Multimetric Structural Covariance in First-episode Major Depressive Disorder: a Graph Theoretical Analysis

Overview

Journal J Psychiatry Neurosci

Specialty Psychiatry

Date 2022 May 4

PMID 35508328

Authors

Chujun Chen

Zhening Liu

Chang Xi

Wenjian Tan

Zebin Fan

Yixin Cheng

Jun Yang

Lena Palaniyappan

Jie Yang

Affiliations

Soon will be listed here.

Abstract

Background: Abnormalities of cortical morphology have been consistently reported in major depressive disorder (MDD), with widespread focal alterations in cortical thickness, surface area and gyrification. However, it is unclear whether these distributed focal changes disrupt the system-level architecture (topology) of brain morphology in MDD. If present, such a topological disruption might explain the mechanisms that underlie altered cortical morphology in MDD.

Methods: Seventy-six patients with first-episode MDD (33 male, 43 female) and 66 healthy controls (32 male, 34 female) underwent structural MRI scans. We calculated cortical indices, including cortical thickness, surface area and local gyrification index, using FreeSurfer. We constructed morphological covariance networks using the 3 cortical indices separately, and we analyzed the topological properties of these group-level morphological covariance networks using graph theoretical approaches.

Results: Topological differences between patients with first-episode MDD and healthy controls were restricted to the thickness-based network. We found a significant decrease in global efficiency but an increase in local efficiency of the left superior frontal gyrus and the right paracentral lobule in patients with first-episode MDD. When we simulated targeted lesions affecting the most highly connected nodes, the thickness-based networks in patients with first-episode MDD disintegrated more rapidly than those in healthy controls.

Limitations: Our sample of patients with first-episode MDD has limited generalizability to patients with chronic and recurrent MDD.

Conclusion: A systems-level disruption in cortical thickness (but not surface area or gyrification) occurs in patients with first-episode MDD.

Citing Articles

Impaired topology and connectivity of grey matter structural networks in major depressive disorder: evidence from a multi-site neuroimaging data-set.

Long J, Qin K, Pan N, Fan W, Li Y Br J Psychiatry. 2024; 224(5):170-178.

PMID: 38602159 PMC: 11039554. DOI: 10.1192/bjp.2024.41.

Analysis of brain structural covariance network in Cushing disease.

Xu C, Kong L, Jiang H, Jiang Y, Sun Y, Bian L Heliyon. 2024; 10(7):e28957.

PMID: 38601682 PMC: 11004566. DOI: 10.1016/j.heliyon.2024.e28957.

Innovative Neuroimaging Biomarker Distinction of Major Depressive Disorder and Bipolar Disorder through Structural Connectome Analysis and Machine Learning Models.

Huang Y, Zhang J, He K, Mo X, Yu R, Min J Diagnostics (Basel). 2024; 14(4).

PMID: 38396428 PMC: 10888009. DOI: 10.3390/diagnostics14040389.

Impact of Stress on Brain Morphology: Insights into Structural Biomarkers of Stress-related Disorders.

Cardoner N, Andero R, Cano M, Marin-Blasco I, Porta-Casteras D, Serra-Blasco M Curr Neuropharmacol. 2023; 22(5):935-962.

PMID: 37403395 PMC: 10845094. DOI: 10.2174/1570159X21666230703091435.

Gyrification patterns in first-episode, drug-naïve major depression: Associations with plasma levels of brain-derived neurotrophic factor and psychiatric symptoms.

Natsuyama T, Okamoto N, Watanabe K, Chibaatar E, Tesen H, Hayasaki G Front Psychiatry. 2023; 13:1031386.

PMID: 36684011 PMC: 9852994. DOI: 10.3389/fpsyt.2022.1031386.

References

Zhou H, Chen X, Shen Y, Li L, Chen N, Zhu Z . Rumination and the default mode network: Meta-analysis of brain imaging studies and implications for depression. Neuroimage. 2019; 206:116287. DOI: 10.1016/j.neuroimage.2019.116287. View

Destrieux C, Fischl B, Dale A, Halgren E . Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage. 2010; 53(1):1-15. PMC: 2937159. DOI: 10.1016/j.neuroimage.2010.06.010. View

Chenn A, Walsh C . Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science. 2002; 297(5580):365-9. DOI: 10.1126/science.1074192. View

Alexander-Bloch A, Giedd J, Bullmore E . Imaging structural co-variance between human brain regions. Nat Rev Neurosci. 2013; 14(5):322-36. PMC: 4043276. DOI: 10.1038/nrn3465. View

Liu J, Xu X, Zhu C, Luo L, Wang Q, Xiao B . Disrupted Structural Brain Network Organization Behind Depressive Symptoms in Major Depressive Disorder. Front Psychiatry. 2020; 11:565890. PMC: 7538511. DOI: 10.3389/fpsyt.2020.565890. View

Bi G, Poo M . Distributed synaptic modification in neural networks induced by patterned stimulation. Nature. 1999; 401(6755):792-6. DOI: 10.1038/44573. View

Ajnakina O, Das T, Lally J, Di Forti M, Pariante C, Marques T . Structural Covariance of Cortical Gyrification at Illness Onset in Treatment Resistance: A Longitudinal Study of First-Episode Psychoses. Schizophr Bull. 2021; 47(6):1729-1739. PMC: 8530394. DOI: 10.1093/schbul/sbab035. View

Bullmore E, Sporns O . Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009; 10(3):186-98. DOI: 10.1038/nrn2575. View

Peng D, Shi F, Li G, Fralick D, Shen T, Qiu M . Surface vulnerability of cerebral cortex to major depressive disorder. PLoS One. 2015; 10(3):e0120704. PMC: 4368815. DOI: 10.1371/journal.pone.0120704. View

10.

Desikan R, Segonne F, Fischl B, Quinn B, Dickerson B, Blacker D . An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006; 31(3):968-80. DOI: 10.1016/j.neuroimage.2006.01.021. View

11.

Hogstrom L, Westlye L, Walhovd K, Fjell A . The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. Cereb Cortex. 2012; 23(11):2521-30. DOI: 10.1093/cercor/bhs231. View

12.

Van Essen D . A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 1997; 385(6614):313-8. DOI: 10.1038/385313a0. View

13.

Yang J, Hellerstein D, Chen Y, McGrath P, Stewart J, Liu Z . Gray matter reorganization underpinnings of antidepressant treatment of persistent depressive disorder. Eur Neuropsychopharmacol. 2021; 43:129-138. DOI: 10.1016/j.euroneuro.2020.12.009. View

14.

Raznahan A, Shaw P, Lalonde F, Stockman M, Wallace G, Greenstein D . How does your cortex grow?. J Neurosci. 2011; 31(19):7174-7. PMC: 3157294. DOI: 10.1523/JNEUROSCI.0054-11.2011. View

15.

Kessler R, Berglund P, Demler O, Jin R, Koretz D, Merikangas K . The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). JAMA. 2003; 289(23):3095-105. DOI: 10.1001/jama.289.23.3095. View

16.

Singh M, Kesler S, Hosseini S, Kelley R, Amatya D, Hamilton J . Anomalous gray matter structural networks in major depressive disorder. Biol Psychiatry. 2013; 74(10):777-85. PMC: 3805751. DOI: 10.1016/j.biopsych.2013.03.005. View

17.

Tan W, Liu Z, Xi C, Deng M, Long Y, Palaniyappan L . Decreased integration of the frontoparietal network during a working memory task in major depressive disorder. Aust N Z J Psychiatry. 2020; 55(6):577-587. DOI: 10.1177/0004867420978284. View

18.

Chen T, Kendrick K, Wang J, Wu M, Li K, Huang X . Anomalous single-subject based morphological cortical networks in drug-naive, first-episode major depressive disorder. Hum Brain Mapp. 2017; 38(5):2482-2494. PMC: 6866860. DOI: 10.1002/hbm.23534. View

19.

Papini C, Palaniyappan L, Kroll J, Froudist-Walsh S, Murray R, Nosarti C . Altered Cortical Gyrification in Adults Who Were Born Very Preterm and Its Associations With Cognition and Mental Health. Biol Psychiatry Cogn Neurosci Neuroimaging. 2020; 5(7):640-650. DOI: 10.1016/j.bpsc.2020.01.006. View

20.

Gong Q, He Y . Depression, neuroimaging and connectomics: a selective overview. Biol Psychiatry. 2014; 77(3):223-235. DOI: 10.1016/j.biopsych.2014.08.009. View