on Children’s Limbic Brain Structures—An MRI Study , 2022, Brain sciences.

[12]  A. Sawa,et al.  Anterior Insula-Associated Social Novelty Recognition: Pivotal Roles of a Local Retinoic Acid Cascade and Oxytocin Signaling. , 2022, The American journal of psychiatry.

[13]  Karina M Quevedo,et al.  Neural Activity Associated with Symptoms Change in Depressed Adolescents following Self-Processing Neurofeedback , 2022, Brain sciences.

[14]  Yi Jin,et al.  Disrupted Spontaneous Neural Activity and Its Interaction With Pain and Emotion in Temporomandibular Disorders , 2022, Frontiers in Neuroscience.

[15]  Jordan E. Pierce,et al.  Explicit and Implicit Emotion Processing in the Cerebellum: A Meta-analysis and Systematic Review , 2022, The Cerebellum.

[16]  Jie Lu,et al.  Distinct patterns of functional brain network integration between treatment-resistant depression and non treatment-resistant depression: A resting-state functional magnetic resonance imaging study , 2022, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[17]  Jingping Shi,et al.  Correlation between cognitive deficits and dorsolateral prefrontal cortex functional connectivity in first-episode depression. , 2022, Journal of affective disorders.

[18]  Bo Xiang,et al.  Altered spontaneous brain activity in major depressive disorder: An activation likelihood estimation meta-analysis. , 2022, Journal of affective disorders.

[19]  Zhiyuan Liu,et al.  Neural mechanisms underlying the processing of emotional stimuli in individuals with depression: An ALE meta-analysis study , 2022, Psychiatry Research.

[20]  Q. Gong,et al.  COVID‐19 vicarious traumatization links functional connectome to general distress , 2022, NeuroImage.

[21]  S. Ng,et al.  Automatic diagnosis of late-life depression by 3D convolutional neural networks and cross-sample Entropy analysis from resting-state fMRI , 2022, Brain Imaging and Behavior.

[22]  Ying Wang,et al.  Neural correlates of negative emotion processing in subthreshold depression , 2022, Social cognitive and affective neuroscience.

[23]  B. Jobst,et al.  Modulation of Emotion Perception via Amygdala Stimulation in Humans , 2022, Frontiers in Neuroscience.

[24]  Q. Gong,et al.  Patterns of a structural covariance network associated with dispositional optimism during late adolescence , 2022, NeuroImage.

[25]  D. Mier,et al.  Effective connectivity of the human mirror neuron system during social cognition , 2022, Social cognitive and affective neuroscience.

[26]  Global, regional, and national burden of 12 mental disorders in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019 , 2022, The lancet. Psychiatry.

[27]  Huafu Chen,et al.  Negative bias effects during audiovisual emotional processing in major depression disorder , 2021, Human brain mapping.

[28]  Maarten J. Vaessen,et al.  Decoding the difference between explicit and implicit body expression representation in high level visual, prefrontal and inferior parietal cortex , 2021, NeuroImage.

[29]  M. Clark,et al.  Persistent depressive symptoms during COVID-19: a national, population-representative, longitudinal study of U.S. adults , 2021, The Lancet Regional Health - Americas.

[30]  B. Czéh,et al.  Childhood maltreatment results in altered deactivation of reward processing circuits in depressed patients: A functional magnetic resonance imaging study of a facial emotion recognition task , 2021, Neurobiology of Stress.

[31]  Huafu Chen,et al.  Prefrontal-limbic-striatum dysconnectivity associated with negative emotional endophenotypes in bipolar disorder during depressive episodes. , 2021, Journal of affective disorders.

[32]  Meijuan Li,et al.  The correlation of facial emotion recognition in patients with drug-naïve depression and suicide ideation. , 2021, Journal of affective disorders.

[33]  Michael T. Moore,et al.  Facial emotion recognition in major depressive disorder: A meta-analytic review. , 2021, Journal of affective disorders.

[34]  Qiyong Gong,et al.  Artificial intelligence applications in psychoradiology , 2021, Psychoradiology.

[35]  Biyu J. He,et al.  Cortical and subcortical signatures of conscious object recognition , 2021, Nature Communications.

[36]  R. Kessler,et al.  The Economic Burden of Adults with Major Depressive Disorder in the United States (2010 and 2018) , 2021, PharmacoEconomics.

[37]  E. Mayo-Wilson,et al.  The PRISMA 2020 statement: an updated guideline for reporting systematic reviews , 2021, BMJ.

[38]  Lyon Ka,et al.  Associations between Facets and Aspects of Big Five Personality and Affective Disorders:A Systematic Review and Best Evidence Synthesis. , 2021, Journal of affective disorders.

[39]  P. Courtet,et al.  I Cannot Read Your Eye Expression: Suicide Attempters Have Difficulties in Interpreting Complex Social Emotions , 2020, Frontiers in Psychiatry.

[40]  Miao Liu,et al.  Health-Related Quality of Life and Its Correlation With Depression Among Chinese Centenarians , 2020, Frontiers in Public Health.

[41]  J. Rothwell,et al.  Influence of theta-burst transcranial magnetic stimulation over the dorsolateral prefrontal cortex on emotion processing in healthy volunteers , 2020, Cognitive, Affective, & Behavioral Neuroscience.

[42]  S. Galea,et al.  Prevalence of Depression Symptoms in US Adults Before and During the COVID-19 Pandemic , 2020, JAMA network open.

[43]  Junjing Wang,et al.  Abnormal neural activities in adults and youths with major depressive disorder during emotional processing: a meta-analysis , 2020, Brain Imaging and Behavior.

[44]  F. d’Oleire Uquillas,et al.  Negative Impact of Sadness on Response Inhibition in Females: An Explicit Emotional Stop Signal Task fMRI Study , 2020, Frontiers in Behavioral Neuroscience.

[45]  Thomas A. W. Bolton,et al.  Triple Network Model Dynamically Revisited: Lower Salience Network State Switching in Pre-psychosis , 2020, Frontiers in Physiology.

[46]  E. Salmon,et al.  Impaired explicit self-awareness but preserved behavioral regulation in patients with Alzheimer disease , 2019, Aging & mental health.

[47]  Q. Hu,et al.  Delineating functional segregations of the human middle temporal gyrus with resting‐state functional connectivity and coactivation patterns , 2019, Human brain mapping.

[48]  Doug Hyun Han,et al.  Investigation of an emotion perception test using functional magnetic resonance imaging , 2019, Comput. Methods Programs Biomed..

[49]  Zar Nawab Khan Swati,et al.  Investigating executive control network and default mode network dysfunction in major depressive disorder , 2019, Neuroscience Letters.

[50]  G. O’Callaghan,et al.  Reward Processing in Adolescent Depression Across Neuroimaging Modalities. , 2019, Zeitschrift fur Kinder- und Jugendpsychiatrie und Psychotherapie.

[51]  M. Catalina Camacho,et al.  Neural architecture supporting active emotion processing in children: A multivariate approach , 2019, NeuroImage.

[52]  R. Saxe,et al.  Parts‐based representations of perceived face movements in the superior temporal sulcus , 2019, Human brain mapping.

[53]  Claudio Gentili,et al.  ROI and phobias: The effect of ROI approach on an ALE meta‐analysis of specific phobias , 2018, Human brain mapping.

[54]  M. Erb,et al.  Neural correlates of processing emotional prosody in unipolar depression , 2018, Human brain mapping.

[55]  G. Yovel,et al.  An Integrated Neural Framework for Dynamic and Static Face Processing , 2018, Scientific Reports.

[56]  D. Bezmaternykh,et al.  fMRI Responses in Healthy Individuals and in Patients with Mild Depression to Presentation of Pleasant and Unpleasant Images , 2018, Bulletin of Experimental Biology and Medicine.

[57]  Katja Koelkebeck,et al.  Emotion recognition from faces with in- and out-group features in patients with depression. , 2018, Journal of affective disorders.

[58]  J. Qiu,et al.  Emotion-related brain structures associated with trait creativity in middle children , 2017, Neuroscience Letters.

[59]  Kendrick Kay,et al.  The Functional Neuroanatomy of Human Face Perception. , 2017, Annual review of vision science.

[60]  Hakwan Lau,et al.  Domain-General and Domain-Specific Patterns of Activity Supporting Metacognition in Human Prefrontal Cortex , 2018, The Journal of Neuroscience.

[61]  V. Arolt,et al.  Differential Abnormal Pattern of Anterior Cingulate Gyrus Activation in Unipolar and Bipolar Depression: an fMRI and Pattern Classification Approach , 2017, Neuropsychopharmacology.

[62]  B. de Gelder,et al.  How white and black bodies are perceived depends on what emotion is expressed , 2017, Scientific Reports.

[63]  Senichiro Kikuchi,et al.  Persistent complex bereavement disorder: clinical utility and classification of the category proposed for Diagnostic and Statistical Manual of Mental Disorders, 5th edition , 2017, Psychogeriatrics : the official journal of the Japanese Psychogeriatric Society.

[64]  Qiyong Gong,et al.  Psychoradiology: The Frontier of Neuroimaging in Psychiatry. , 2016, Radiology.

[65]  Yi Cai,et al.  The characteristics of brain function activity between patients with bipolar depression and major depressive disorder: a functional magnetic resonance imaging study of affective pictures task , 2016 .

[66]  Jason S. Nomi,et al.  Dynamic functional network connectivity reveals unique and overlapping profiles of insula subdivisions , 2016, Human brain mapping.

[67]  H. Heinze,et al.  Implicit and explicit processing of emotional facial expressions in Parkinson’s disease , 2016, Behavioural Brain Research.

[68]  Jeffrey S. Anderson,et al.  A failure of suppression within the default mode network in depressed adolescents with compulsive internet game play. , 2016, Journal of affective disorders.

[69]  Wolfram Schultz,et al.  Dopamine reward prediction-error signalling: a two-component response , 2016, Nature Reviews Neuroscience.

[70]  Colm G. Connolly,et al.  Fusiform Gyrus Dysfunction is Associated with Perceptual Processing Efficiency to Emotional Faces in Adolescent Depression: A Model-Based Approach , 2016, Front. Psychol..

[71]  Yuejia Luo,et al.  The Core Neural Mechanisms underlying Depression Disorder: A Meta-analysis of fMRI Studies , 2015 .

[72]  J. P. Hamilton,et al.  Meta-analysis of Functional Neuroimaging of Major Depressive Disorder in Youth. , 2015, JAMA psychiatry.

[73]  N. Skokauskas,et al.  The role of sexual abuse on functional neuroimaging markers associated with major depressive disorder , 2015, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[74]  Yong He,et al.  Interactions between the Salience and Default-Mode Networks Are Disrupted in Cocaine Addiction , 2015, The Journal of Neuroscience.

[75]  S. Langenecker,et al.  Age and gender modulate the neural circuitry supporting facial emotion processing in adults with major depressive disorder. , 2015, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

[76]  M. Phillips,et al.  Regulation of neural responses to emotion perception by ketamine in individuals with treatment-resistant major depressive disorder , 2015, Translational Psychiatry.

[77]  M. Goldacre,et al.  Risk of self-harm and suicide in people with specific psychiatric and physical disorders: comparisons between disorders using English national record linkage , 2014, Journal of the Royal Society of Medicine.

[78]  Weina Zhang,et al.  The neural correlates of reward-related processing in major depressive disorder: a meta-analysis of functional magnetic resonance imaging studies. , 2013, Journal of affective disorders.

[79]  M. Bar,et al.  The role of the parahippocampal cortex in cognition , 2013, Trends in Cognitive Sciences.

[80]  Yan Wang,et al.  Abnormal activation of the occipital lobes during emotion picture processing in major depressive disorder patients , 2013, Neural regeneration research.

[81]  Jia Liu,et al.  The Hierarchical Brain Network for Face Recognition , 2013, PloS one.

[82]  J. Meaney,et al.  Recruitment of the left hemispheric emotional attention neural network in risk for and protection from depression. , 2013, Journal of psychiatry & neuroscience : JPN.

[83]  S. Costafreda,et al.  Emotional valence modulates brain functional abnormalities in depression: Evidence from a meta-analysis of fMRI studies , 2013, Neuroscience & Biobehavioral Reviews.

[84]  Qing Lu,et al.  Impaired prefrontal–amygdala effective connectivity is responsible for the dysfunction of emotion process in major depressive disorder: A dynamic causal modeling study on MEG , 2012, Neuroscience Letters.

[85]  Wang Xiang,et al.  Elevated amygdala activity to negative faces in young adults with early onset major depressive disorder , 2012, Psychiatry Research: Neuroimaging.

[86]  M. Schlund,et al.  Generalized anxiety modulates frontal and limbic activation in major depression , 2012, Behavioral and Brain Functions.

[87]  P. Falkai,et al.  Common and distinct neural correlates of emotional processing in Bipolar Disorder and Major Depressive Disorder: A voxel-based meta-analysis of functional magnetic resonance imaging studies , 2012, European Neuropsychopharmacology.

[88]  Udo Dannlowski,et al.  Facial emotion processing in major depression: a systematic review of neuroimaging findings , 2011, Biology of Mood & Anxiety Disorders.

[89]  V. Menon Large-scale brain networks and psychopathology: a unifying triple network model , 2011, Trends in Cognitive Sciences.

[90]  U. Habel,et al.  Neural correlates of social approach and withdrawal in patients with major depression , 2011, Social neuroscience.

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

[92]  R. Cabeza,et al.  Neural correlates of emotional processing in depression: changes with cognitive behavioral therapy and predictors of treatment response. , 2011, Journal of Psychiatric Research.

[93]  J. Buitelaar,et al.  Neural basis of emotion recognition deficits in first-episode major depression , 2010, Psychological Medicine.

[94]  P. de Jonge,et al.  Presence of individual (residual) symptoms during depressive episodes and periods of remission: a 3-year prospective study , 2010, Psychological Medicine.

[95]  Catherine A. Sugar,et al.  fMRI activation in the amygdala and the orbitofrontal cortex in unmedicated subjects with major depressive disorder , 2010, Psychiatry Research: Neuroimaging.

[96]  H. Möller,et al.  Orbitofrontal volume reductions during emotion recognition in patients with major depression. , 2010, Journal of psychiatry & neuroscience : JPN.

[97]  A. Stang Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses , 2010, European Journal of Epidemiology.

[98]  T. Singer,et al.  The role of anterior insular cortex in social emotions , 2010, Brain Structure and Function.

[99]  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.

[100]  Margaret A. Sheridan,et al.  A Review of Adversity, The Amygdala and the Hippocampus: A Consideration of Developmental Timing , 2009, Front. Hum. Neurosci..

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

[102]  B. Dubois,et al.  Functions of the left superior frontal gyrus in humans: a lesion study. , 2006, Brain : a journal of neurology.

[103]  Michael G. Hardin,et al.  Triadic model of the neurobiology of motivated behavior in adolescence , 2005, Psychological Medicine.

[104]  D. Zald The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[105]  Yan-Fang Chen,et al.  Chinese Classification of Mental Disorders (CCMD-3): Towards Integration in International Classification , 2002, Psychopathology.

[106]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[107]  H. Critchley,et al.  Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study , 2000, Human brain mapping.

[108]  E. Leibenluft,et al.  Brain Mechanisms of Attention Orienting Following Frustration: Associations With Irritability and Age in Youths. , 2019, The American journal of psychiatry.

[109]  Qiang Li,et al.  Disrupted coupling of large-scale networks is associated with relapse behaviour in heroin-dependent men. , 2018, Journal of psychiatry & neuroscience : JPN.

[110]  Richard J Porter,et al.  Brain activation during processing of genuine facial emotion in depression: Preliminary findings. , 2018, Journal of affective disorders.

[111]  P. Fox,et al.  Altered Brain Activity in Unipolar Depression Revisited: Meta-analyses of Neuroimaging Studies , 2017, JAMA psychiatry.

[112]  Chien-Han Lai Patterns of cortico-limbic activations during visual processing of sad faces in depression patients: a coordinate-based meta-analysis. , 2014, The Journal of neuropsychiatry and clinical neurosciences.

[113]  Gregory G. Brown,et al.  Adolescents with major depression demonstrate increased amygdala activation. , 2010, Journal of the American Academy of Child and Adolescent Psychiatry.

[114]  Zhening Liu,et al.  [Diffusion tensor imaging and resting state functional magnetic resonance imaging on young patients with major depressive disorder]. , 2010, Zhong nan da xue xue bao. Yi xue ban = Journal of Central South University. Medical sciences.

[115]  Kin-yin. Mak,et al.  Neural bases of emotion regulation , 2009 .

[116]  Cao Yan Neural Substrates for Explicit Recognition of Dynamic Facial Expressions in Male Patients with Major Depressive Disorder:a fMRI Study , 2008 .

[117]  Implementation of the International Statistical Classification of Diseases and Related Health Problems, Tenth Revision (ICD-10). , 1997, Epidemiological bulletin.