Dynamic functional connectivity reveals altered variability in functional connectivity among patients with major depressive disorder

Human Brain Mapping

Volumn 37, Issue 8, 2016, Pages 2918-2930

  Demirtaş, Murat ^a   Tornador, Cristian ^a   Falcón, Carles ^b,c   López Solà, Marina ^d,e   Hernández Ribas, Rosa ^f,g   Pujol, Jesús ^e   Menchón, José M ^f,g,h   Ritter, Petra ^i,j   Cardoner, Narcis ^g,k   Soriano Mas, Carles ^f,g,l   Deco, Gustavo ^a,m  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b Clinical Research Program   (Spain)

^c BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^d UNIVERSITY OF COLORADO   (United States)

^e HOSPITAL DEL MAR   (Spain)

^f CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE SALUD MENTAL CIBERSAM   (Spain)

^g HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^h UNIVERSITY OF BARCELONA   (Spain)

ⁱ MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

^j CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^k Depression and Anxiety Program   (Spain)

^l UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^m INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

more..

Author keywords

dynamic functional connectivity; fMRI; major depressive disorder; mood disorders; resting state

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; DEFAULT MODE NETWORK; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MAJOR DEPRESSION; MALE; PRIORITY JOURNAL;

EID: 84978880729     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.23215     Document Type: Article

References (44)

1. Alexopoulos GS, Hoptman MJ, Kanellopoulos D, Murphy CF, Lim KO, Gunning FM (2012): Functional connectivity in the cognitive control network and the default mode network in late-life depression. J Affect Disord 139:56–65. doi:10.1016/j.jad.2011.12.002.
2. Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD. 2014. Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex. 24:663–676. doi:10.1093/cercor/bhs352.
3. Anand A, Li Y, Wang Y, Wu J, Gao S, Bukhari L, Mathews VP, Kalnin A, Lowe MJ (2005): Activity and connectivity of brain mood regulating circuit in depression: A functional magnetic resonance study. Biol Psychiatry 57:1079–1088. doi:10.1016/j.biopsych.2005.02.021.
4. Avery JA, Drevets WC, Moseman SE, Bodurka J, Barcalow JC, Kyle Simmons W. 2014. Major depressive disorder is associated with abnormal interoceptive activity and functional connectivity in the insula. Biol Psychiatry 76: 258–266. doi:10.1016/j.biopsych.2013.11.027.
5. Berman MG, Misic B, Buschkuehl M, Kross E, Deldin PJ, Peltier S, Churchill NW, Jaeggi SM, Vakorin V, McIntosh AR, Jonides J (2014): Does resting-state connectivity reflect depressive rumination? A tale of two analyses. Neuroimage 103:267–279. doi:10.1016/j.neuroimage.2014.09.027.
6. Berman MG, Peltier S, Evan Nee D, Kross E, Deldin PJ, Jonides J (2011): Depression, rumination and the default network. Soc Cognit Affect Neurosci 6:548–555. doi:10.1093/scan/nsq080.
7. Bluhm R, Williamson P, Lanius R, Théberge J, Densmore M, Bartha R, Neufeld R, Osuch E (2009): Resting state default-mode network connectivity in early depression using a seed region-of-interest analysis: Decreased connectivity with caudate nucleus. Psychiatry Clin Neurosci 63:754–761. doi:10.1111/j.1440-1819.2009.02030.x.
8. Bohr IJ, Kenny E, Blamire A, O'Brien JT, Thomas A, Richardson J, Kaiser M (2013): Resting-state functional connectivity in late-life depression: Higher global connectivity and more long distance connections. Neuropsychiatr Imag Stimul 3:116. doi:10.3389/fpsyt.2012.00116.
9. Connolly CG, Wu J, Ho TC, Hoeft F, Wolkowitz O, Eisendrath S, Frank G, Hendren R, Max JE, Paulus MP, Tapert SF, Banerjee D, Simmons AN, Yang TT (2013): Resting-state functional connectivity of subgenual anterior cingulate cortex in depressed adolescents. Biol Psychiatry 74:898–907. doi:10.1016/j.biopsych.2013.05.036.
10. Cullen KR, Gee DG, Klimes-Dougan B, Gabbay V, Hulvershorn L, Mueller BA, Camchong J, Bell CJ, Houri A, Kumra S, Lim KO, Castellanos FX, Milham MP (2009): A preliminary study of functional connectivity in comorbid adolescent depression. Neurosci Lett 460:227–231. doi:10.1016/j.neulet.2009.05.022.
11. Damaraju E, Allen EA, Belger A, Ford JM, McEwen S, Mathalon DH, Mueller BA, Pearlson GD, Potkin SG, Preda A, Turner JA, Vaidya JG, van Erp TG, Calhoun VD (2014): Dynamic functional connectivity analysis reveals transient states of dysconnectivity in schizophrenia. Neuroimage 5:298–308. doi:10.1016/j.nicl.2014.07.003.
12. Fan J, Xu P, Van Dam NT, Eilam-Stock T, Gu X, Luo Y, Hof PR (2012): Spontaneous brain activity relates to autonomic arousal. J Neurosci 32:11176–11186. doi:10.1523/JNEUROSCI.1172-12.2012.
13. Ferrari AJ, Charlson FJ, Norman RE, Patten SB, Freedman G, Murray CJL, Vos T, Whiteford HA (2013): Burden of depressive disorders by country, sex, age, and year: Findings from the Global Burden of Disease Study 2010. PLoS Med 10:e1001547. doi:10.1371/journal.pmed.1001547.
14. Glerean E, Salmi J, Lahnakoski JM, Jaaskelainen IP, Sams M (2012): Functional magnetic resonance imaging phase synchronization as a measure of dynamic functional connectivity. Brain Connect 2:91–101. doi:10.1089/brain.2011.0068.
15. Gong Q, He Y (2015): Depression, neuroimaging and connectomics: A selective overview. Biol Psychiatry 77:223–235. doi:10.1016/j.biopsych.2014.08.009.
16. Greicius MD, Flores BH, Menon V, Glover GH, Solvason HB, Kenna H, Reiss AL, Schatzberg AF (2007): Resting-state functional connectivity in major depression: Abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 62:429–437. doi:10.1016/j.biopsych.2006.09.020.
17. Grimm S, Ernst J, Boesiger P, Schuepbach D, Boeker H, Northoff G (2011): Reduced negative BOLD responses in the default-mode network and increased self-focus in depression. World J Biol Psychiatry 12:627–637. doi:10.3109/15622975.2010.545145.
18. Guo W-b, Sun X-l, Liu L, Xu Q, Wu R-R, Liu Z-n, Tan C-l, Chen H-f, Zhao J-P (2011): Disrupted regional homogeneity in treatment-resistant depression: A resting-state fMRI study. Prog Neuropsychopharmacol Biol Psychiatry 35:1297–1302. doi:10.1016/j.pnpbp.2011.02.006.
19. Hamilton JP, Furman DJ, Chang C, Thomason ME, Dennis E, Gotlib IH. 2011. Default-mode and task-positive network activity in major depressive disorder: Implications for adaptive and maladaptive rumination. Biol Psychiatry70: 327–333. doi:10.1016/j.biopsych.2011.02.003.
20. Hochberg Y, Benjamini Y (1990): More powerful procedures for multiple significance testing. Stat Med 9:811–818. doi:10.1002/sim.4780090710.
21. Li B, Liu L, Friston KJ, Shen H, Wang L, Zeng L-L, Hu D. 2013. A treatment-resistant default mode subnetwork in major depression. Biol Psychiatry74: 48–54. doi:10.1016/j.biopsych.2012.11.007.
22. Liston C, Chen AC, Zebley BD, Drysdale AT, Gordon R, Leuchter B, Voss HU, Casey BJ, Etkin A, Dubin MJ. 2014. Default mode network mechanisms of transcranial magnetic stimulation in depression. Biol Psychiatry 76: 517–526. doi:10.1016/j.biopsych.2014.01.023.
23. Lui S, Wu Q, Qiu L, Yang X, Kuang W, Chan RCK, Huang X, Kemp GJ, Mechelli A, Gong Q (2011): Resting-state functional connectivity in treatment-resistant depression. Am J Psychiatry 168:642–648. doi:10.1176/appi.ajp.2010.10101419.
24. Ponce-Alvarez A, Deco G, Hagmann P, Luca Romani G, Mantini D, Corbetta M (2015): Resting-state temporal synchronization networks emerge from connectivity topology and heterogeneity. PLoS Comput Biol 11:e1004100. doi:10.1371/journal.pcbi.1004100.
25. Prichard D, Theiler J (1994): Generating surrogate data for time series with several simultaneously measures variables. Phys Rev Lett 73:951–954.
26. Ramasubbu R, Konduru N, Cortese F, Bray S, Gaxiola I, Goodyear B (2014): Reduced intrinsic connectivity of amygdala in adults with major depressive disorder. Neuropsychiatr Imag Stimul 5:17. doi:10.3389/fpsyt.2014.00017.
27. Rashid B, Damaraju E, Pearlson GD, Calhoun VD (2014): Dynamic connectivity states estimated from resting fMRI identify differences among schizophrenia, bipolar disorder, and healthy control subjects. Front Hum Neurosci 8:897. doi:10.3389/fnhum.2014.00897.
28. Ritter P, Becker R, Freyer F, Villringer A. 2009. EEG quality: The image acquisition artefact. In: Christoph M, Louis L, editors. EEG - fMRI. Berlin, Germany: Springer Berlin Heidelberg. pp. 153–171. http://link.springer.com/chapter/10.1007/978-3-540-87919-0_9.
29. Schirner M, Rothmeier S, Ritter P. 2013. Constructing subject-specific virtual brains from multimodal neuroimaging data. Front Neurosci Conference Abstract: Neuroinformatics 2015. doi:10.3389/conf.fnins.2015.91.00005.
30. Sheline YI, Price JL, Yan Z, Mintun MA (2010): Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proc Natl Acad Sci USA 107:11020–11025. doi:10.1073/pnas.1000446107.
31. Tagliazucchi E, Von Wegner F, Morzelewski A, Brodbeck V, Laufs H (2012): Dynamic BOLD functional connectivity in humans and its electrophysiological correlates. Front Hum Neurosci 6:339. doi:10.3389/fnhum.2012.00339.
32. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002): Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289. doi:10.1006/nimg.2001.0978.
33. Veer IM, Beckmann C, Van Tol M-J, Ferrarini L, Milles J, Veltman D, Aleman A, Van Buchem MA, Van Der Wee NJA, Rombouts SAR (2010): Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Front Syst Neurosci 4:41. doi:10.3389/fnsys.2010.00041.
34. Wang L, Hermens DF, Hickie IB, Lagopoulos J (2012): A systematic review of resting-state functional-MRI studies in major depression. J Affect Disord 142:6–12. doi:10.1016/j.jad.2012.04.013.
35. Wang L, Li K, Zhang QE, Zeng YW, Jin Z, Dai WJ, Su YA, Wang G, Tan YL, Yu X, Si TM (2013): Interhemispheric functional connectivity and its relationships with clinical characteristics in major depressive disorder: A resting state fMRI study. PLoS One 8:e60191. doi:10.1371/journal.pone.0060191.
36. Wee C-Y, Yap P-T, Denny K, Browndyke JN, Potter GG, Welsh-Bohmer KA, Wang L, Shen D (2012): Resting-state multi-spectrum functional connectivity networks for identification of MCI patients. PLoS ONE 7:e37828. doi:10.1371/journal.pone.0037828.
37. Wei M, Qin J, Yan R, Li H, Yao Z, Lu Q (2013): Identifying major depressive disorder using hurst exponent of resting-state brain networks. Psychiatry Res Neuroimag 214:306–312. doi:10.1016/j.pscychresns.2013.09.008.
38. Wei M, Qin J, Yan R, Bi K, Liu C, Yao Z, Lu Q (2015): Association of resting-state network dysfunction with their dynamics of inter-network interactions in depression. J Affect Disord 174:527–534. doi:10.1016/j.jad.2014.12.020.
39. Wittchen HU, Jacobi F, Rehm J, Gustavsson A, Svensson M, Jönsson B, Olesen J, Allgulander C, Alonso J, Faravelli C, Fratiglioni L, Jennum P, Lieb R, Maercker A, van Os J, Preisig M, Salvador-Carulla L, Simon R, Steinhausen HC (2011): The size and burden of mental disorders and other disorders of the brain in Europe 2010. Eur Neuropsychopharmacol 21:655–679. doi:10.1016/j.euroneuro.2011.07.018.
40. Xia M, Wang J, He Y (2013): BrainNet viewer: A network visualization tool for human brain connectomics. PLoS One 8:e68910. doi:10.1371/journal.pone.0068910.
41. Yang GJ, Murray JD, Repovs G, Cole MW, Savic A, Glasser MF, Pittenger C, Krystal JH, Wang XJ, Pearlson GD, Glahn DC, Anticevic A (2014): Altered global brain signal in schizophrenia. Proc Natl Acad Sci USA 111:7438–7443. doi:10.1073/pnas.1405289111.
42. Yu Q, Erhardt EB, Sui J, Du Y, He H, Hjelm D Cetin MS, et al. (2015): Assessing dynamic brain graphs of time-varying connectivity in FMRI data: Application to healthy controls and patients with schizophrenia. Neuroimage 107:345–355. doi:10.1016/j.neuroimage.2014.12.020.
43. Zalesky A, Fornito A, Bullmore ET (2010): Network-based statistic: identifying differences in brain networks. Neuroimage 53:1197–1207. doi:10.1016/j.neuroimage.2010.06.041.
44. Zhou Y, Yu C, Zheng H, Liu Y, Song M, Qin W, Li K, Jiang T (2010): Increased neural resources recruitment in the intrinsic organization in major depression. J Affect Disord 121:220–230. doi:10.1016/j.jad.2009.05.029.