Static and dynamic connectomics differentiate between depressed patients with and without suicidal ideation

Neural circuit dysfunction underlies the biological mechanisms of suicidal ideation (SI). However, little is known about how the brain's “dynome” differentiate between depressed patients with and without SI. This study included depressed patients (n = 48) with SI, without SI (NSI), and healthy controls (HC, n = 30). All participants underwent resting‐state functional magnetic resonance imaging. We constructed dynamic and static connectomics on 200 nodes using a sliding window and full‐length time–series correlations, respectively. Specifically, the temporal variability of dynamic connectomic was quantified using the variance of topological properties across sliding window. The overall topological properties of both static and dynamic connectomics further differentiated between SI and NSI, and also predicted the severity of SI. The SI showed decreased overall topological properties of static connectomic relative to the HC. The SI exhibited increases in overall topological properties with regard to the dynamic connectomic when compared with the HC and the NSI. Importantly, combining the overall topological properties of dynamic and static connectomics yielded mean 75% accuracy (all p < .001) with mean 71% sensitivity and mean 75% specificity in differentiating between SI and NSI. Moreover, these features may predict the severity of SI (mean r = .55, all p < .05). The findings revealed that combining static and dynamic connectomics could differentiate between SI and NSI, offering new insight into the physiopathological mechanisms underlying SI. Furthermore, combining the brain's connectome and dynome may be considered a neuromarker for diagnostic and predictive models in the study of SI.

[1]  Éric Gaussier,et al.  A Probabilistic Interpretation of Precision, Recall and F-Score, with Implication for Evaluation , 2005, ECIR.

[2]  M. Fava,et al.  Reduced orbitofrontal-thalamic functional connectivity related to suicidal ideation in patients with major depressive disorder , 2017, Scientific Reports.

[3]  Xiaoqi Huang,et al.  Disrupted Brain Connectivity Networks in Drug-Naive, First-Episode Major Depressive Disorder , 2011, Biological Psychiatry.

[4]  Kevin Murphy,et al.  Resting-state fMRI confounds and cleanup , 2013, NeuroImage.

[5]  Zachary C. Irving,et al.  Mind-wandering as spontaneous thought: a dynamic framework , 2016, Nature Reviews Neuroscience.

[6]  Huafu Chen,et al.  Differential patterns of dynamic functional connectivity variability of striato–cortical circuitry in children with benign epilepsy with centrotemporal spikes , 2018, Human brain mapping.

[7]  Yong He,et al.  Chronnectome fingerprinting: Identifying individuals and predicting higher cognitive functions using dynamic brain connectivity patterns , 2018, Human brain mapping.

[8]  Liang Wang,et al.  Parcellation‐dependent small‐world brain functional networks: A resting‐state fMRI study , 2009, Human brain mapping.

[9]  Meiling Li,et al.  Dynamic functional network connectivity in idiopathic generalized epilepsy with generalized tonic–clonic seizure , 2017, Human brain mapping.

[10]  S. Whitfield-Gabrieli,et al.  Dynamic Resting-State Functional Connectivity in Major Depression , 2016, Neuropsychopharmacology.

[11]  Jessica R. Cohen The behavioral and cognitive relevance of time-varying, dynamic changes in functional connectivity , 2017, NeuroImage.

[12]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[13]  M. Furey,et al.  Neural Correlates of Suicidal Ideation and Its Reduction in Depression , 2015, The international journal of neuropsychopharmacology.

[14]  M. Bogren,et al.  Long‐term suicide risk of depression in the Lundby cohort 1947–1997 – severity and gender , 2008, Acta psychiatrica Scandinavica.

[15]  Sylvain Houle,et al.  Abnormal intrinsic brain functional network dynamics in Parkinson’s disease , 2017, Brain : a journal of neurology.

[16]  Eswar Damaraju,et al.  Tracking whole-brain connectivity dynamics in the resting state. , 2014, Cerebral cortex.

[17]  Lena S. Geiger,et al.  Dynamic brain network reconfiguration as a potential schizophrenia genetic risk mechanism modulated by NMDA receptor function , 2016, Proceedings of the National Academy of Sciences.

[18]  Huafu Chen,et al.  Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. , 2011, Brain : a journal of neurology.

[19]  Jong H. Yoon,et al.  General and Specific Functional Connectivity Disturbances in First-Episode Schizophrenia During Cognitive Control Performance , 2011, Biological Psychiatry.

[20]  M. Fava,et al.  Reduced frontal-subcortical white matter connectivity in association with suicidal ideation in major depressive disorder , 2016, Translational psychiatry.

[21]  Laura C. Buchanan,et al.  The spatial structure of resting state connectivity stability on the scale of minutes , 2014, Front. Neurosci..

[22]  Jinkun Zeng,et al.  Fronto-limbic disconnection in depressed patients with suicidal ideation: A resting-state functional connectivity study. , 2017, Journal of affective disorders.

[23]  D. Hu,et al.  Identifying major depression using whole-brain functional connectivity: a multivariate pattern analysis. , 2012, Brain : a journal of neurology.

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

[25]  Yihong Yang,et al.  Spontaneous functional network dynamics and associated structural substrates in the human brain , 2015, Front. Hum. Neurosci..

[26]  Dimitri Van De Ville,et al.  On spurious and real fluctuations of dynamic functional connectivity during rest , 2015, NeuroImage.

[27]  Y. Zang,et al.  Identifying Corticothalamic Network Epicenters in Patients with Idiopathic Generalized Epilepsy , 2015, American Journal of Neuroradiology.

[28]  C. Baeken,et al.  Is there a neuroanatomical basis of the vulnerability to suicidal behavior? A coordinate-based meta-analysis of structural and functional MRI studies , 2014, Front. Hum. Neurosci..

[29]  Andres Hoyos Idrobo,et al.  Assessing and tuning brain decoders: Cross-validation, caveats, and guidelines , 2016, NeuroImage.

[30]  Yong He,et al.  Individual differences and time-varying features of modular brain architecture , 2017, NeuroImage.

[31]  Yufeng Zang,et al.  DynamicBC: A MATLAB Toolbox for Dynamic Brain Connectome Analysis , 2014, Brain Connect..

[32]  M. Iwata,et al.  Suicidal ideation is associated with reduced prefrontal activation during a verbal fluency task in patients with major depressive disorder. , 2015, Journal of affective disorders.

[33]  E. D. Klonsky,et al.  Differentiating suicide attempters from suicide ideators: a critical frontier for suicidology research. , 2014, Suicide & life-threatening behavior.

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

[35]  Eric D A Hermes,et al.  Multimodal Neuroimaging of Frontolimbic Structure and Function Associated With Suicide Attempts in Adolescents and Young Adults With Bipolar Disorder. , 2017, The American journal of psychiatry.

[36]  W. Liao,et al.  Decreased Network Efficiency in Benign Epilepsy with Centrotemporal Spikes. , 2017, Radiology.

[37]  E. Bullmore,et al.  Functional Connectivity and Brain Networks in Schizophrenia , 2010, The Journal of Neuroscience.

[38]  Eiko I. Fried,et al.  Depression sum-scores don’t add up: why analyzing specific depression symptoms is essential , 2015, BMC Medicine.

[39]  M. Pompili,et al.  Understanding Suicidal Behavior: The Contribution of Recent Resting-State fMRI Techniques , 2016, Front. Psychiatry.

[40]  C. Heeringen,et al.  Neuroscience and Biobehavioral Reviews Suicidal Brains: a Review of Functional and Structural Brain Studies in Association with Suicidal Behaviour , 2022 .

[41]  Wei Liao,et al.  Dynamical intrinsic functional architecture of the brain during absence seizures , 2013, Brain Structure and Function.

[42]  E. Bullmore,et al.  Opportunities and Challenges for Psychiatry in the Connectomic Era. , 2017, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[43]  O. Almeida,et al.  Identifying suicidal ideation among older adults in a general practice setting. , 2004, Journal of affective disorders.

[44]  Q. Gong,et al.  Dysfunction of neural circuitry in depressive patients with suicidal behaviors: A review of structural and functional neuroimaging studies , 2014, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[45]  R Cameron Craddock,et al.  A whole brain fMRI atlas generated via spatially constrained spectral clustering , 2012, Human brain mapping.

[46]  M. Kramer,et al.  Beyond the Connectome: The Dynome , 2014, Neuron.

[47]  Ravi S. Menon,et al.  Resting‐state networks show dynamic functional connectivity in awake humans and anesthetized macaques , 2013, Human brain mapping.

[48]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[49]  L. Williams,et al.  Abnormal Structural Networks Characterize Major Depressive Disorder: A Connectome Analysis , 2014, Biological Psychiatry.

[50]  O. Sporns,et al.  Network neuroscience , 2017, Nature Neuroscience.

[51]  A. Meyer-Lindenberg,et al.  Psychopathology and the Human Connectome: Toward a Transdiagnostic Model of Risk For Mental Illness , 2012, Neuron.

[52]  Yufeng Zang,et al.  Relationship Between Large-Scale Functional and Structural Covariance Networks in Idiopathic Generalized Epilepsy , 2013, Brain Connect..

[53]  A. Beck,et al.  Assessment of suicidal intention: the Scale for Suicide Ideation. , 1979, Journal of consulting and clinical psychology.

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

[55]  Vince D. Calhoun,et al.  Classification of schizophrenia and bipolar patients using static and dynamic resting-state fMRI brain connectivity , 2016, NeuroImage.

[56]  Aiping Liu,et al.  A Combined Static and Dynamic Model for Resting-State Brain Connectivity Networks , 2016, IEEE Journal of Selected Topics in Signal Processing.

[57]  Yong He,et al.  GRETNA: a graph theoretical network analysis toolbox for imaging connectomics , 2015, Front. Hum. Neurosci..

[58]  Dimitri Van De Ville,et al.  The dynamic functional connectome: State-of-the-art and perspectives , 2017, NeuroImage.

[59]  H. Blumberg,et al.  Neurobiological risk factors for suicide: insights from brain imaging. , 2014, American journal of preventive medicine.

[60]  Gerd Wagner,et al.  Structural brain alterations in patients with major depressive disorder and high risk for suicide: Evidence for a distinct neurobiological entity? , 2011, NeuroImage.