Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T21:23:44.402Z Has data issue: false hasContentIssue false
  • English
  • Français

The reductions in the subcallosal region cortical volume and surface area in major depressive disorder across the adult life span

Published online by Cambridge University Press:  01 March 2019

Dongtao Wei Open the ORCID record for Dongtao Wei [Opens in a new window] ,
Kangcheng Wang ,
Jie Meng ,
Kaixiang Zhuang ,
Qunlin Chen ,
Wenjing Yan ,
Peng Xie  and
Jiang Qiu
Dongtao Wei
Affiliation:
Key Laboratory of Cognition and Personality (Ministry of Education), Chongqing400715, China School of Psychology, Southwest University, Chongqing400715, China
Kangcheng Wang
Affiliation:
Key Laboratory of Cognition and Personality (Ministry of Education), Chongqing400715, China School of Psychology, Southwest University, Chongqing400715, China
Jie Meng
Affiliation:
Key Laboratory of Cognition and Personality (Ministry of Education), Chongqing400715, China School of Psychology, Southwest University, Chongqing400715, China
Kaixiang Zhuang
Affiliation:
Key Laboratory of Cognition and Personality (Ministry of Education), Chongqing400715, China School of Psychology, Southwest University, Chongqing400715, China
Qunlin Chen
Affiliation:
Key Laboratory of Cognition and Personality (Ministry of Education), Chongqing400715, China School of Psychology, Southwest University, Chongqing400715, China
Wenjing Yan
Affiliation:
Key Laboratory of Cognition and Personality (Ministry of Education), Chongqing400715, China School of Psychology, Southwest University, Chongqing400715, China
Peng Xie*
Affiliation:
Institute of Neuroscience, Chongqing Medical University, Chongqing, China Chongqing Key Laboratory of Neurobiology, Chongqing, China Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China
Jiang Qiu*
Affiliation:
Key Laboratory of Cognition and Personality (Ministry of Education), Chongqing400715, China School of Psychology, Southwest University, Chongqing400715, China
*
Author for correspondence: Peng Xie, E-mail: [email protected]; Jiang Qiu, E-mail: [email protected]
Author for correspondence: Peng Xie, E-mail: [email protected]; Jiang Qiu, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Imaging studies have shown that the subcallosal region (SCR) volume was decreased in patients with major depressive disorder (MDD). However, whether the volumetric reductions in the SCR are due to thinning of the cortex or a loss of surface area (SA) remains unclear. In addition, the relationship between cortical measurements of the SCR and age through the adult life span in MDD remains unclear.

Methods

We used a cross-sectional design from 114 individuals with MDD and 112 matched healthy control (HC) individuals across the adult life span (range: 18–74 years). The mean cortical volume (CV), SA and cortical thickness (CT) of the SCR were computed using cortical parcellation based on FreeSurfer software. Multivariate analyses of covariance models were performed to compare differences between the MDD and HC groups on cortical measurements of the SCR. Multiple linear regression models were used to test age-by-group interaction effects on these cortical measurements of the SCR.

Results

The MDD had significant reductions in the CV and SA of the left SCR compared with HC individuals after controlling of other variables. The left SCR CV and SA reductions compared with matched controls were observed only in early adulthood patients. We also found a significant age-related CT reduction in the SCR both in the MDD and HC participants.

Conclusions

The SCR volume reduction was mainly driven by SA in MDD. The different trajectories between the CT and SA of the SCR with age may provide valuable information to distinguish pathological processes and normal ageing in MDD.

Keywords

Cortical thicknessdepressionFreeSurfersubcallosal regionsurface area
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 3 , February 2020 , pp. 422 - 430
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Addis, DR, Pan, L, Vu, MA, Laiser, N and Schacter, DL (2009) Constructive episodic simulation of the future and the past: distinct subsystems of a core brain network mediate imagining and remembering. Neuropsychologia 47, 2222–2238.CrossRefGoogle ScholarPubMed
Amlien, IK, Fjell, AM, Tamnes, CK, Grydeland, H, Krogsrud, SK, Chaplin, TA, Rosa, MGP and Walhovd, KB (2016) Organizing principles of human cortical development--thickness and area from 4 to 30 years: insights from comparative primate neuroanatomy. Cerebral Cortex 26, 257–267.CrossRefGoogle ScholarPubMed
Anderson, BJ (2011) Plasticity of gray matter volume: the cellular and synaptic plasticity that underlies volumetric change. Developmental Psychobiology 53, 456–465.CrossRefGoogle ScholarPubMed
Bijanki, KR, Hodis, B, Brumm, MC, Harlynn, EL and Mccormick, LM (2014) Hippocampal and left subcallosal anterior cingulate atrophy in psychotic depression. PLoS One 9, e110770.CrossRefGoogle ScholarPubMed
Botteron, KN, Raichle, ME, Drevets, WC, Heath, AC and Todd, RD (2002) Volumetric reduction in left subgenual prefrontal cortex in early onset depression. Biological Psychiatry 51, 342–344.CrossRefGoogle ScholarPubMed
Cheng, W, Rolls, ET, Qiu, J, Liu, W, Tang, Y, Huang, CC, Wang, X, Zhang, J, Lin, W, Zheng, L, Pu, J, Tsai, SJ, Yang, AC, Lin, CP, Wang, F, Xie, P and Feng, J (2016) Medial reward and lateral non-reward orbitofrontal cortex circuits change in opposite directions in depression. Brain 139, 3296–3309.CrossRefGoogle ScholarPubMed
Chenn, A and Walsh, CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365–369.CrossRefGoogle ScholarPubMed
Destrieux, C, Fischl, B, Dale, A and Halgren, E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53, 1–15.CrossRefGoogle ScholarPubMed
Dickerson, BC, Feczko, E, Augustinack, JC, Pacheco, J, Morris, JC, Fischl, B and Buckner, RL (2009) Differential effects of aging and Alzheimer's disease on medial temporal lobe cortical thickness and surface area. Neurobiology of Aging 30, 420–431.CrossRefGoogle ScholarPubMed
Drevets, WC, Ongur, D and Price, JL (1998) Neuroimaging abnormalities in the subgenual prefrontal cortex: implications for the pathophysiology of familial mood disorders. Molecular Psychiatry 3, 220–226.CrossRefGoogle ScholarPubMed
Du, MY, Wu, QZ, Yue, Q, Li, J, Liao, Y, Kuang, WH, Huang, XQ, Chan, RC, Mechelli, A and Gong, QY (2012) Voxelwise meta-analysis of gray matter reduction in major depressive disorder. Progress in Neuropsychopharmacology Biological Psychiatry 36, 11–16.CrossRefGoogle ScholarPubMed
Du, M, Liu, J, Chen, Z, Huang, X, Li, J, Kuang, W, Yang, Y, Zhang, W, Zhou, D, Bi, F, Kendrick, KM and Gong, Q (2014) Brain grey matter volume alterations in late-life depression. Journal of Psychiatry & Neuroscience 39, 397–406.CrossRefGoogle ScholarPubMed
Ducharme, S, Albaugh, MD, Hudziak, JJ, Botteron, KN, Nguyen, TV, Truong, C, Evans, AC and Karama, S and Brain Development Cooperative G (2014) Anxious/depressed symptoms are linked to right ventromedial prefrontal cortical thickness maturation in healthy children and young adults. Cerebral Cortex 24, 2941–2950.CrossRefGoogle ScholarPubMed
Dunlop, BW, Rajendra, JK, Craighead, WE, Kelley, ME, Mcgrath, CL, Choi, KS, Kinkead, B, Nemeroff, CB and Mayberg, HS (2017) Functional connectivity of the subcallosal cingulate cortex and differential outcomes to treatment with cognitive-behavioral therapy or antidepressant medication for major depressive disorder. American Journal of Psychiatry 174, 533–545.CrossRefGoogle ScholarPubMed
Ecker, C, Ginestet, C, Feng, Y, Johnston, P, Lombardo, MV, Lai, MC, Suckling, J, Palaniyappan, L, Daly, E, Murphy, CM, Williams, SC, Bullmore, ET, Baron-Cohen, S, Brammer, M, Murphy, DG and Consortium, MA (2013) Brain surface anatomy in adults with autism: the relationship between surface area, cortical thickness, and autistic symptoms. JAMA Psychiatry 70, 59–70.CrossRefGoogle ScholarPubMed
Fjell, AM, Walhovd, KB, Westlye, LT, Østby, Y, Tamnes, CK, Jernigan, TL, Gamst, A and Dale, AM (2010) When does brain aging accelerate? Dangers of quadratic fits in cross-sectional studies. Neuroimage 50, 1376–1383.CrossRefGoogle ScholarPubMed
Gianaros, PJ, Van Der Veen, FM and Jennings, JR (2004) Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: implication for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology 41, 521–530.CrossRefGoogle Scholar
Hamani, C, Mayberg, H, Snyder, B, Giacobbe, P, Kennedy, S and Lozano, AM (2009) Deep brain stimulation of the subcallosal cingulate gyrus for depression: anatomical location of active contacts in clinical responders and a suggested guideline for targeting. Journal of Neurosurgery 111, 1209–1215.CrossRefGoogle Scholar
Hamani, C, Mayberg, H, Stone, S, Laxton, A, Haber, S and Lozano, AM (2011) The subcallosal cingulate gyrus in the context of major depression. Biological Psychiatry 69, 301–308.CrossRefGoogle ScholarPubMed
Hastie, T and Tibshirani, R (1995) Generalized additive models for medical research. Statistical Methods in Medical Research 4, 187–196.CrossRefGoogle ScholarPubMed
Herringa, RJ, Birn, RM, Ruttle, PL, Burghy, CA, Stodola, DE, Davidson, RJ and Essex, MJ (2013) Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proceeding of National Academy of Science of the United States of America 110, 19119–19124.CrossRefGoogle ScholarPubMed
Hirayasu, Y, Shenton, ME, Salisbury, DF, Kwon, JS, Wible, CG, Fischer, IA, Yurgelun-Todd, D, Zarate, C, Kikinis, R and Jolesz, FA (1999) Subgenual cingulate cortex volume in first-episode psychosis. American Journal of Psychiatry 156, 1091–1093.Google ScholarPubMed
Hogstrom, LJ, Westlye, LT, Walhovd, KB and Fjell, AM (2013) The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. Cerebral Cortex 23, 2521–2530.CrossRefGoogle ScholarPubMed
Holtzheimer, PE, Kelley, ME, Gross, RE, Filkowski, MM, Garlow, SJ, Barrocas, A, Wint, D, Craighead, MC, Kozarsky, J, Chismar, R, Moreines, JL, Mewes, K, Posse, PR, Gutman, DA and Mayberg, HS (2012) Subcallosal cingulate deep brain stimulation for treatment-resistant unipolar and bipolar depression. Archives of General Psychiatry 69, 150–158.CrossRefGoogle ScholarPubMed
Jaworska, N, Yucel, K, Courtright, A, Macmaster, FP, Sembo, M and Macqueen, G (2016) Subgenual anterior cingulate cortex and hippocampal volumes in depressed youth: the role of comorbidity and age. Journal of Affective Disorders 190, 726–732.CrossRefGoogle Scholar
Keding, TJ and Herringa, RJ (2015) Abnormal structure of fear circuitry in pediatric post-traumatic stress disorder. Neuropsychopharmacology 40, 537–545.CrossRefGoogle ScholarPubMed
Kempton, MJ, Salvador, Z, Munafo, MR, Geddes, JR, Simmons, A, Frangou, S and Williams, SCR (2011) Structural neuroimaging studies in major depressive disorder meta-analysis and comparison with bipolar disorder. Archives of General Psychiatry 68, 675–690.CrossRefGoogle ScholarPubMed
Koo, M-S, Levitt, JJ, Salisbury, DF, Nakamura, M, Shenton, ME and Mccarley, RW (2008) A cross-sectional and longitudinal magnetic resonance imaging study of cingulate gyrus gray matter volume abnormalities in first-episode schizophrenia and first-episode affective psychosis. Archives of General Psychiatry 65, 746–760.CrossRefGoogle ScholarPubMed
Lemaitre, H, Goldman, AL, Sambataro, F, Verchinski, BA, Meyer-Lindenberg, A, Weinberger, DR and Mattay, VS (2012) Normal age-related brain morphometric changes: nonuniformity across cortical thickness, surface area and gray matter volume? Neurobiology of Aging 33, 617.e1–617.e9.CrossRefGoogle ScholarPubMed
Levinson, DJ (1986) A conception of adult development. American Psychologist 41, 3–13.CrossRefGoogle Scholar
Lozano, AM, Mayberg, HS, Giacobbe, P, Hamani, C, Craddock, RC and Kennedy, SH (2008) Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biological Psychiatry 64, 461–467.CrossRefGoogle ScholarPubMed
Mandell, D, Siegle, GJ, Shutt, L, Feldmiller, J and Thase, ME (2014) Neural substrates of trait ruminations in depression. Journal of Abnormal Psychology 123, 35–48.CrossRefGoogle ScholarPubMed
Murre, JM and Sturdy, DP (1995) The connectivity of the brain: multi-level quantitative analysis. Biological Cybernetics 73, 529–545.CrossRefGoogle ScholarPubMed
Myers-Schulz, B and Koenigs, M (2012) Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders. Molecular Psychiatry 17, 132–141.CrossRefGoogle ScholarPubMed
Panizzon, MS, Fennema-Notestine, C, Eyler, LT, Jernigan, TL, Prom-Wormley, E, Neale, M, Jacobson, K, Lyons, MJ, Grant, MD, Franz, CE, Xian, H, Tsuang, M, Fischl, B, Seidman, L, Dale, A and Kremen, WS (2009) Distinct genetic influences on cortical surface area and cortical thickness. Cerebral Cortex 19, 2728–2735.CrossRefGoogle ScholarPubMed
Rakic, P (1988) Specification of cerebral cortical areas. Science 241, 170–176.CrossRefGoogle ScholarPubMed
Rimol, LM, Nesvag, R, Hagler, DJ JR., Bergmann, O, Fennema-Notestine, C, Hartberg, CB, Haukvik, UK, Lange, E, Pung, CJ, Server, A, Melle, I, Andreassen, OA, Agartz, I and Dale, AM (2012) Cortical volume, surface area, and thickness in schizophrenia and bipolar disorder. Biological Psychiatry 71, 552–560.CrossRefGoogle ScholarPubMed
Riva-Posse, P, Choi, KS, Holtzheimer, PE, Crowell, AL, Garlow, SJ, Rajendra, JK, Mcintyre, CC, Gross, RE and Mayberg, HS (2018) A connectomic approach for subcallosal cingulate deep brain stimulation surgery: prospective targeting in treatment-resistant depression. Molecular Psychiatry 23, 843–849.CrossRefGoogle ScholarPubMed
Rodriguez-Cano, E, Sarro, S, Monte, GC, Maristany, T, Salvador, R, Mckenna, PJ and Pomarol-Clotet, E (2014) Evidence for structural and functional abnormality in the subgenual anterior cingulate cortex in major depressive disorder. Psychological Medicine 44, 3263–3273.CrossRefGoogle ScholarPubMed
Ruppin, E, Schwartz, EL and Yeshurun, Y (1993) Examining the volume efficiency of the cortical architecture in a multi-processor network model. Biological Cybernetics 70, 89–94.CrossRefGoogle Scholar
Schmaal, L, Hibar, DP, Samann, PG, Hall, GB, Baune, BT, Jahanshad, N, Cheung, JW, Van Erp, TGM, Bos, D, Ikram, MA, Vernooij, MW, Niessen, WJ, Tiemeier, H, Hofman, A, Wittfeld, K, Grabe, HJ, Janowitz, D, Bulow, R, Selonke, M, Volzke, H, Grotegerd, D, Dannlowski, U, Arolt, V, Opel, N, Heindel, W, Kugel, H, Hoehn, D, Czisch, M, Couvy-Duchesne, B, Renteria, ME, Strike, LT, Wright, MJ, Mills, NT, De Zubicaray, GI, Mcmahon, KL, Medland, SE, Martin, NG, Gillespie, NA, Goya-Maldonado, R, Gruber, O, Kramer, B, Hatton, SN, Lagopoulos, J, Hickie, IB, Frodl, T, Carballedo, A, Frey, EM, Van Velzen, LS, Penninx, B, Van Tol, MJ, Van Der Wee, NJ, Davey, CG, Harrison, BJ, Mwangi, B, Cao, B, Soares, JC, Veer, IM, Walter, H, Schoepf, D, Zurowski, B, Konrad, C, Schramm, E, Normann, C, Schnell, K, Sacchet, MD, Gotlib, IH, Macqueen, GM, Godlewska, BR, Nickson, T, Mcintosh, AM, Papmeyer, M, Whalley, HC, Hall, J, Sussmann, JE, Li, M, Walter, M, Aftanas, L, Brack, I, Bokhan, NA, Thompson, PM and Veltman, DJ (2017) Cortical abnormalities in adults and adolescents with major depression based on brain scans from 20 cohorts worldwide in the ENIGMA Major Depressive Disorder Working Group. Molecular Psychiatry 22, 900–909.CrossRefGoogle ScholarPubMed
Somerville, LH (2016) Searching for signatures of brain maturity: what are we searching for? Neuron 92, 1164–1167.CrossRefGoogle ScholarPubMed
Storsve, AB, Fjell, AM, Tamnes, CK, Westlye, LT, Overbye, K, Aasland, HW and Walhovd, KB (2014) Differential longitudinal changes in cortical thickness, surface area and volume across the adult life span: regions of accelerating and decelerating change. Journal of Neuroscience 34, 8488–8498.CrossRefGoogle ScholarPubMed
Tamnes, CK, Herting, MM, Goddings, AL, Meuwese, R, Blakemore, SJ, Dahl, RE, Guroglu, B, Raznahan, A, Sowell, ER, Crone, EA and Mills, KL (2017) Development of the cerebral Cortex across adolescence: a multisample study of inter-related longitudinal changes in cortical volume, surface area, and thickness. Journal of Neuroscience 37, 3402–3412.CrossRefGoogle ScholarPubMed
Treadway, MT, Waskom, ML, Dillon, DG, Holmes, AJ, Park, MTM, Chakravarty, MM, Dutra, SJ, Polli, FE, Iosifescu, DV, Fava, M, Gabrieli, JDE and Pizzagalli, DA (2015) Illness progression, recent stress, and morphometry of hippocampal subfields and medial prefrontal cortex in major depression. Biological Psychiatry 77, 285–294.CrossRefGoogle ScholarPubMed
Valentin, VV, Dickinson, A and O'doherty, JP (2007) Determining the neural substrates of goal-directed learning in the human brain. Journal of Neuroscience 27, 4019–4026.CrossRefGoogle ScholarPubMed
van der Meer, L, Costafreda, S, Aleman, A and David, AS (2010) Self-reflection and the brain: a theoretical review and meta-analysis of neuroimaging studies with implications for schizophrenia. Neuroscience and Biobehavioral Reviews 34, 935–946.CrossRefGoogle Scholar
Wager, TD, Davidson, ML, Hughes, BL, Lindquist, MA and Ochsner, KN (2008) Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59, 1037–1050.CrossRefGoogle ScholarPubMed
Wierenga, LM, Langen, M, Oranje, B and Durston, S (2014) Unique developmental trajectories of cortical thickness and surface area. Neuroimage 87, 120–126.CrossRefGoogle ScholarPubMed
Wood, SN (2004) Stable and efficient multiple smoothing parameter estimation for generalized additive models. Journal of the American Statistical Association 99, 673–686.CrossRefGoogle Scholar
Wood, SN (2006) Generalized Additive Models: An Introduction with R. Boca Raton, FL: Chapman and Hall/CRC.CrossRefGoogle Scholar