Graph theory analysis of whole brain functional connectivity to assess disturbances associated with suicide attempts in bipolar disorder.
Journal
Translational psychiatry
ISSN: 2158-3188
Titre abrégé: Transl Psychiatry
Pays: United States
ID NLM: 101562664
Informations de publication
Date de publication:
10 01 2022
10 01 2022
Historique:
received:
19
02
2021
accepted:
12
11
2021
revised:
25
10
2021
entrez:
11
1
2022
pubmed:
12
1
2022
medline:
1
2
2022
Statut:
epublish
Résumé
Brain targets to lower the high risk of suicide in Bipolar Disorder (BD) are needed. Neuroimaging studies employing analyses dependent on regional assumptions could miss hubs of dysfunction critical to the pathophysiology of suicide behaviors and their prevention. This study applied intrinsic connectivity distribution (ICD), a whole brain graph-theoretical approach, to identify hubs of functional connectivity (FC) disturbances associated with suicide attempts in BD. ICD, from functional magnetic resonance imaging data acquired while performing a task involving implicit emotion regulation processes important in BD and suicide behaviors, was compared across 40 adults with BD with prior suicide attempts (SAs), 49 with BD with no prior attempts (NSAs) and 51 healthy volunteers (HVs). Areas of significant group differences were used as seeds to identify regional FC differences and explore associations with suicide risk-related measures. ICD was significantly lower in SAs than in NSAs and HVs in bilateral ventromedial prefrontal cortex (vmPFC) and right anterior insula (RaIns). Seed connectivity revealed altered FC from vmPFC to bilateral anteromedial orbitofrontal cortex, left ventrolateral PFC (vlPFC) and cerebellum, and from RaIns to right vlPFC and temporopolar cortices. VmPFC and RaIns ICD were negatively associated with suicidal ideation severity, and vmPFC ICD with hopelessness and attempt lethality severity. The findings suggest that SAs with BD have vmPFC and RaIns hubs of dysfunction associated with altered FC to other ventral frontal, temporopolar and cerebellar cortices, and with suicidal ideation, hopelessness, and attempt lethality. These hubs may be targets for novel therapeutics to reduce suicide risk in BD.
Identifiants
pubmed: 35013103
doi: 10.1038/s41398-021-01767-z
pii: 10.1038/s41398-021-01767-z
pmc: PMC8748935
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7Subventions
Organisme : NIMH NIH HHS
ID : R01 MH113230
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001863
Pays : United States
Organisme : NIMH NIH HHS
ID : R61 MH111929
Pays : United States
Organisme : NIMH NIH HHS
ID : RC1 MH088366
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH069747
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH070902
Pays : United States
Organisme : NIMH NIH HHS
ID : UG3 MH111929
Pays : United States
Organisme : NIMH NIH HHS
ID : R24 MH114805
Pays : United States
Organisme : NCATS NIH HHS
ID : TL1 TR001864
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH121095
Pays : United States
Informations de copyright
© 2021. The Author(s).
Références
Abreu LND, Lafer B, Baca-Garcia E, Oquendo MA. Suicidal ideation and suicide attempts in bipolar disorder type I: An update for the clinician. Braz J Psychiatry. 2009;31:271–80.
pubmed: 19787156
doi: 10.1590/S1516-44462009005000003
Schmaal L, van Harmelen A-L, Chatzi V, Lippard ET, Toenders YJ, Averill LA. Imaging suicidal thoughts and behaviors: A comprehensive review of 2 decades of neuroimaging studies. Mol Psychiatry. 2020;25:408–27.
pubmed: 31787757
doi: 10.1038/s41380-019-0587-x
Pompili M, Gonda X, Serafini G, Innamorati M, Sher L, Amore M, et al. Epidemiology of suicide in bipolar disorders: A systematic review of the literature. Bipolar Disord. 2013;15:457–90.
pubmed: 23755739
doi: 10.1111/bdi.12087
Phillips ML, Ladouceur CD, Drevets WC. A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry. 2008;13:833.
doi: 10.1038/mp.2008.65
Sankar A, Purves K, Colic L, Lippard ETC, Millard H, Fan S, et al. Altered frontal cortex functioning in emotion regulation and hopelessness in bipolar disorder. Bipolar Disord. 2021;23:152–64.
pubmed: 32521570
doi: 10.1111/bdi.12954
Johnston JAY, Wang F, Liu J, Blond BN, Wallace A, Liu J, et al. Multimodal neuroimaging of frontolimbic structure and function associated with suicide attempts in adolescents and young adults with bipolar disorder. Am J Psychiatry. 2017;174:667–75.
pubmed: 28135845
pmcid: 5939580
doi: 10.1176/appi.ajp.2016.15050652
Benedetti F, Radaelli D, Poletti S, Locatelli C, Falini A, Colombo C, et al. Opposite effects of suicidality and lithium on gray matter volumes in bipolar depression. J Affect Disord. 2011;135:139–47.
pubmed: 21807414
doi: 10.1016/j.jad.2011.07.006
Giakoumatos CI, Tandon N, Shah J, Mathew IT, Brady RO, Clementz BA, et al. Are structural brain abnormalities associated with suicidal behavior in patients with psychotic disorders? J Psychiatr Res. 2013;47:1389–95.
pubmed: 23866739
pmcid: 4075042
doi: 10.1016/j.jpsychires.2013.06.011
Rigucci S, Sarubbi S, Erbuto D, Rogante E, Hantouche EG, Innamorati M, et al. Negative emotion dysregulation is linked to the intensity of suicidal ideation in a mixed inpatient sample. J Affect Disord. 2021;281:605–8.
pubmed: 33257041
doi: 10.1016/j.jad.2020.11.108
Vai B, Serretti A, Poletti S, Mascia M, Lorenzi C, Colombo C, et al. Cortico-limbic functional connectivity mediates the effect of early life stress on suicidality in bipolar depressed 5-HTTLPR* s carriers. J Affect Disord. 2020;263:420–7.
pubmed: 31969273
doi: 10.1016/j.jad.2019.11.142
Jiang H, Zhu R, Tian S, Wang H, Chen Z, Wang X, et al. Structural–functional decoupling predicts suicide attempts in bipolar disorder patients with a current major depressive episode. Neuropsychopharmacol. 2020;45:1735–42.
doi: 10.1038/s41386-020-0753-5
Wang H, Zhu R, Dai Z, Tian S, Shao J, Wang X, et al. Aberrant functional connectivity and graph properties in bipolar II disorder with suicide attempts. J Affect Disord. 2020;275:202–9.
pubmed: 32734909
doi: 10.1016/j.jad.2020.07.016
Cao J, Chen X, Chen J, Ai M, Gan Y, Wang W, et al. Resting-state functional MRI of abnormal baseline brain activity in young depressed patients with and without suicidal behavior. J Affect Disord. 2016;205:252–63.
pubmed: 27467529
doi: 10.1016/j.jad.2016.07.002
Scheinost D, Benjamin J, Lacadie C, Vohr B, Schneider KC, Ment LR, et al. The intrinsic connectivity distribution: A novel contrast measure reflecting voxel level functional connectivity. Neuroimage. 2012;62:1510–9.
pubmed: 22659477
doi: 10.1016/j.neuroimage.2012.05.073
Holmes SE, Scheinost D, Finnema SJ, Naganawa M, Davis MT, DellaGioia N, et al. Lower synaptic density is associated with depression severity and network alterations. Nat Commun. 2019;10:1–10.
doi: 10.1038/s41467-019-09562-7
Scheinost D, Holmes SE, DellaGioia N, Schleifer C, Matuskey D, Abdallah CG, et al. Multimodal investigation of network level effects using intrinsic functional connectivity, anatomical covariance, and structure-to-function correlations in unmedicated major depressive disorder. Neuropsychopharmacol. 2018;43:1119–27.
doi: 10.1038/npp.2017.229
Malhi GS, Das P, Outhred T, Bryant RA, Calhoun V, Mann JJ. Default mode dysfunction underpins suicidal activity in mood disorders. Psychol Med 2020;50:1214–23.
pubmed: 31144614
doi: 10.1017/S0033291719001132
Svensén M, Kruggel F, Benali H. ICA of fMRI group study data. NeuroImage. 2002;16:551–63.
pubmed: 12169242
doi: 10.1006/nimg.2002.1122
Garrison KA, Sinha R, Lacadie CM, Scheinost D, Jastreboff AM, Constable RT, et al. Functional connectivity during exposure to favorite-food, stress, and neutral-relaxing imagery differs between smokers and nonsmokers. Nicotine Tob Res. 2016;18:1820–9.
pubmed: 26995796
pmcid: 4978981
doi: 10.1093/ntr/ntw088
Mitchell MR, Balodis IM, DeVito EE, Lacadie CM, Yeston J, Scheinost D, et al. A preliminary investigation of Stroop-related intrinsic connectivity in cocaine dependence: associations with treatment outcomes. Am J Drug Alcohol Abus. 2013;39:392–402.
doi: 10.3109/00952990.2013.841711
Greene AS, Gao S, Scheinost D, Constable RT. Task-induced brain state manipulation improves prediction of individual traits. Nat Commun. 2018;9:1–13.
doi: 10.1038/s41467-018-04920-3
Phillips ML, Ladouceur CD, Drevets WC. A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry. 2008;13:833.
doi: 10.1038/mp.2008.65
Liu J, Blond BN, van Dyck LI, Spencer L, Wang F, Blumberg HP. Trait and state corticostriatal dysfunction in bipolar disorder during emotional face processing. Bipolar Disord. 2012;14:432–41.
pubmed: 22524493
pmcid: 3361579
doi: 10.1111/j.1399-5618.2012.01018.x
Wang F, McIntosh AM, He Y, Gelernter J, Blumberg HP. The association of genetic variation in CACNA1C with structure and function of a frontotemporal system. Bipolar Disord. 2011;13:696–700.
pubmed: 22085483
pmcid: 3233238
doi: 10.1111/j.1399-5618.2011.00963.x
Oquendo MA, Halberstam B, Mann JJ. Risk factors for suicidal behavior. Standardized Evaluation Clin Pract. 2003;22:103–29.
First MB Structured clinical interview for the DSM (SCID). The Encyclopedia of Clinical Psychology 2014:1–6.
Lish JD, Weissman MM, Adams PB, Hoven CW, Bird H. Family psychiatric screening instrument for epidemiologic studies: pilot testing and validation. Psychiatry Res. 1995;57:169–80.
pubmed: 7480383
doi: 10.1016/0165-1781(95)02632-7
Williams J, Link M, Rosenthal N, Terman M. Structured interview guide for the hamilton depression rating scale—Seasonal affective disorder version (SIGH-SAD). New York State Psychiatric Institute, New York 1988.
Young R, Biggs J, Ziegler V, Meyer D. A rating scale for mania: reliability, validity and sensitivity. Br J Psychiatry. 1978;133:429–35.
pubmed: 728692
doi: 10.1192/bjp.133.5.429
Beck AT, Weissman A, Lester D, Trexler L. The measurement of pessimism: The hopelessness scale. J Consult Clin Psychol. 1974;42:861.
pubmed: 4436473
doi: 10.1037/h0037562
Beck AT, Kovacs M, Weissman A. Assessment of suicidal intention: The scale for suicide ideation. J Consult Clin Psychol. 1979;47:343–52.
pubmed: 469082
doi: 10.1037/0022-006X.47.2.343
Beck AT, Beck R, Kovacs M. Classification of suicidal behaviors: I. Quantifying intent and medical lethality. Am J Psychiatry. 1975;132:285–7.
pubmed: 1115273
doi: 10.1176/ajp.132.3.285
Wang F, Bobrow L, Liu J, Spencer L, Blumberg HP. Corticolimbic functional connectivity in adolescents with bipolar disorder. PloS One. 2012;7:e50177.
pubmed: 23185566
pmcid: 3503984
doi: 10.1371/journal.pone.0050177
Scheinost D, Papademetris X, Constable RT. The impact of image smoothness on intrinsic functional connectivity and head motion confounds. Neuroimage. 2014;95:13–21.
pubmed: 24657356
doi: 10.1016/j.neuroimage.2014.03.035
Mazziotta JC, Toga AW, Evans A, Fox P, Lancaster J. A probabilistic atlas of the human brain: theory and rationale for its development. Neuroimage. 1995;2:89–101.
pubmed: 9343592
doi: 10.1006/nimg.1995.1012
Rubinov M, Sporns O. Complex network measures of brain connectivity: Uses and interpretations. Neuroimage. 2010;52:1059–69.
pubmed: 19819337
doi: 10.1016/j.neuroimage.2009.10.003
Thomason ME, Scheinost D, Manning JH, Grove LE, Hect J, Marshall N, et al. Weak functional connectivity in the human fetal brain prior to preterm birth. Sci Rep. 2017;7:1–10.
doi: 10.1038/srep39286
Gyurak A, Gross JJ, Etkin A. Explicit and implicit emotion regulation: A dual-process framework. Cogn Emot. 2011;25:400–12.
pubmed: 21432682
pmcid: 3280343
doi: 10.1080/02699931.2010.544160
Malhi GS, Bargh DM, Kuiper S, Coulston CM, Das P. Modeling bipolar disorder suicidality. Bipolar Disord. 2013;15:559–74.
pubmed: 23848394
doi: 10.1111/bdi.12093
Fan S, Lippard ET, Sankar A, Wallace A, Johnston JA, Wang F, et al. Gray and white matter differences in adolescents and young adults with prior suicide attempts across bipolar and major depressive disorders. J Affect Disord. 2019;245:1089–97.
pubmed: 30699851
doi: 10.1016/j.jad.2018.11.095
Just MA, Pan L, Cherkassky VL, McMakin DL, Cha C, Nock MK, et al. Machine learning of neural representations of suicide and emotion concepts identifies suicidal youth. Nat. Human. Behav. 2017;1:911.
Hallensleben N, Glaesmer H, Forkmann T, Rath D, Strauss M, Kersting A, et al. Predicting suicidal ideation by interpersonal variables, hopelessness and depression in real-time. An ecological momentary assessment study in psychiatric inpatients with depression. Eur Psychiatry. 2019;56:43–50.
pubmed: 30530103
doi: 10.1016/j.eurpsy.2018.11.003
Durant T, Mercy J, Kresnow M-J, Simon T, Potter L, Hammond WR. Racial differences in hopelessness as a risk factor for a nearly lethal suicide attempt. J Black Psychol. 2006;32:285–302.
doi: 10.1177/0095798406290468
Schutter DJ, van Honk J. The cerebellum in emotion regulation: A repetitive transcranial magnetic stimulation study. Cerebellum. 2009;8:28–34.
pubmed: 18855096
doi: 10.1007/s12311-008-0056-6
Schmahmann JD, Weilburg JB, Sherman JC. The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum. 2007;6:254–67.
pubmed: 17786822
doi: 10.1080/14734220701490995
Schraa-Tam CK, Rietdijk WJ, Verbeke WJ, Dietvorst RC, Van Den Berg WE, Bagozzi RP, et al. fMRI activities in the emotional cerebellum: a preference for negative stimuli and goal-directed behavior. Cerebellum. 2012;11:233–45.
pubmed: 21761197
doi: 10.1007/s12311-011-0301-2
Kang S-G, Na K-S, Choi J-W, Kim J-H, Son Y-D, Lee YJ. Resting-state functional connectivity of the amygdala in suicide attempters with major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2017;77:222–7.
pubmed: 28445688
doi: 10.1016/j.pnpbp.2017.04.029
Pan L, Hassel S, Segreti A, Nau S, Brent D, Phillips ML. Differential patterns of activity and functional connectivity in emotion processing neural circuitry to angry and happy faces in adolescents with and without suicide attempt. Psychol Med. 2013;43:2129–42.
pubmed: 23298821
doi: 10.1017/S0033291712002966
Menon V, Uddin LQ. Saliency, switching, attention and control: A network model of insula function. Brain Struct Funct. 2010;214:655–67.
pubmed: 20512370
pmcid: 2899886
doi: 10.1007/s00429-010-0262-0
Zubieta J-K, Smith YR, Bueller JA, Xu Y, Kilbourn MR, Jewett DM, et al. Regional mu opioid receptor regulation of sensory and affective dimensions of pain. Science. 2001;293:311–5.
pubmed: 11452128
doi: 10.1126/science.1060952
Ochsner KN, Zaki J, Hanelin J, Ludlow DH, Knierim K, Ramachandran T, et al. Your pain or mine? Common and distinct neural systems supporting the perception of pain in self and other. Soc Cogn Affect Neurosci. 2008;3:144–60.
pubmed: 19015105
pmcid: 2555461
doi: 10.1093/scan/nsn006
Liberzon I, Taylor SF, Phan KL, Britton JC, Fig LM, Bueller JA, et al. Altered central μ-opioid receptor binding after psychological trauma. Biol Psychiatry. 2007;61:1030–8.
pubmed: 16945349
doi: 10.1016/j.biopsych.2006.06.021
Ducasse D, Holden RR, Boyer L, Artero S, Calati R, Guillaume S, et al. Psychological pain in suicidality: A meta-analysis. J. Clin. Psychol. 2017;79:0–0.
Nutt DJ. The role of the opioid system in alcohol dependence. J Psychopharmacol. 2014;28:8–22.
pubmed: 24048097
doi: 10.1177/0269881113504017
Strosche A, Zhang X, Kirsch M, Hermann D, Ende G, Kiefer F, et al. Investigation of brain functional connectivity to assess cognitive control over cue-processing in alcohol use disorder. Addict Biol. 2021;26:e12863.
pubmed: 31908107
doi: 10.1111/adb.12863
Mesulam M-M. Principles of behavioral and cognitive neurology. Oxford University Press 2000.
Mesulam M-M, Mufson EJ. The insula of Reil in man and monkey. Association and Auditory Cortices. Springer 1985, pp 179–226.
Wang F, Kalmar JH, Womer FY, Edmiston EE, Chepenik LG, Chen R, et al. Olfactocentric paralimbic cortex morphology in adolescents with bipolar disorder. Brain. 2011;134:2005–12.
pubmed: 21666263
pmcid: 3122371
doi: 10.1093/brain/awr124
Lippard ETC, Johnston JA, Spencer L, Quatrano S, Fan S, Sankar A, et al. Preliminary examination of gray and white matter structure and longitudinal structural changes in frontal systems associated with future suicide attempts in adolescents and young adults with mood disorders. J Affect Disord. 2019;245:1139–48.
pubmed: 30699858
doi: 10.1016/j.jad.2018.11.097
Bolding MS, White DM, Hadley JA, Weiler M, Holcomb HH, Lahti AC. Antipsychotic drugs alter functional connectivity between the medial frontal cortex, hippocampus, and nucleus accumbens as measured by H215O PET. Front Psychiatry. 2012;3:105.
pubmed: 23230425
pmcid: 3515723
doi: 10.3389/fpsyt.2012.00105
Sheridan MA, Hinshaw S, D’Esposito M. Stimulant medication and prefrontal functional connectivity during working memory in ADHD: A preliminary report. J Atten Disord. 2010;14:69–78.
pubmed: 20576647
pmcid: 2935299
doi: 10.1177/1087054709347444
Chopra S, Francey SM, O’Donoghue B, Sabaroedin K, Arnatkeviciute A, Cropley V et al. Functional Connectivity in Antipsychotic-Treated and Antipsychotic-Naive Patients With First-Episode Psychosis and Low Risk of Self-harm or Aggression. JAMA Psychiatry 2021;78:994–1004.
Allen M, Poggiali D, Whitaker K, Marshall TR, Kievit RA. Raincloud plots: A multi-platform tool for robust data visualization. Wellcome Open Res. 2019; 4:63.