Disrupted interhemispheric coordination of sensory-motor networks and insula in major depressive disorder

Objective Prior researches have identified distinct differences in neuroimaging characteristics between healthy controls (HCs) and patients with major depressive disorder (MDD). However, the correlations between homotopic connectivity and clinical characteristics in patients with MDD have yet to be fully understood. The present study aimed to investigate common and unique patterns of homotopic connectivity and their relationships with clinical characteristics in patients with MDD. Methods We recruited 42 patients diagnosed with MDD and 42 HCs. We collected a range of clinical variables, as well as exploratory eye movement (EEM), event-related potentials (ERPs) and resting-state functional magnetic resonance imaging (rs-fMRI) data. The data were analyzed using correlation analysis, support vector machine (SVM), and voxel-mirrored homotopic connectivity (VMHC). Results Compared with HCs, patients with MDD showed decreased VMHC in the insula, and increased VMHC in the cerebellum 8/vermis 8/vermis 9 and superior/middle occipital gyrus. SVM analysis using VMHC values in the cerebellum 8/vermis 8/vermis 9 and insula, or VMHC values in the superior/middle occipital gyrus and insula as inputs can distinguish HCs and patients with MDD with high accuracy, sensitivity, and specificity. Conclusion The study demonstrated that decreased VMHC in the insula and increased VMHC values in the sensory-motor networks may be a distinctive neurobiological feature for patients with MDD, which could potentially serve as imaging markers to discriminate HCs and patients with MDD.

[1]  Xiaohua Liu,et al.  P300 event-related potentials in patients with different subtypes of depressive disorders , 2023, Frontiers in Psychiatry.

[2]  Jiajia Zhu,et al.  Functional connectivity gradients of the insula to different cerebral systems , 2022, Human brain mapping.

[3]  G. Fries,et al.  Molecular pathways of major depressive disorder converge on the synapse , 2022, Molecular Psychiatry.

[4]  Jiayu Wu,et al.  Altered functional connectivity in emotional subregions of the anterior cingulate cortex in young and middle-aged patients with major depressive disorder: A resting-state fMRI study , 2022, Biological Psychology.

[5]  Sha Liu,et al.  Baseline cognitive functioning can predict the trajectory of acute treatment in first-episode major depressive disorder , 2022, European Archives of Psychiatry and Clinical Neuroscience.

[6]  Jun Wu,et al.  The decreased connectivity in middle temporal gyrus can be used as a potential neuroimaging biomarker for left temporal lobe epilepsy , 2022, Frontiers in Psychiatry.

[7]  Weihui Li,et al.  Altered Effective Connectivity Among the Cerebellum and Cerebrum in Patients with Major Depressive Disorder Using Multisite Resting-State fMRI , 2022, The Cerebellum.

[8]  I. Heitland,et al.  Altered functional connectivity in common resting-state networks in patients with major depressive disorder: A resting-state functional connectivity study. , 2022, Journal of psychiatric research.

[9]  Jun Wu,et al.  Altered voxel-mirrored homotopic connectivity in right temporal lobe epilepsy as measured using resting-state fMRI and support vector machine analyses , 2022, Frontiers in Psychiatry.

[10]  Feng Liu,et al.  Abnormal spontaneous neural activity in hippocampal–cortical system of patients with obsessive–compulsive disorder and its potential for diagnosis and prediction of early treatment response , 2022, Frontiers in Cellular Neuroscience.

[11]  Chu-Chung Huang,et al.  Abnormal Reginal Homogeneity in Left Anterior Cingulum Cortex and Precentral Gyrus as a Potential Neuroimaging Biomarker for First-Episode Major Depressive Disorder , 2022, Frontiers in Psychiatry.

[12]  Jinou Zheng,et al.  Aberrant resting-state interhemispheric functional connectivity in patients with anti-N-methyl-D-aspartate receptor encephalitis , 2022, Neuroradiology.

[13]  M. Cha,et al.  Modulation of Neuropathic Pain by Glial Regulation in the Insular Cortex of Rats , 2022, Frontiers in Molecular Neuroscience.

[14]  Zhou Zhifeng,et al.  Aberrant Inter-hemispheric Connectivity in Patients With Recurrent Major Depressive Disorder: A Multimodal MRI Study , 2022, Frontiers in Neurology.

[15]  Feng Liu,et al.  Disrupted Cerebellar-Default Mode Network Functional Connectivity in Major Depressive Disorder With Gastrointestinal Symptoms , 2022, Frontiers in Cellular Neuroscience.

[16]  D. St. Clair,et al.  The similar eye movement dysfunction between major depressive disorder, bipolar depression and bipolar mania , 2022, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[17]  Hao Hu,et al.  Altered Static and Dynamic Interhemispheric Resting-State Functional Connectivity in Patients With Thyroid-Associated Ophthalmopathy , 2021, Frontiers in Neuroscience.

[18]  Nana Li,et al.  Risk factors for the frequent attendance of older patients at community health service centers in China: a cross-sectional study based on stratified sampling , 2021, BMC Family Practice.

[19]  Wenbin Guo,et al.  Abnormal interhemispheric homotopic functional connectivity is correlated with gastrointestinal symptoms in patients with major depressive disorder. , 2021, Journal of psychiatric research.

[20]  Reed J. D. Sorensen,et al.  Global prevalence and burden of depressive and anxiety disorders in 204 countries and territories in 2020 due to the COVID-19 pandemic , 2021, The Lancet.

[21]  Chang-Hong Wang,et al.  A combination of P300 and eye movement data improves the accuracy of auxiliary diagnoses of depression. , 2021, Journal of affective disorders.

[22]  Y. Assaf,et al.  Inner Hemispheric and Interhemispheric Connectivity Balance in the Human Brain , 2021, The Journal of Neuroscience.

[23]  Shouliang Qi,et al.  Integrating Structural and Functional Interhemispheric Brain Connectivity of Gait Freezing in Parkinson's Disease , 2021, Frontiers in Neurology.

[24]  C. Habas Functional Connectivity of the Cognitive Cerebellum , 2021, Frontiers in Systems Neuroscience.

[25]  A. Bala,et al.  Anatomical aspects of the insula, opercula and peri-insular white matter for a transcortical approach to insular glioma resection , 2021, Neurosurgical Review.

[26]  G. Moseley,et al.  Considerations for using the Wisconsin Card Sorting Test to assess cognitive flexibility , 2021, Behavior Research Methods.

[27]  Feng Liu,et al.  Shared and distinct homotopic connectivity changes in melancholic and non-melancholic depression. , 2021, Journal of affective disorders.

[28]  Wei-Kuang Liang,et al.  Event-related components are structurally represented by intrinsic event-related potentials , 2021, Scientific Reports.

[29]  P. Sullivan,et al.  Genetic heterogeneity and subtypes of major depression , 2021, Molecular Psychiatry.

[30]  T. Andlauer,et al.  The genetic basis of major depression , 2021, Psychological Medicine.

[31]  W. Au,et al.  The Interactive Effects of Cognition on Coping Styles among Chinese during the COVID-19 Pandemic , 2021, International journal of environmental research and public health.

[32]  A. Hakim,et al.  Depression, dementia and immune dysregulation. , 2020, Brain : a journal of neurology.

[33]  M. Wong,et al.  Landscapes of bacterial and metabolic signatures and their interaction in major depressive disorders , 2020, Science Advances.

[34]  Ying Yang,et al.  Cerebellar-cerebral dynamic functional connectivity alterations in major depressive disorder. , 2020, Journal of affective disorders.

[35]  Ru Yang,et al.  Decreased Resting-State Interhemispheric Functional Connectivity in Medication-Free Obsessive-Compulsive Disorder , 2020, Frontiers in Psychiatry.

[36]  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.

[37]  C. Pisanu,et al.  Application of Support Vector Machine on fMRI Data as Biomarkers in Schizophrenia Diagnosis: A Systematic Review , 2020, Frontiers in Psychiatry.

[38]  Xuntao Yin,et al.  Atrophic Corpus Callosum Associated with Altered Functional Asymmetry in Major Depressive Disorder , 2020, Neuropsychiatric disease and treatment.

[39]  Ying Shen,et al.  Cerebellar Dysfunction, Cerebro-cerebellar Connectivity and Autism Spectrum Disorders , 2020, Neuroscience.

[40]  V. van de Ven,et al.  Contributions of Cerebro-Cerebellar Default Mode Connectivity Patterns to Memory Performance in Mild Cognitive Impairment , 2020, Journal of Alzheimer's disease : JAD.

[41]  M. Chakravarty,et al.  The P300 event-related potential in bipolar disorder: A systematic review and meta-analysis. , 2019, Journal of affective disorders.

[42]  S. Lhatoo,et al.  Insular resection may lead to autonomic function changes , 2019, Epilepsy & Behavior.

[43]  R. Schneggenburger,et al.  Insular cortex processes aversive somatosensory information and is crucial for threat learning , 2019, Science.

[44]  Greg Hajcak,et al.  The Utility of Event-Related Potentials in Clinical Psychology. , 2019, Annual review of clinical psychology.

[45]  Paavo H. T. Leppänen,et al.  Review of Abnormal Self-Knowledge in Major Depressive Disorder , 2019, Front. Psychiatry.

[46]  S. Umeda,et al.  Anterior insular cortex stimulation and its effects on emotion recognition , 2019, Brain Structure and Function.

[47]  Ning Zhang,et al.  Abnormal resting state activity of left middle occipital gyrus and its functional connectivity in female patients with major depressive disorder , 2018, BMC Psychiatry.

[48]  Fei Wang,et al.  Decreased Functional Connectivity in Insular Subregions in Depressive Episodes of Bipolar Disorder and Major Depressive Disorder , 2018, Front. Neurosci..

[49]  P. Sullivan,et al.  Genetics of response to cognitive behavior therapy in adults with major depression: a preliminary report , 2018, Molecular Psychiatry.

[50]  Huafu Chen,et al.  Decreased interhemispheric coordination in the posterior default-mode network and visual regions as trait alterations in first-episode, drug-naive major depressive disorder , 2018, Brain Imaging and Behavior.

[51]  Wenbin Guo,et al.  Voxel-Mirrored Homotopic Connectivity of Resting-State Functional Magnetic Resonance Imaging in Blepharospasm , 2018, Front. Psychol..

[52]  R. Lanius,et al.  The cerebellum after trauma: Resting‐state functional connectivity of the cerebellum in posttraumatic stress disorder and its dissociative subtype , 2018, Human brain mapping.

[53]  B. Grant,et al.  Epidemiology of Adult DSM-5 Major Depressive Disorder and Its Specifiers in the United States , 2018, JAMA psychiatry.

[54]  Xiao-ping Wu,et al.  Insular subdivisions functional connectivity dysfunction within major depressive disorder. , 2018, Journal of affective disorders.

[55]  N. Pliskin,et al.  Depression and performance on the Repeatable Battery for the Assessment of Neuropsychological Status , 2017, Applied neuropsychology. Adult.

[56]  M. Xuan,et al.  Difference in resting-state fractional amplitude of low-frequency fluctuation between bipolar depression and unipolar depression patients. , 2017, European review for medical and pharmacological sciences.

[57]  Yonggui Yuan,et al.  Prognostic value of imbalanced interhemispheric functional coordination in early therapeutic efficacy in major depressive disorder , 2016, Psychiatry Research: Neuroimaging.

[58]  Feng Liu,et al.  Clinical significance of increased cerebellar default-mode network connectivity in resting-state patients with drug-naive somatization disorder , 2016, Medicine.

[59]  G. Deco,et al.  Dynamic functional connectivity reveals altered variability in functional connectivity among patients with major depressive disorder , 2016, Human brain mapping.

[60]  Ravi S. Menon,et al.  Medial Prefrontal and Anterior Insular Connectivity in Early Schizophrenia and Major Depressive Disorder: A Resting Functional MRI Evaluation of Large-Scale Brain Network Models , 2016, Front. Hum. Neurosci..

[61]  Karl J. Friston,et al.  Anterior insula coordinates hierarchical processing of tactile mismatch responses , 2016, NeuroImage.

[62]  Yan Zhou,et al.  Altered Functional Connectivity in Patients with Subcortical Vascular Cognitive Impairment—A Resting-State Functional Magnetic Resonance Imaging Study , 2015, PloS one.

[63]  Qian Cui,et al.  Disrupted cortical hubs in functional brain networks in social anxiety disorder , 2015, Clinical Neurophysiology.

[64]  Feng Liu,et al.  Decreased insular connectivity in drug-naive major depressive disorder at rest. , 2015, Journal of affective disorders.

[65]  Warren W. Kretzschmar,et al.  Sparse whole genome sequencing identifies two loci for major depressive disorder , 2015, Nature.

[66]  Yu-Te Wu,et al.  Decreased inter-hemispheric connectivity in anterior sub-network of default mode network and cerebellum: significant findings in major depressive disorder. , 2014, The international journal of neuropsychopharmacology.

[67]  Jerzy Bodurka,et al.  Major Depressive Disorder Is Associated With Abnormal Interoceptive Activity and Functional Connectivity in the Insula , 2014, Biological Psychiatry.

[68]  Huafu Chen,et al.  Is there a cerebellar compensatory effort in first-episode, treatment-naive major depressive disorder at rest? , 2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[69]  Feng Liu,et al.  Abnormal resting-state cerebellar–cerebral functional connectivity in treatment-resistant depression and treatment sensitive depression , 2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[70]  N. Sadato,et al.  The anterior insular and anterior cingulate cortices in emotional processing for self-face recognition , 2013, Social cognitive and affective neuroscience.

[71]  D. Sliz,et al.  Major Depressive Disorder and Alterations in Insular Cortical Activity: A Review of Current Functional Magnetic Imaging Research , 2012, Front. Hum. Neurosci..

[72]  K. Yuan,et al.  Reduced Fractional Anisotropy of Corpus Callosum Modulates Inter-Hemispheric Resting State Functional Connectivity in Migraine Patients without Aura , 2012, PloS one.

[73]  Feng Liu,et al.  Abnormal neural activities in first-episode, treatment-naïve, short-illness-duration, and treatment-response patients with major depressive disorder: a resting-state fMRI study. , 2011, Journal of affective disorders.

[74]  Xi-Nian Zuo,et al.  REST: A Toolkit for Resting-State Functional Magnetic Resonance Imaging Data Processing , 2011, PloS one.

[75]  Paul E. Croarkin,et al.  Functional Connectivity of Brain Structures Correlates with Treatment Outcome in Major Depressive Disorder , 2011, Front. Psychiatry.

[76]  Alan C. Evans,et al.  Growing Together and Growing Apart: Regional and Sex Differences in the Lifespan Developmental Trajectories of Functional Homotopy , 2010, The Journal of Neuroscience.

[77]  S. Rombouts,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[78]  Chaogan Yan,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010, Front. Syst. Neurosci..

[79]  Lumy Sawaki,et al.  Roles of the Insular Cortex in the Modulation of Pain: Insights from Brain Lesions , 2009, The Journal of Neuroscience.

[80]  R. Lencer,et al.  Neurophysiology and neuroanatomy of smooth pursuit in humans , 2008, Brain and Cognition.

[81]  T. Paus,et al.  Functional coactivation map of the human brain. , 2008, Cerebral cortex.

[82]  Anthony R. McIntosh,et al.  Task-related activity in prefrontal cortex and its relation to recognition memory performance in young and old adults , 2005, Neuropsychologia.

[83]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[84]  Page Widick,et al.  Take it to the bridge: an interhemispheric processing advantage for emotional faces. , 2005, Brain research. Cognitive brain research.

[85]  R. Bagby,et al.  The Hamilton Depression Rating Scale: has the gold standard become a lead weight? , 2004, The American journal of psychiatry.

[86]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[87]  Roberto Cabeza,et al.  Aging Gracefully: Compensatory Brain Activity in High-Performing Older Adults , 2002, NeuroImage.

[88]  J. Ellingson,et al.  Substance versus style: a new look at social desirability in motivating contexts. , 2002, The Journal of applied psychology.

[89]  A. Olincy,et al.  Eye movement task measures inhibition and spatial working memory in adults with schizophrenia, ADHD, and a normal comparison group , 2000, Psychiatry Research.