Multilayer MEG functional connectivity as a potential marker for suicidal thoughts in major depressive disorder

Allison C Nugent, Elizabeth D Ballard, Jessica R Gilbert, Prejaas K Tewarie, Matthew J Brookes, Carlos A Zarate Jr, Allison C Nugent, Elizabeth D Ballard, Jessica R Gilbert, Prejaas K Tewarie, Matthew J Brookes, Carlos A Zarate Jr

Abstract

Major depressive disorder (MDD) is highly heterogeneous in its clinical presentation. The present exploratory study used magnetoencephalography (MEG) to investigate electrophysiological intrinsic connectivity differences between healthy volunteers and unmedicated participants with treatment-resistant MDD. The study examined canonical frequency bands from delta through gamma. In addition to group comparisons, correlational studies were conducted to determine whether connectivity was related to five symptom factors: depressed mood, tension, negative cognition, suicidal thoughts, and amotivation. The MDD and healthy volunteer groups did not differ significantly at baseline when corrected across all frequencies and clusters, although evidence of generalized slowing in MDD was observed. Notably, however, electrophysiological connectivity was strongly related to suicidal thoughts, particularly as coupling of low frequency power fluctuations (delta and theta) with alpha and beta power. This analysis revealed hub areas underlying this symptom cluster, including left hippocampus, left anterior insula, and bilateral dorsolateral prefrontal cortex. No other symptom cluster demonstrated a relationship with neurophysiological connectivity, suggesting a specificity to these results as markers of suicidal ideation.

Trial registration: ClinicalTrials.gov NCT00088699.

Keywords: Connectivity; Frequency; Magnetoencephalography; Major depressive disorder; Oscillation; Suicide.

Conflict of interest statement

Dr. Zarate is listed as a co-inventor on a patent for the use of ketamine in major depression and suicidal ideation; as a co-inventor on a patent for the use of (2R,6R)-hydroxynorketamine, (S)-dehydronorketamine, and other stereoisomeric dehydro and hydroxylated metabolites of (R,S)-ketamine metabolites in the treatment of depression and neuropathic pain; and as a co-inventor on a patent application for the use of (2R,6R)-hydroxynorketamine and (2S,6S)-hydroxynorketamine in the treatment of depression, anxiety, anhedonia, suicidal ideation, and post-traumatic stress disorders. He has assigned his patent rights to the U.S. government but will share a percentage of any royalties that may be received by the government. All other authors have no conflict of interest to disclose, financial or otherwise.

Copyright © 2020. Published by Elsevier Inc.

Figures

Fig. 1
Fig. 1
Super-adjacency matrices illustrating mean connectivity in A) healthy controls (HCs) and B) participants with major depressive disorder (MDD). The raw correlation matrices were converted using the Fisher r-to-z transform before averaging. C) Mean connectivity, with standard error, for each tile in both groups. D) Z-value for the difference between HC and MDD participants.
Fig. 2
Fig. 2
A) As an aid to visualization, the total connectivity for each node was calculated as a summation of adjacency matrix along one axis for the healthy control (HC) and major depressive disorder (MDD) groups separately, and then subtracted. The size of each thus represents the difference in total connectivity of that node between groups for within-frequency theta connectivity (top) and within-frequency alpha connectivity (bottom). B) The Z-score for the difference in total theta connectivity between groups for each node pair is plotted versus the difference in total alpha connectivity, indicating that nodes showing the greatest increase in theta-mediated connectivity tended to show the greatest decrease in alpha-mediated connectivity in participants with MDD compared to HCs.
Fig. 3
Fig. 3
Super-adjacency matrix showing Z-values for the association between connectivity and the magnitude of suicidal thoughts. Supra-threshold (Z = 4.45, q 

Fig. 4

Expanded delta band connectivity tile…

Fig. 4

Expanded delta band connectivity tile from Fig. 1 at the same statistical threshold…

Fig. 4
Expanded delta band connectivity tile from Fig. 1 at the same statistical threshold (Z = 4.45, q 

Fig. 5

Expanded theta band connectivity tile…

Fig. 5

Expanded theta band connectivity tile from Fig. 1 at the same statistical threshold…

Fig. 5
Expanded theta band connectivity tile from Fig. 1 at the same statistical threshold (Z = 4.45, q 

Fig. 6

Graph illustrating within- and across-frequency…

Fig. 6

Graph illustrating within- and across-frequency connections correlating with the suicidal thoughts (ST) factor,…

Fig. 6
Graph illustrating within- and across-frequency connections correlating with the suicidal thoughts (ST) factor, where region nodes are collapsed according to their network membership. All connections show a positive relationship with the ST factor, as in Fig. 3. The graph is thresholded to show only the 50 most significant edges for clarity (Z = 4.9, q = 3.6e-6). Abbreviations: DMN: default mode network; CEN: central executive network; SAL: salience network; SubCort: subcortical regions; Dep: depression-associated regions; Vis: visual regions; Mot: motor regions.

Fig. 7

A) Map of nodes with…

Fig. 7

A) Map of nodes with size scaled according to total Z-value for the…

Fig. 7
A) Map of nodes with size scaled according to total Z-value for the difference between healthy controls (HCs) and individuals with major depressive disorder (MDD) with high suicidal thoughts (ST) factor scores (MDD_S). B) Within- and across-frequency connections where MDD_S participants showed greater connectivity than HCs. Regions of interest (ROIs) have been collapsed according to their network membership. The graph is thresholded to show only the 50 most significant edges for clarity (Z = 3.45, q = 0.0034). C) For all 14,365 connections in the super-adjacency matrix, the Z-score difference in connectivity between MDD_S and HC participants was plotted versus the Z-score for the association of connectivity with the magnitude of ST factor score.
All figures (7)
Similar articles
Cited by
References
    1. APA . American Psychiatric Association; Washington, DC: 2013. Diagnostic and Statistical Manual of Mental Disorders: Fifth Edition, DSM-5.
    1. Balcioglu Y.H., Kose S. Neural substrates of suicide and suicidal behaviour: from a neuroimaging perspective. Psychiat. Clin. Psych. 2018;28:314–328.
    1. Ballard E.D., Yarrington J.S., Farmer C.A., Lener M.S., Kadriu B., Lally N., Williams D., Machado-Vieira R., Niciu M.J., Park L., Zarate C.A., Jr Parsing the heterogeneity of depression: an exploratory factor analysis across commonly used depression rating scales. J. Affect. Disord. 2018;231:51–57. - PMC - PubMed
    1. Becker R., Hervais-Adelman A. Resolving the connectome — spectrally-specific functional connectivity networks and their distinct contributions to behaviour. bioRxiv. 2019 doi: 10.1101/700278. - DOI - PMC - PubMed
    1. Betzel R.F., Bassett D.S. Multi-scale brain networks. NeuroImage. 2017;160:73–83. - PMC - PubMed
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Fig. 4
Fig. 4
Expanded delta band connectivity tile from Fig. 1 at the same statistical threshold (Z = 4.45, q 

Fig. 5

Expanded theta band connectivity tile…

Fig. 5

Expanded theta band connectivity tile from Fig. 1 at the same statistical threshold…

Fig. 5
Expanded theta band connectivity tile from Fig. 1 at the same statistical threshold (Z = 4.45, q 

Fig. 6

Graph illustrating within- and across-frequency…

Fig. 6

Graph illustrating within- and across-frequency connections correlating with the suicidal thoughts (ST) factor,…

Fig. 6
Graph illustrating within- and across-frequency connections correlating with the suicidal thoughts (ST) factor, where region nodes are collapsed according to their network membership. All connections show a positive relationship with the ST factor, as in Fig. 3. The graph is thresholded to show only the 50 most significant edges for clarity (Z = 4.9, q = 3.6e-6). Abbreviations: DMN: default mode network; CEN: central executive network; SAL: salience network; SubCort: subcortical regions; Dep: depression-associated regions; Vis: visual regions; Mot: motor regions.

Fig. 7

A) Map of nodes with…

Fig. 7

A) Map of nodes with size scaled according to total Z-value for the…

Fig. 7
A) Map of nodes with size scaled according to total Z-value for the difference between healthy controls (HCs) and individuals with major depressive disorder (MDD) with high suicidal thoughts (ST) factor scores (MDD_S). B) Within- and across-frequency connections where MDD_S participants showed greater connectivity than HCs. Regions of interest (ROIs) have been collapsed according to their network membership. The graph is thresholded to show only the 50 most significant edges for clarity (Z = 3.45, q = 0.0034). C) For all 14,365 connections in the super-adjacency matrix, the Z-score difference in connectivity between MDD_S and HC participants was plotted versus the Z-score for the association of connectivity with the magnitude of ST factor score.
All figures (7)
Similar articles
Cited by
References
    1. APA . American Psychiatric Association; Washington, DC: 2013. Diagnostic and Statistical Manual of Mental Disorders: Fifth Edition, DSM-5.
    1. Balcioglu Y.H., Kose S. Neural substrates of suicide and suicidal behaviour: from a neuroimaging perspective. Psychiat. Clin. Psych. 2018;28:314–328.
    1. Ballard E.D., Yarrington J.S., Farmer C.A., Lener M.S., Kadriu B., Lally N., Williams D., Machado-Vieira R., Niciu M.J., Park L., Zarate C.A., Jr Parsing the heterogeneity of depression: an exploratory factor analysis across commonly used depression rating scales. J. Affect. Disord. 2018;231:51–57. - PMC - PubMed
    1. Becker R., Hervais-Adelman A. Resolving the connectome — spectrally-specific functional connectivity networks and their distinct contributions to behaviour. bioRxiv. 2019 doi: 10.1101/700278. - DOI - PMC - PubMed
    1. Betzel R.F., Bassett D.S. Multi-scale brain networks. NeuroImage. 2017;160:73–83. - PMC - PubMed
Show all 73 references
Publication types
Associated data
Related information
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Fig. 5
Fig. 5
Expanded theta band connectivity tile from Fig. 1 at the same statistical threshold (Z = 4.45, q 

Fig. 6

Graph illustrating within- and across-frequency…

Fig. 6

Graph illustrating within- and across-frequency connections correlating with the suicidal thoughts (ST) factor,…

Fig. 6
Graph illustrating within- and across-frequency connections correlating with the suicidal thoughts (ST) factor, where region nodes are collapsed according to their network membership. All connections show a positive relationship with the ST factor, as in Fig. 3. The graph is thresholded to show only the 50 most significant edges for clarity (Z = 4.9, q = 3.6e-6). Abbreviations: DMN: default mode network; CEN: central executive network; SAL: salience network; SubCort: subcortical regions; Dep: depression-associated regions; Vis: visual regions; Mot: motor regions.

Fig. 7

A) Map of nodes with…

Fig. 7

A) Map of nodes with size scaled according to total Z-value for the…

Fig. 7
A) Map of nodes with size scaled according to total Z-value for the difference between healthy controls (HCs) and individuals with major depressive disorder (MDD) with high suicidal thoughts (ST) factor scores (MDD_S). B) Within- and across-frequency connections where MDD_S participants showed greater connectivity than HCs. Regions of interest (ROIs) have been collapsed according to their network membership. The graph is thresholded to show only the 50 most significant edges for clarity (Z = 3.45, q = 0.0034). C) For all 14,365 connections in the super-adjacency matrix, the Z-score difference in connectivity between MDD_S and HC participants was plotted versus the Z-score for the association of connectivity with the magnitude of ST factor score.
All figures (7)
Fig. 6
Fig. 6
Graph illustrating within- and across-frequency connections correlating with the suicidal thoughts (ST) factor, where region nodes are collapsed according to their network membership. All connections show a positive relationship with the ST factor, as in Fig. 3. The graph is thresholded to show only the 50 most significant edges for clarity (Z = 4.9, q = 3.6e-6). Abbreviations: DMN: default mode network; CEN: central executive network; SAL: salience network; SubCort: subcortical regions; Dep: depression-associated regions; Vis: visual regions; Mot: motor regions.
Fig. 7
Fig. 7
A) Map of nodes with size scaled according to total Z-value for the difference between healthy controls (HCs) and individuals with major depressive disorder (MDD) with high suicidal thoughts (ST) factor scores (MDD_S). B) Within- and across-frequency connections where MDD_S participants showed greater connectivity than HCs. Regions of interest (ROIs) have been collapsed according to their network membership. The graph is thresholded to show only the 50 most significant edges for clarity (Z = 3.45, q = 0.0034). C) For all 14,365 connections in the super-adjacency matrix, the Z-score difference in connectivity between MDD_S and HC participants was plotted versus the Z-score for the association of connectivity with the magnitude of ST factor score.

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Source: PubMed

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