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History of suicide attempt associated with amygdala and hippocampus changes among individuals with schizophrenia

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European Archives of Psychiatry and Clinical Neuroscience Aims and scope Submit manuscript

Abstract

Abnormalities in subcortical brain structures may reflect higher suicide risk in mood disorders, but less is known about its associations for schizophrenia. This cross-sectional imaging study aimed to explore whether the history of suicide attempts was associated with subcortical changes among individuals with schizophrenia. We recruited 44 individuals with schizophrenia and a history of suicide attempts (SZ-SA) and 44 individuals with schizophrenia but without a history of suicide attempts (SZ-NSA) and 44 healthy controls. Linear regression showed that SZ-SA had smaller volumes of the hippocampus (Cohen’s d = −0.72), the amygdala (Cohen’s d = −0.69), and some nuclei of the amygdala (Cohen’s d, −0.57 to −0.72) than SZ-NSA after adjusting for age, sex, illness phase, and intracranial volume. There was no difference in the volume of the subfields of the hippocampus. It suggests the history of suicide attempts is associated with subcortical volume alterations in schizophrenia.

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References

  1. Lu L, Dong M, Zhang L, Zhu XM, Ungvari GS, Ng CH, Wang G, Xiang YT (2019) Prevalence of suicide attempts in individuals with schizophrenia: a meta-analysis of observational studies. Epidemiol Psychiatr Sci 29:e39. https://doi.org/10.1017/S2045796019000313

    Article  PubMed  PubMed Central  Google Scholar 

  2. Nock MK, Borges G, Bromet EJ, Alonso J, Angermeyer M, Beautrais A, Bruffaerts R, Chiu WT, De Girolamo G, Gluzman S, De Graaf R, Gureje O, Haro JM, Huang Y, Karam E, Kessler RC, Lepine JP, Levinson D, Medina-Mora ME, Ono Y, Posada-Villa J, Williams D (2008) Cross-national prevalence and risk factors for suicidal ideation, plans and attempts. Br J Psychiatry 192(2):98–105. https://doi.org/10.1192/bjp.bp.107.040113

    Article  PubMed  PubMed Central  Google Scholar 

  3. World Health Organization (2021) Suicide worldwide in 2019: Global health estimates. World Health Organization, Geneva

    Google Scholar 

  4. Fu XL, Qian Y, Jin XH, Yu HR, Wu H, Du L, Chen HL, Shi YQ (2021) Suicide rates among people with serious mental illness: a systematic review and meta-analysis. Psychol Med. https://doi.org/10.1017/s0033291721001549

    Article  PubMed  Google Scholar 

  5. Dong M, Zeng LN, Lu L, Li XH, Ungvari GS, Ng CH, Chow IHI, Zhang L, Zhou Y, Xiang YT (2019) Prevalence of suicide attempt in individuals with major depressive disorder: a meta-analysis of observational surveys. Psychol Med 49(10):1691–1704. https://doi.org/10.1017/s0033291718002301

    Article  PubMed  Google Scholar 

  6. Yin Y, Tong J, Huang J, Tian B, Chen S, Tan S, Wang Z, Yang F, Tong Y, Fan F, Kochunov P, Tan Y, Hong LE (2022) Auditory hallucinations, depressive symptoms, and current suicidal ideation or behavior among patients with acute-episode schizophrenia. Arch Suicide Res. https://doi.org/10.1080/13811118.2021.1993399

    Article  Google Scholar 

  7. Chang Q, Wu D, Rong H, Wu Z, Tao W, Liu H, Zhou P, Luo G, Xie G, Huang S, Qian C, Yuan Y, Yip PSF, Liu T (2019) Suicide ideation, suicide attempts, their sociodemographic and clinical associates among the elderly Chinese patients with schizophrenia spectrum disorders. J Affect Disord 256:611–617. https://doi.org/10.1016/j.jad.2019.06.069

    Article  PubMed  Google Scholar 

  8. Yin Y, Tong J, Huang J, Tian B, Chen S, Cui Y, An H, Tan S, Wang Z, Yang F, Tian L, Tong Y, Hong LE, Tan Y (2020) Suicidal ideation, suicide attempts, and neurocognitive dysfunctions among patients with first-episode schizophrenia. Suicide Life Threat Behav 50:1181–1188. https://doi.org/10.1111/sltb.12689

    Article  PubMed  Google Scholar 

  9. Bornheimer LA, Wojtalik JA, Li J, Cobia D, Smith MJ (2021) Suicidal ideation in first-episode psychosis: considerations for depression, positive symptoms, clinical insight, and cognition. Schizophr Res 228:298–304. https://doi.org/10.1016/j.schres.2020.12.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Mann JJ, Rizk MM (2020) A brain-centric model of suicidal behavior. Am J Psychiatry 177(10):902–916. https://doi.org/10.1176/appi.ajp.2020.20081224

    Article  PubMed  PubMed Central  Google Scholar 

  11. Van Velzen LS, Dauvermann MR, Colic L, Villa LM, Savage HS, Toenders YJ, Zhu AH, Bright JK, Campos AI, Salminen LE, Ambrogi S, Ayesa-Arriola R, Banaj N, Basgoze Z, Bauer J, Blair K, Blair RJ, Brosch K, Cheng Y, Colle R, Connolly CG, Corruble E, Couvy-Duchesne B, Crespo-Facorro B, Cullen KR, Dannlowski U, Davey CG, Dohm K, Fullerton JM, Gonul AS, Gotlib IH, Grotegerd D, Hahn T, Harrison BJ, He M, Hickie IB, Ho TC, Iorfino F, Jansen A, Jollant F, Kircher T, Klimes-Dougan B, Klug M, Leehr EJ, Lippard ETC, Mclaughlin KA, Meinert S, Miller AB, Mitchell PB, Mwangi B, Nenadic I, Ojha A, Overs BJ, Pfarr JK, Piras F, Ringwald KG, Roberts G, Romer G, Sanches M, Sheridan MA, Soares JC, Spalletta G, Stein F, Teresi GI, Tordesillas-Gutierrez D, Uyar-Demir A, Van Der Wee NJA, Van Der Werff SJ, Vermeiren R, Winter A, Wu MJ, Yang TT, Thompson PM, Renteria ME, Jahanshad N, Blumberg HP, Van Harmelen AL, Thoughts ES, Behaviours C, Schmaal L (2022) Structural brain alterations associated with suicidal thoughts and behaviors in young people: Results from 21 international studies from the ENIGMA suicidal thoughts and behaviours consortium. Mol Psychiatry. https://doi.org/10.1038/s41380-022-01734-0

    Article  PubMed  PubMed Central  Google Scholar 

  12. Besteher B, Wagner G, Koch K, Schachtzabel C, Reichenbach JR, Schlosser R, Sauer H, Schultz CC (2016) Pronounced prefronto-temporal cortical thinning in schizophrenia: Neuroanatomical correlate of suicidal behavior? Schizophr Res 176(2–3):151–157. https://doi.org/10.1016/j.schres.2016.08.010

    Article  PubMed  Google Scholar 

  13. Yin Y, Tong J, Huang J, Tian B, Chen S, Tan S, Wang Z, Yang F, Tong Y, Fan F, Kochunov P, Jahanshad N, Li CR, Hong LE, Tan Y (2022) History of suicide attempts associated with the thinning right superior temporal gyrus among individuals with schizophrenia. Brain Imaging Behav 16(4):1893–1901. https://doi.org/10.1007/s11682-021-00624-3

    Article  PubMed  PubMed Central  Google Scholar 

  14. Campos AI, Thompson PM, Veltman DJ, Pozzi E, Van Veltzen LS, Jahanshad N, Adams MJ, Baune BT, Berger K, Brosch K, Bülow R, Connolly CG, Dannlowski U, Davey CG, De Zubicaray GI, Dima D, Erwin-Grabner T, Evans JW, Fu CHY, Gotlib IH, Goya-Maldonado R, Grabe HJ, Grotegerd D, Harris MA, Harrison BJ, Hatton SN, Hermesdorf M, Hickie IB, Ho TC, Kircher T, Krug A, Lagopoulos J, Lemke H, Mcmahon K, Macmaster FP, Martin NG, Mcintosh AM, Medland SE, Meinert S, Meller T, Nenadic I, Opel N, Redlich R, Reneman L, Repple J, Sacchet MD, Schmitt S, Schrantee A, Sim K, Singh A, Stein F, Strike LT, Van Der Wee NJA, Van Der Werff SJA, Völzke H, Waltemate L, Whalley HC, Wittfeld K, Wright MJ, Yang TT, Zarate CA, Schmaal L, Rentería ME (2021) Brain correlates of suicide attempt in 18,925 participants across 18 international cohorts. Biol Psychiatry 90(4):243–252. https://doi.org/10.1016/j.biopsych.2021.03.015

    Article  PubMed  PubMed Central  Google Scholar 

  15. Pan LA, Ramos L, Segreti A, Brent DA, Phillips ML (2015) Right superior temporal gyrus volume in adolescents with a history of suicide attempt. Br J Psychiatry 206(4):339–340. https://doi.org/10.1192/bjp.bp.114.151316

    Article  PubMed  PubMed Central  Google Scholar 

  16. Dimick MK, Kennedy KG, Mitchell RHB, Sinyor M, Macintosh BJ, Goldstein BI (2021) Neurostructural differences associated with self-harm in youth bipolar disorder. Bipolar Disord 24(3):275–285. https://doi.org/10.1111/bdi.13137

    Article  PubMed  Google Scholar 

  17. Van Erp TG, Hibar DP, Rasmussen JM, Glahn DC, Pearlson GD, Andreassen OA, Agartz I, Westlye LT, Haukvik UK, Dale AM, Melle I, Hartberg CB, Gruber O, Kraemer B, Zilles D, Donohoe G, Kelly S, Mcdonald C, Morris DW, Cannon DM, Corvin A, Machielsen MW, Koenders L, De Haan L, Veltman DJ, Satterthwaite TD, Wolf DH, Gur RC, Gur RE, Potkin SG, Mathalon DH, Mueller BA, Preda A, Macciardi F, Ehrlich S, Walton E, Hass J, Calhoun VD, Bockholt HJ, Sponheim SR, Shoemaker JM, Van Haren NE, Hulshoff Pol HE, Ophoff RA, Kahn RS, Roiz-Santianez R, Crespo-Facorro B, Wang L, Alpert KI, Jonsson EG, Dimitrova R, Bois C, Whalley HC, Mcintosh AM, Lawrie SM, Hashimoto R, Thompson PM, Turner JA (2016) Subcortical brain volume abnormalities in 2028 individuals with schizophrenia and 2540 healthy controls via the ENIGMA consortium. Mol Psychiatry 21(4):547–553. https://doi.org/10.1038/mp.2015.63

    Article  PubMed  Google Scholar 

  18. Gutman BA, Van Erp TGM, Alpert K, Ching CRK, Isaev D, Ragothaman A, Jahanshad N, Saremi A, Zavaliangos-Petropulu A, Glahn DC, Shen L, Cong S, Alnaes D, Andreassen OA, Doan NT, Westlye LT, Kochunov P, Satterthwaite TD, Wolf DH, Huang AJ, Kessler C, Weideman A, Nguyen D, Mueller BA, Faziola L, Potkin SG, Preda A, Mathalon DH, Bustillo J, Calhoun V, Ford JM, Walton E, Ehrlich S, Ducci G, Banaj N, Piras F, Piras F, Spalletta G, Canales-Rodríguez EJ, Fuentes-Claramonte P, Pomarol-Clotet E, Radua J, Salvador R, Sarró S, Dickie EW, Voineskos A, Tordesillas-Gutiérrez D, Crespo-Facorro B, Setién-Suero E, Van Son JM, Borgwardt S, Schönborn-Harrisberger F, Morris D, Donohoe G, Holleran L, Cannon D, Mcdonald C, Corvin A, Gill M, Filho GB, Rosa PGP, Serpa MH, Zanetti MV, Lebedeva I, Kaleda V, Tomyshev A, Crow T, James A, Cervenka S, Sellgren CM, Fatouros-Bergman H, Agartz I, Howells F, Stein DJ, Temmingh H, Uhlmann A, De Zubicaray GI, Mcmahon KL, Wright M, Cobia D, Csernansky JG, Thompson PM, Turner JA, Wang L (2022) A meta-analysis of deep brain structural shape and asymmetry abnormalities in 2,833 individuals with schizophrenia compared with 3,929 healthy volunteers via the ENIGMA consortium. Hum Brain Mapp 43(1):352–372. https://doi.org/10.1002/hbm.25625

    Article  PubMed  Google Scholar 

  19. Spoletini I, Piras F, Fagioli S, Rubino IA, Martinotti G, Siracusano A, Caltagirone C, Spalletta G (2011) Suicidal attempts and increased right amygdala volume in schizophrenia. Schizophr Res 125(1):30–40. https://doi.org/10.1016/j.schres.2010.08.023

    Article  PubMed  Google Scholar 

  20. Colle R, Chupin M, Cury C, Vandendrie C, Gressier F, Hardy P, Falissard B, Colliot O, Ducreux D, Corruble E (2015) Depressed suicide attempters have smaller hippocampus than depressed patients without suicide attempts. J Psychiatr Res 61:13–18. https://doi.org/10.1016/j.jpsychires.2014.12.010

    Article  PubMed  Google Scholar 

  21. Kim DJ, Bartlett EA, Delorenzo C, Parsey RV, Kilts C, Cáceda R (2021) Examination of structural brain changes in recent suicidal behavior. Psychiatry Res Neuroimaging 307:111216. https://doi.org/10.1016/j.pscychresns.2020.111216

    Article  PubMed  Google Scholar 

  22. Wang L, Zhao Y, Edmiston EK, Womer FY, Zhang R, Zhao P, Jiang X, Wu F, Kong L, Zhou Y, Tang Y, Wei S (2020) Structural and functional abnormities of amygdala and prefrontal cortex in major depressive disorder with suicide attempts. Front Psychiatry 10:923. https://doi.org/10.3389/fpsyt.2019.00923

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gifuni AJ, Chakravarty MM, Lepage M, Ho TC, Geoffroy MC, Lacourse E, Gotlib IH, Turecki G, Renaud J, Jollant F (2021) Brain cortical and subcortical morphology in adolescents with depression and a history of suicide attempt. J Psychiatry Neurosci 46(3):E347-e357. https://doi.org/10.1503/jpn.200198

    Article  PubMed  PubMed Central  Google Scholar 

  24. Rentería ME, Schmaal L, Hibar DP, Couvy-Duchesne B, Strike LT, Mills NT, De Zubicaray GI, Mcmahon KL, Medland SE, Gillespie NA, Hatton SN, Lagopoulos J, Veltman DJ, Van Der Wee N, Van Erp TGM, Wittfeld K, Grabe HJ, Block A, Hegenscheid K, Völzke H, Veer IM, Walter H, Schnell K, Schramm E, Normann C, Schoepf D, Konrad C, Zurowski B, Godlewska BR, Cowen PJ, Penninx B, Jahanshad N, Thompson PM, Wright MJ, Martin NG, Christensen H, Hickie IB (2017) Subcortical brain structure and suicidal behaviour in major depressive disorder: a meta-analysis from the ENIGMA-MDD working group. Transl Psychiatry 7(5):1116. https://doi.org/10.1038/tp.2017.84

    Article  Google Scholar 

  25. Kang W, Shin JH, Han KM, Kim A, Kang Y, Kang J, Tae WS, Paik JW, Lee HW, Seong JK, Ham BJ (2020) Local shape volume alterations in subcortical structures of suicide attempters with major depressive disorder. Hum Brain Mapp 41(17):4925–4934. https://doi.org/10.1002/hbm.25168

    Article  PubMed  PubMed Central  Google Scholar 

  26. Zhang Q, Hong S, Cao J, Zhou Y, Xu X, Ai M, Kuang L (2021) Hippocampal subfield volumes in major depressive disorder adolescents with a history of suicide attempt. Biomed Res Int 2021:5524846. https://doi.org/10.1155/2021/5524846

    Article  PubMed  PubMed Central  Google Scholar 

  27. American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders: DSM-IV. American Psychiatric Association, Washington, DC

    Google Scholar 

  28. Posner K, Oquendo MA, Gould M, Stanley B, Davies M (2007) Columbia classification algorithm of suicide assessment (C-CASA): Classification of suicidal events in the FDA’s pediatric suicidal risk analysis of antidepressants. Am J Psychiatry 164(7):1035–1043. https://doi.org/10.1176/ajp.2007.164.7.1035

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13(2):261–276. https://doi.org/10.1093/schbul/13.2.261

    Article  CAS  PubMed  Google Scholar 

  30. He Y, Zhang M (2000) Yang xing yin xing zheng zhuang de zhong guo chang mo he yin zi fen xi [the Chinese norm and factor analysis of PANSS]. Chin J Clin Psychol 8(2):65–69. https://doi.org/10.3969/j.issn.1005-3611.2000.02.001

    Article  Google Scholar 

  31. Leucht S, Samara M, Heres S, Davis JM (2016) Dose equivalents for antipsychotic drugs: the ddd method. Schizophr Bull 42(Suppl 1):S90-94. https://doi.org/10.1093/schbul/sbv167

    Article  PubMed  PubMed Central  Google Scholar 

  32. Leucht S, Samara M, Heres S, Patel MX, Woods SW, Davis JM (2014) Dose equivalents for second-generation antipsychotics: the minimum effective dose method. Schizophr Bull 40(2):314–326. https://doi.org/10.1093/schbul/sbu001

    Article  PubMed  PubMed Central  Google Scholar 

  33. Fischl B, Van Der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14(1):11–22. https://doi.org/10.1093/cercor/bhg087

    Article  PubMed  Google Scholar 

  34. Fischl B (2012) Freesurfer. Neuroimage 62(2):774–781. https://doi.org/10.1016/j.neuroimage.2012.01.021

    Article  PubMed  Google Scholar 

  35. Iglesias JE, Augustinack JC, Nguyen K, Player CM, Player A, Wright M, Roy N, Frosch MP, Mckee AC, Wald LL, Fischl B, Van Leemput K (2015) A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: application to adaptive segmentation of in vivo MRI. Neuroimage 115:117–137. https://doi.org/10.1016/j.neuroimage.2015.04.042

    Article  PubMed  Google Scholar 

  36. Saygin ZM, Kliemann D, Iglesias JE, Van Der Kouwe AJW, Boyd E, Reuter M, Stevens A, Van Leemput K, Mckee A, Frosch MP, Fischl B, Augustinack JC (2017) High-resolution magnetic resonance imaging reveals nuclei of the human amygdala: manual segmentation to automatic atlas. Neuroimage 155:370–382. https://doi.org/10.1016/j.neuroimage.2017.04.046

    Article  CAS  PubMed  Google Scholar 

  37. Zugman A, Harrewijn A, Cardinale EM, Zwiebel H, Freitag GF, Werwath KE, Bas-Hoogendam JM, Groenewold NA, Aghajani M, Hilbert K, Cardoner N, Porta-Casteras D, Gosnell S, Salas R, Blair KS, Blair JR, Hammoud MZ, Milad M, Burkhouse K, Phan KL, Schroeder HK, Strawn JR, Beesdo-Baum K, Thomopoulos SI, Grabe HJ, Van Der Auwera S, Wittfeld K, Nielsen JA, Buckner R, Smoller JW, Mwangi B, Soares JC, Wu MJ, Zunta-Soares GB, Jackowski AP, Pan PM, Salum GA, Assaf M, Diefenbach GJ, Brambilla P, Maggioni E, Hofmann D, Straube T, Andreescu C, Berta R, Tamburo E, Price R, Manfro GG, Critchley HD, Makovac E, Mancini M, Meeten F, Ottaviani C, Agosta F, Canu E, Cividini C, Filippi M, Kostic M, Munjiza A, Filippi CA, Leibenluft E, Alberton BAV, Balderston NL, Ernst M, Grillon C, Mujica-Parodi LR, Van Nieuwenhuizen H, Fonzo GA, Paulus MP, Stein MB, Gur RE, Gur RC, Kaczkurkin AN, Larsen B, Satterthwaite TD, Harper J, Myers M, Perino MT, Yu Q, Sylvester CM, Veltman DJ, Lueken U, Van Der Wee NJA, Stein DJ, Jahanshad N, Thompson PM, Pine DS, Winkler AM (2022) Mega-analysis methods in ENIGMA: the experience of the generalized anxiety disorder working group. Hum Brain Mapp 43(1):255–277. https://doi.org/10.1002/hbm.25096

    Article  PubMed  Google Scholar 

  38. Radua J, Vieta E, Shinohara R, Kochunov P, Quide Y, Green MJ, Weickert CS, Weickert T, Bruggemann J, Kircher T, Nenadic I, Cairns MJ, Seal M, Schall U, Henskens F, Fullerton JM, Mowry B, Pantelis C, Lenroot R, Cropley V, Loughland C, Scott R, Wolf D, Satterthwaite TD, Tan Y, Sim K, Piras F, Spalletta G, Banaj N, Pomarol-Clotet E, Solanes A, Albajes-Eizagirre A, Canales-Rodriguez EJ, Sarro S, Di Giorgio A, Bertolino A, Stablein M, Oertel V, Knochel C, Borgwardt S, Du Plessis S, Yun JY, Kwon JS, Dannlowski U, Hahn T, Grotegerd D, Alloza C, Arango C, Janssen J, Diaz-Caneja C, Jiang W, Calhoun V, Ehrlich S, Yang K, Cascella NG, Takayanagi Y, Sawa A, Tomyshev A, Lebedeva I, Kaleda V, Kirschner M, Hoschl C, Tomecek D, Skoch A, Van Amelsvoort T, Bakker G, James A, Preda A, Weideman A, Stein DJ, Howells F, Uhlmann A, Temmingh H, Lopez-Jaramillo C, Diaz-Zuluaga A, Fortea L, Martinez-Heras E, Solana E, Llufriu S, Jahanshad N, Thompson P, Turner J, Van Erp T, Collaborators EC (2020) Increased power by harmonizing structural MRI site differences with the combat batch adjustment method in ENIGMA. Neuroimage 218:116956. https://doi.org/10.1016/j.neuroimage.2020.116956

    Article  PubMed  Google Scholar 

  39. Fortin JP, Cullen N, Sheline YI, Taylor WD, Aselcioglu I, Cook PA, Adams P, Cooper C, Fava M, Mcgrath PJ, Mcinnis M, Phillips ML, Trivedi MH, Weissman MM, Shinohara RT (2018) Harmonization of cortical thickness measurements across scanners and sites. Neuroimage 167:104–120. https://doi.org/10.1016/j.neuroimage.2017.11.024

    Article  PubMed  Google Scholar 

  40. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57(1):289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x

    Article  Google Scholar 

  41. Benjamini Y (2010) Discovering the false discovery rate. J R Stat Soc Series B Stat Methodol 72:405–416

    Article  Google Scholar 

  42. Larivière S, Paquola C, Park BY, Royer J, Wang Y, Benkarim O, Vos De Wael R, Valk SL, Thomopoulos SI, Kirschner M, Lewis LB, Evans AC, Sisodiya SM, Mcdonald CR, Thompson PM, Bernhardt BC (2021) The ENIGMA toolbox: Multiscale neural contextualization of multisite neuroimaging datasets. Nat Methods 18(7):698–700. https://doi.org/10.1038/s41592-021-01186-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Monkul ES, Hatch JP, Nicoletti MA, Spence S, Brambilla P, Lacerda AL, Sassi RB, Mallinger AG, Keshavan MS, Soares JC (2007) Fronto-limbic brain structures in suicidal and non-suicidal female patients with major depressive disorder. Mol Psychiatry 12(4):360–366. https://doi.org/10.1038/sj.mp.4001919

    Article  CAS  PubMed  Google Scholar 

  44. Schmaal L, Van Harmelen AL, Chatzi V, Lippard ETC, Toenders YJ, Averill LA, Mazure CM, Blumberg HP (2020) Imaging suicidal thoughts and behaviors: a comprehensive review of 2 decades of neuroimaging studies. Mol Psychiatry 25(2):408–427. https://doi.org/10.1038/s41380-019-0587-x

    Article  PubMed  Google Scholar 

  45. Johnston JAY, Wang F, Liu J, Blond BN, Wallace A, Liu J, Spencer L, Cox Lippard ET, Purves KL, Landeros-Weisenberger A, Hermes E, Pittman B, Zhang S, King R, Martin A, Oquendo MA, Blumberg HP (2017) Multimodal neuroimaging of frontolimbic structure and function associated with suicide attempts in adolescents and young adults with bipolar disorder. Am J Psychiatry 174(7):667–675. https://doi.org/10.1176/appi.ajp.2016.15050652

    Article  PubMed  PubMed Central  Google Scholar 

  46. Shrestha P, Shan Z, Mamcarz M, Ruiz KSA, Zerihoun AT, Juan CY, Herrero-Vidal PM, Pelletier J, Heintz N, Klann E (2020) Amygdala inhibitory neurons as loci for translation in emotional memories. Nature 586(7829):407–411. https://doi.org/10.1038/s41586-020-2793-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Gothard KM (2020) Multidimensional processing in the amygdala. Nat Rev Neurosci 21(10):565–575. https://doi.org/10.1038/s41583-020-0350-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Alarcón G, Sauder M, Teoh JY, Forbes EE, Quevedo K (2019) Amygdala functional connectivity during self-face processing in depressed adolescents with recent suicide attempt. J Am Acad Child Adolesc Psychiatry 58(2):221–231. https://doi.org/10.1016/j.jaac.2018.06.036

    Article  PubMed  Google Scholar 

  49. Pérez-Ortiz JM, García-Gutiérrez MS, Navarrete F, Giner S, Manzanares J (2013) Gene and protein alterations of FKBP5 and glucocorticoid receptor in the amygdala of suicide victims. Psychoneuroendocrinology 38(8):1251–1258. https://doi.org/10.1016/j.psyneuen.2012.11.008

    Article  CAS  PubMed  Google Scholar 

  50. Fardet L, Petersen I, Nazareth I (2012) Suicidal behavior and severe neuropsychiatric disorders following glucocorticoid therapy in primary care. Am J Psychiatry 169(5):491–497. https://doi.org/10.1176/appi.ajp.2011.11071009

    Article  PubMed  Google Scholar 

  51. Yin H, Galfalvy H, Pantazatos SP, Huang YY, Rosoklija GB, Dwork AJ, Burke A, Arango V, Oquendo MA, Mann JJ (2016) Glucocorticoid receptor-related genes: genotype and brain gene expression relationships to suicide and major depressive disorder. Depress Anxiety 33(6):531–540. https://doi.org/10.1002/da.22499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Herry C, Johansen JP (2014) Encoding of fear learning and memory in distributed neuronal circuits. Nat Neurosci 17(12):1644–1654. https://doi.org/10.1038/nn.3869

    Article  CAS  PubMed  Google Scholar 

  53. Janak PH, Tye KM (2015) From circuits to behaviour in the amygdala. Nature 517(7534):284–292. https://doi.org/10.1038/nature14188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Terburg D, Scheggia D, Triana Del Rio R, Klumpers F, Ciobanu AC, Morgan B, Montoya ER, Bos PA, Giobellina G, Van Den Burg EH, De Gelder B, Stein DJ, Stoop R, Van Honk J (2018) The basolateral amygdala is essential for rapid escape: a human and rodent study. Cell 175(3):723–735. https://doi.org/10.1016/j.cell.2018.09.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Jezzini A, Padoa-Schioppa C (2020) Neuronal activity in the primate amygdala during economic choice. J Neurosci 40(6):1286–1301. https://doi.org/10.1523/JNEUROSCI.0961-19.2019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Wassum KM, Izquierdo A (2015) The basolateral amygdala in reward learning and addiction. Neurosci Biobehav Rev 57:271–283. https://doi.org/10.1016/j.neubiorev.2015.08.017

    Article  PubMed  PubMed Central  Google Scholar 

  57. Zhang X, Kim J, Tonegawa S (2020) Amygdala reward neurons form and store fear extinction memory. Neuron 105(6):1077-1093.e1077. https://doi.org/10.1016/j.neuron.2019.12.025

    Article  CAS  PubMed  Google Scholar 

  58. Tsypes A, Szanto K, Bridge JA, Brown VM, Keilp JG, Dombrovski AY (2022) Delay discounting in suicidal behavior: myopic preference or inconsistent valuation? J Abnorm Psychol 131(1):34–44. https://doi.org/10.1037/abn0000717

    Article  Google Scholar 

  59. Ballard ED, Ionescu DF, Vande Voort JL, Slonena EE, Franco-Chaves JA, Zarate Jr CA, Grillon C (2014) Increased fear-potentiated startle in major depressive disorder patients with lifetime history of suicide attempt. J Affect Disord 162:34–38. https://doi.org/10.1016/j.jad.2014.03.027

    Article  PubMed  PubMed Central  Google Scholar 

  60. Selby EA, Anestis MD, Bender TW, Ribeiro JD, Nock MK, Rudd MD, Bryan CJ, Lim IC, Baker MT, Gutierrez PM, Joiner Jr TE (2010) Overcoming the fear of lethal injury: Evaluating suicidal behavior in the military through the lens of the interpersonal-psychological theory of suicide. Clin Psychol Rev 30(3):298–307. https://doi.org/10.1016/j.cpr.2009.12.004

    Article  PubMed  Google Scholar 

  61. Bhatnagar S, Vining C, Denski K (2004) Regulation of chronic stress-induced changes in hypothalamic-pituitary-adrenal activity by the basolateral amygdala. Ann N Y Acad Sci 1032:315–319. https://doi.org/10.1196/annals.1314.050

    Article  CAS  PubMed  Google Scholar 

  62. Werbart Törnblom A, Sorjonen K, Runeson B, Rydelius PA (2021) Life events and coping strategies among young people who died by suicide or sudden violent death. Front Psychiatry 12:670246. https://doi.org/10.3389/fpsyt.2021.670246

    Article  PubMed  PubMed Central  Google Scholar 

  63. Gosnell SN, Velasquez KM, Molfese DL, Molfese PJ, Madan A, Fowler JC, Christopher Frueh B, Baldwin PR, Salas R (2016) Prefrontal cortex, temporal cortex, and hippocampus volume are affected in suicidal psychiatric patients. Psychiatry Res Neuroimaging 256:50–56. https://doi.org/10.1016/j.pscychresns.2016.09.005

    Article  PubMed  PubMed Central  Google Scholar 

  64. Bellmund JLS, Gärdenfors P, Moser EI, Doeller CF (2018) Navigating cognition: spatial codes for human thinking. Science 362(6415):eaat6766. https://doi.org/10.1126/science.aat6766

    Article  CAS  PubMed  Google Scholar 

  65. Li J, Cao D, Dimakopoulos V, Shi W, Yu S, Fan L, Stieglitz L, Imbach L, Sarnthein J, Jiang T (2022) Anterior-posterior hippocampal dynamics support working memory processing. J Neurosci 42(3):443–453. https://doi.org/10.1523/jneurosci.1287-21.2021

    Article  CAS  PubMed  Google Scholar 

  66. Vikbladh OM, Meager MR, King J, Blackmon K, Devinsky O, Shohamy D, Burgess N, Daw ND (2019) Hippocampal contributions to model-based planning and spatial memory. Neuron 102(3):683–693. https://doi.org/10.1016/j.neuron.2019.02.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Nyberg N, Duvelle É, Barry C, Spiers HJ (2022) Spatial goal coding in the hippocampal formation. Neuron 110(3):394–422. https://doi.org/10.1016/j.neuron.2021.12.012

    Article  CAS  PubMed  Google Scholar 

  68. Shi J, Guo H, Liu S, Xue W, Fan F, Li H, Fan H, An H, Wang Z, Tan S, Yang F, Tan Y (2021) Subcortical brain volumes relate to neurocognition in first-episode schizophrenia, bipolar disorder, major depression disorder, and healthy controls. Front Psychiatry 12:747386. https://doi.org/10.3389/fpsyt.2021.747386

    Article  PubMed  Google Scholar 

  69. Fu S, Czajkowski N, Rund BR, Torgalsboen AK (2017) The relationship between level of cognitive impairments and functional outcome trajectories in first-episode schizophrenia. Schizophr Res 190:144–149. https://doi.org/10.1016/j.schres.2017.03.002

    Article  PubMed  Google Scholar 

  70. Zhang WC, Jia CX, Zhang JY, Wang LL, Liu XC (2015) Negative life events and attempted suicide in rural China. PLoS ONE 10(1):e0116634. https://doi.org/10.1371/journal.pone.0116634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Sweeney K (2008) Crisis decision theory: decisions in the face of negative events. Psychol Bull 134(1):61–76. https://doi.org/10.1037/0033-2909.134.1.61

    Article  PubMed  Google Scholar 

  72. Boldrini M, Galfalvy H, Dwork AJ, Rosoklija GB, Trencevska-Ivanovska I, Pavlovski G, Hen R, Arango V, Mann JJ (2019) Resilience is associated with larger dentate gyrus, while suicide decedents with major depressive disorder have fewer granule neurons. Biol Psychiatry 85(10):850–862. https://doi.org/10.1016/j.biopsych.2018.12.022

    Article  PubMed  PubMed Central  Google Scholar 

  73. Chen F, Bertelsen AB, Holm IE, Nyengaard JR, Rosenberg R, Dorph-Petersen K-A (2020) Hippocampal volume and cell number in depression, schizophrenia, and suicide subjects. Brain Res 1727:146546. https://doi.org/10.1016/j.brainres.2019.146546

    Article  CAS  PubMed  Google Scholar 

  74. Baglivo V, Cao B, Mwangi B, Bellani M, Perlini C, Lasalvia A, Dusi N, Bonetto C, Cristofalo D, Alessandrini F, Zoccatelli G, Ciceri E, Dario L, Enrico C, Francesca P, Mazzi F, Paolo S, Balestrieri M, Soares JC, Ruggeri M, Brambilla P (2018) Hippocampal subfield volumes in patients with first-episode psychosis. Schizophr Bull 44(3):552–559. https://doi.org/10.1093/schbul/sbx108

    Article  PubMed  Google Scholar 

  75. Roeske MJ, Konradi C, Heckers S, Lewis AS (2021) Hippocampal volume and hippocampal neuron density, number and size in schizophrenia: a systematic review and meta-analysis of postmortem studies. Mol Psychiatry 26(7):3524–3535. https://doi.org/10.1038/s41380-020-0853-y

    Article  PubMed  Google Scholar 

  76. Glavan D, Gheorman V, Gresita A, Hermann DM, Udristoiu I, Popa-Wagner A (2021) Identification of transcriptome alterations in the prefrontal cortex, hippocampus, amygdala and hippocampus of suicide victims. Sci Rep 11(1):18853. https://doi.org/10.1038/s41598-021-98210-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China [Y. Tan, 82171507, 81761128021; S. Chen, 82001415], the National Institutes of Health [L. E. Hong, R01MH112180]. Funders have no roles in data analysis, interpretation of the findings, or decision to publish the findings.

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Contributions

Conceptualization: Y. Tan, L. E. Hong, and Y. Yin; Methodology: S. Chen, F. Fan, P. Kochunov, and Y. Tong; Investigation: J. Tong, J. Huang, L. Wang, B. Tian, S. Tan, Z. Wang, T. Yu, Y. Li; Data curation: Y. Yin, T. Yu, and F. Fan; Formal Analysis: Y. Yin; Visualization: Y. Yin; Validation: Y. Tan; Interpretation of results: Y. Yin and Y. Tan; Writing – original draft: Y. Yin and Y. Tan; Writing – review and editing: J. Tong, J. Huang, L. Wang, B. Tian, S. Chen, S. Tan, Z. Wang, T. Yu, Y. Li, Y. Tong, P. Kochunov, and L. E. Hong; Approval of final version to be published and agreement to be accountable for the integrity and accuracy of all aspects of the work: All authors; Funding acquisition: Y. Tan, S. Chen, and L. E. Hong; Supervision: Y. Tan.

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Correspondence to Yunlong Tan.

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Conflict of interest

Dr. Hong has received or is planning to receive research funding or consulting fees from Mitsubishi, Your Energy Systems LLC, Neuralstem, Taisho, Heptares, Pfizer, Sound Pharma, Luye Pharma, IGC Pharma, Takeda, and Regeneron. None was involved in the design, analysis, or outcomes of the study. Other authors declared that the research was conducted without any relationships that could be interpreted as a potential conflict of interest or financial conflict.

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Yin, Y., Tong, J., Huang, J. et al. History of suicide attempt associated with amygdala and hippocampus changes among individuals with schizophrenia. Eur Arch Psychiatry Clin Neurosci 273, 921–930 (2023). https://doi.org/10.1007/s00406-023-01554-5

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