Electroconvulsive therapy-induced volumetric brain changes converge on a common causal circuit in depression.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
20 Nov 2023
20 Nov 2023
Historique:
received:
11
05
2023
accepted:
06
11
2023
revised:
23
10
2023
pubmed:
21
11
2023
medline:
21
11
2023
entrez:
21
11
2023
Statut:
aheadofprint
Résumé
Neurostimulation is a mainstream treatment option for major depression. Neuromodulation techniques apply repetitive magnetic or electrical stimulation to some neural target but significantly differ in their invasiveness, spatial selectivity, mechanism of action, and efficacy. Despite these differences, recent analyses of transcranial magnetic stimulation (TMS) and deep brain stimulation (DBS)-treated individuals converged on a common neural network that might have a causal role in treatment response. We set out to investigate if the neuronal underpinnings of electroconvulsive therapy (ECT) are similarly associated with this causal depression network (CDN). Our aim here is to provide a comprehensive analysis in three cohorts of patients segregated by electrode placement (N = 246 with right unilateral, 79 with bitemporal, and 61 with mixed) who underwent ECT. We conducted a data-driven, unsupervised multivariate neuroimaging analysis Principal Component Analysis (PCA) of the cortical and subcortical volume changes and electric field (EF) distribution to explore changes within the CDN associated with antidepressant outcomes. Despite the different treatment modalities (ECT vs TMS and DBS) and methodological approaches (structural vs functional networks), we found a highly similar pattern of change within the CDN in the three cohorts of patients (spatial similarity across 85 regions: r = 0.65, 0.58, 0.40, df = 83). Most importantly, the expression of this pattern correlated with clinical outcomes (t = -2.35, p = 0.019). This evidence further supports that treatment interventions converge on a CDN in depression. Optimizing modulation of this network could serve to improve the outcome of neurostimulation in depression.
Identifiants
pubmed: 37985787
doi: 10.1038/s41380-023-02318-2
pii: 10.1038/s41380-023-02318-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH)
ID : K23MH120504
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH)
ID : R21MH119616
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH)
ID : MH128690
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH)
ID : MH111826
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : RE4458/1-1 to RR
Commentaires et corrections
Type : UpdateOf
Type : ErratumIn
Informations de copyright
© 2023. The Author(s).
Références
UK ECT Review Group. Efficacy and safety of electroconvulsive therapy in depressive disorders: a systematic review and meta-analysis. Lancet. 2003;361:799–808.
doi: 10.1016/S0140-6736(03)12705-5
Mutz J, Vipulananthan V, Carter B, Hurlemann R, Fu CHY, Young AH. Comparative efficacy and acceptability of non-surgical brain stimulation for the acute treatment of major depressive episodes in adults: systematic review and network meta-analysis. BMJ. 2019;364:l1079.
doi: 10.1136/bmj.l1079
pubmed: 30917990
pmcid: 6435996
Siddiqi SH, Schaper FLWVJ, Horn A, Hsu J, Padmanabhan JL, Brodtmann A, et al. Brain stimulation and brain lesions converge on common causal circuits in neuropsychiatric disease. Nat Hum Behav. 2021;5:1707–16.
doi: 10.1038/s41562-021-01161-1
pubmed: 34239076
pmcid: 8688172
Siddiqi SH, Kletenik I, Anderson MC, Cavallari M, Chitnis T, Glanz BI, et al. Lesion network localization of depression in multiple sclerosis. Nat Ment Health. 2023;1:36–44.
doi: 10.1038/s44220-022-00002-y
Morawetz C, Riedel MC, Salo T, Berboth S, Eickhoff SB, Laird AR, et al. Multiple large-scale neural networks underlying emotion regulation. Neurosci Biobehav Rev. 2020;116:382–95.
doi: 10.1016/j.neubiorev.2020.07.001
pubmed: 32659287
Huang Y, Liu AA, Lafon B, Friedman D, Dayan M, Wang X et al. Measurements and models of electric fields in the in vivo human brain during transcranial electric stimulation. eLife (2017); 6. https://doi.org/10.7554/eLife.18834 .
Bai S, Loo C, Al Abed A, Dokos S. A computational model of direct brain excitation induced by electroconvulsive therapy: comparison among three conventional electrode placements. Brain Stimul. 2012;5:408–21.
doi: 10.1016/j.brs.2011.07.004
pubmed: 21962983
Bai S, Gálvez V, Dokos S, Martin D, Bikson M, Loo C. Computational models of bitemporal, bifrontal and right unilateral ECT predict differential stimulation of brain regions associated with efficacy and cognitive side effects. Eur Psychiatry. 2017;41:21–29.
doi: 10.1016/j.eurpsy.2016.09.005
pubmed: 28049077
Deng Z-D, Lisanby SH, Peterchev AV. Effect of anatomical variability on electric field characteristics of electroconvulsive therapy and magnetic seizure therapy: a parametric modeling study. IEEE Trans Neural Syst Rehabil Eng. 2015;23:22–31.
doi: 10.1109/TNSRE.2014.2339014
pubmed: 25055384
Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973;232:331–56.
doi: 10.1113/jphysiol.1973.sp010273
pubmed: 4727084
pmcid: 1350458
Hesse GW, Teyler TJ. Reversible loss of hippocampal long term potentiation following electronconvulsive seizures. Nature. 1976;264:562–4.
doi: 10.1038/264562a0
pubmed: 1004596
Huang Y-Z, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45:201–6.
doi: 10.1016/j.neuron.2004.12.033
pubmed: 15664172
Ito M, Seki T, Liu J, Nakamura K, Namba T, Matsubara Y, et al. Effects of repeated electroconvulsive seizure on cell proliferation in the rat hippocampus. Synapse. 2010;64:814–21.
doi: 10.1002/syn.20796
pubmed: 20340175
Zhao C, Warner-Schmidt J, Duman RS, Gage FH. Electroconvulsive seizure promotes spine maturation in newborn dentate granule cells in adult rat. Dev Neurobiol. 2012;72:937–42.
doi: 10.1002/dneu.20986
pubmed: 21976455
pmcid: 3623264
Oltedal L, Bartsch H, Sørhaug OJE, Kessler U, Abbott C, Dols A, et al. The Global ECT-MRI Research Collaboration (GEMRIC): establishing a multi-site investigation of the neural mechanisms underlying response to electroconvulsive therapy. Neuroimage Clin. 2017;14:422–32.
doi: 10.1016/j.nicl.2017.02.009
pubmed: 28275543
pmcid: 5328749
Oltedal L, Narr KL, Abbott C, Anand A, Argyelan M, Bartsch H, et al. Volume of the human hippocampus and clinical response following electroconvulsive therapy. Biol Psychiatry. 2018;84:574–81.
doi: 10.1016/j.biopsych.2018.05.017
pubmed: 30006199
pmcid: 6697556
Ousdal OT, Argyelan M, Narr KL, Abbott C, Wade B, Vandenbulcke M, et al. Brain changes induced by electroconvulsive therapy are broadly distributed. Biol Psychiatry. 2020;87:451–61.
doi: 10.1016/j.biopsych.2019.07.010
pubmed: 31561859
Argyelan M, Oltedal L, Deng Z-D, Wade B, Bikson M, Joanlanne A et al. Electric field causes volumetric changes in the human brain. eLife 2019;8. https://doi.org/10.7554/eLife.49115 .
Deng Z-D, Argyelan M, Miller J, Quinn DK, Lloyd M, Jones TR, et al. Electroconvulsive therapy, electric field, neuroplasticity, and clinical outcomes. Mol Psychiatry. 2022;27:1676–82.
doi: 10.1038/s41380-021-01380-y
pubmed: 34853404
Takamiya A, Bouckaert F, Laroy M, Blommaert J, Radwan A, Khatoun A, et al. Biophysical mechanisms of electroconvulsive therapy-induced volume expansion in the medial temporal lobe: a longitudinal in vivo human imaging study. Brain Stimul. 2021;14:1038–47.
doi: 10.1016/j.brs.2021.06.011
pubmed: 34182182
pmcid: 8474653
Fridgeirsson EA, Deng Z-D, Denys D, van Waarde JA, van Wingen GA. Electric field strength induced by electroconvulsive therapy is associated with clinical outcome. Neuroimage Clin. 2021;30:102581.
doi: 10.1016/j.nicl.2021.102581
pubmed: 33588322
pmcid: 7895836
Abbott CC, Quinn D, Miller J, Ye E, Iqbal S, Lloyd M, et al. Electroconvulsive therapy pulse amplitude and clinical outcomes. Am J Geriatr Psychiatry. 2021;29:166–78.
doi: 10.1016/j.jagp.2020.06.008
pubmed: 32651051
Gryglewski G, Lanzenberger R, Silberbauer LR, Pacher D, Kasper S, Rupprecht R, et al. Meta-analysis of brain structural changes after electroconvulsive therapy in depression. Brain Stimul. 2021;14:927–37.
doi: 10.1016/j.brs.2021.05.014
pubmed: 34119669
Mulders PCR, Llera A, Beckmann CF, Vandenbulcke M, Stek M, Sienaert P, et al. Structural changes induced by electroconvulsive therapy are associated with clinical outcome. Brain Stimul. 2020;13:696–704.
doi: 10.1016/j.brs.2020.02.020
pubmed: 32289700
Merkel D. Docker: lightweight linux containers for consistent development and deployment. Linux J 2014;239:2. https://www.linuxjournal.com/content/docker-lightweight-linux-containers-consistent-development-and-deployment .
Jovicich J, Czanner S, Greve D, Haley E, van der Kouwe A, Gollub R, et al. Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. Neuroimage. 2006;30:436–43.
doi: 10.1016/j.neuroimage.2005.09.046
pubmed: 16300968
Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33:341–55.
doi: 10.1016/S0896-6273(02)00569-X
pubmed: 11832223
Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968–80.
doi: 10.1016/j.neuroimage.2006.01.021
pubmed: 16530430
Reuter M, Schmansky NJ, Rosas HD, Fischl B. Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage. 2012;61:1402–18.
doi: 10.1016/j.neuroimage.2012.02.084
pubmed: 22430496
O’Connor MK, Knapp R, Husain M, Rummans TA, Petrides G, Smith G, et al. The influence of age on the response of major depression to electroconvulsive therapy: a C.O.R.E. Report. Am J Geriatr Psychiatry. 2001;9:382–90.
doi: 10.1097/00019442-200111000-00006
pubmed: 11739064
van Diermen L, van den Ameele S, Kamperman AM, Sabbe BCG, Vermeulen T, Schrijvers D, et al. Prediction of electroconvulsive therapy response and remission in major depression: meta-analysis. Br J Psychiatry. 2018;212:71–80.
doi: 10.1192/bjp.2017.28
pubmed: 29436330
Socci C, Medda P, Toni C, Lattanzi L, Tripodi B, Vannucchi G, et al. Electroconvulsive therapy and age: age-related clinical features and effectiveness in treatment resistant major depressive episode. J Affect Disord. 2018;227:627–32.
doi: 10.1016/j.jad.2017.11.064
pubmed: 29172056
Gibson BC, Vakhtin A, Clark VP, Abbott CC, Quinn DK. Revisiting hemispheric asymmetry in mood regulation: implications for rTMS for major depressive disorder. Brain Sci. 2022;12. https://doi.org/10.3390/brainsci12010112 .
Sartorius A. Electric field distribution models in ECT research. Mol Psychiatry. 2022;27:3571–2.
doi: 10.1038/s41380-022-01516-8
pubmed: 35304563
pmcid: 9708590
Argyelan M, Lencz T, Kang S, Ali S, Masi PJ, Moyett E, et al. ECT-induced cognitive side effects are associated with hippocampal enlargement. Transl Psychiatry. 2021;11:516.
doi: 10.1038/s41398-021-01641-y
pubmed: 34625534
pmcid: 8501017
Elias GJB, Germann J, Loh A, Boutet A, Pancholi A, Beyn ME, et al. Habenular involvement in response to subcallosal cingulate deep brain stimulation for depression. Front Psychiatry. 2022;13:810777.
Chakravarty MM, Hamani C, Martinez-Canabal A, Ellegood J, Laliberté C, Nobrega JN, et al. Deep brain stimulation of the ventromedial prefrontal cortex causes reorganization of neuronal processes and vasculature. Neuroimage. 2016;125:422–7.
May A, Hajak G, Gänssbauer S, Steffens T, Langguth B, Kleinjung T, et al. Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity. Cereb Cortex. 2007;17:205–10.
Lan MJ, Chhetry BT, Liston C, Mann JJ, Dubin M. Transcranial Magnetic Stimulation of Left Dorsolateral Prefrontal Cortex Induces Brain Morphological Changes in Regions Associated with a Treatment Resistant Major Depressive Episode: An Exploratory Analysis. Brain Stimulat. 2016;9:577–83.
Boes AD, Uitermarkt BD, Albazron FM, Lan MJ, Liston C, Pascual-Leone A, et al. Rostral anterior cingulate cortex is a structural correlate of repetitive TMS treatment response in depression. Brain Stimulat. 2018;11:575–81.
Mayberg HS. Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatry Clin Neurosci. 1997;9:471–81.
Baron RM, Kenny DA. The moderator–mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol. 1986;51:1173–82.
doi: 10.1037/0022-3514.51.6.1173
pubmed: 3806354
Ousdal OT, Brancati GE, Kessler U, Erchinger V, Dale AM, Abbott C, et al. The neurobiological effects of electroconvulsive therapy studied through magnetic resonance: what have we learned, and where do we go? Biol Psychiatry. 2022;91:540–9.
doi: 10.1016/j.biopsych.2021.05.023
pubmed: 34274106
Gainotti G, Caltagirone C, Zoccolotti P. Left/right and cortical/subcortical dichotomies in the neuropsychological study of human emotions. Cogn Emot. 1993;7:71–93.
doi: 10.1080/02699939308409178
Gainotti G. Emotions and the right hemisphere: can new data clarify old models? Neuroscientist. 2019;25:258–70.