Hostname: page-component-7c8c6479df-fqc5m Total loading time: 0 Render date: 2024-03-29T03:55:15.969Z Has data issue: false hasContentIssue false

Effects of early life stress on depression, cognitive performance and brain morphology

Published online by Cambridge University Press:  29 September 2016

A. Saleh
Affiliation:
The Center for Cognitive Medicine, Department of Psychiatry, Vanderbilt University Medical Center, Nashville, TN 37212, USA
G. G. Potter
Affiliation:
Department of Psychiatry and Behavioral Sciences, Duke University Medical Center, Durham, NC 27710, USA
D. R. McQuoid
Affiliation:
Department of Psychiatry and Behavioral Sciences, Duke University Medical Center, Durham, NC 27710, USA
B. Boyd
Affiliation:
The Center for Cognitive Medicine, Department of Psychiatry, Vanderbilt University Medical Center, Nashville, TN 37212, USA
R. Turner
Affiliation:
The Center for Cognitive Medicine, Department of Psychiatry, Vanderbilt University Medical Center, Nashville, TN 37212, USA
J. R. MacFall
Affiliation:
Department of Radiology, Duke University Medical Center, Durham, NC 27710, USA
W. D. Taylor*
Affiliation:
The Center for Cognitive Medicine, Department of Psychiatry, Vanderbilt University Medical Center, Nashville, TN 37212, USA The Geriatric Research, Education, and Clinical Center (GRECC), Department of Veterans Affairs Medical Center, Tennessee Valley Healthcare System, Nashville, TN 37212, USA
*
*Address for correspondence: W. D. Taylor, M.D., M.H.Sc., Vanderbilt University, 1601 23rd Avenue South, Nashville, TN 37212, USA. (Email: warren.d.taylor@vanderbilt.edu)

Abstract

Background

Childhood early life stress (ELS) increases risk of adulthood major depressive disorder (MDD) and is associated with altered brain structure and function. It is unclear whether specific ELSs affect depression risk, cognitive function and brain structure.

Method

This cross-sectional study included 64 antidepressant-free depressed and 65 never-depressed individuals. Both groups reported a range of ELSs on the Early Life Stress Questionnaire, completed neuropsychological testing and 3T magnetic resonance imaging (MRI). Neuropsychological testing assessed domains of episodic memory, working memory, processing speed and executive function. MRI measures included cortical thickness and regional gray matter volumes, with a priori focus on the cingulate cortex, orbitofrontal cortex (OFC), amygdala, caudate and hippocampus.

Results

Of 19 ELSs, only emotional abuse, sexual abuse and severe family conflict independently predicted adulthood MDD diagnosis. The effect of total ELS score differed between groups. Greater ELS exposure was associated with slower processing speed and smaller OFC volumes in depressed subjects, but faster speed and larger volumes in non-depressed subjects. In contrast, exposure to ELSs predictive of depression had similar effects in both diagnostic groups. Individuals reporting predictive ELSs exhibited poorer processing speed and working memory performance, smaller volumes of the lateral OFC and caudate, and decreased cortical thickness in multiple areas including the insula bilaterally. Predictive ELS exposure was also associated with smaller left hippocampal volume in depressed subjects.

Conclusions

Findings suggest an association between childhood trauma exposure and adulthood cognitive function and brain structure. These relationships appear to differ between individuals who do and do not develop depression.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

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

Baker, LM, Williams, LM, Korgaonkar, MS, Cohen, RA, Heaps, JM, Paul, RH (2013). Impact of early vs. late childhood early life stress on brain morphometrics. Brain Imaging and Behavior 7, 196203.Google Scholar
Brewin, CR (2014). Episodic memory, perceptual memory, and their interaction: foundations for a theory of posttraumatic stress disorder. Psychological Bulletin 140, 6997.Google Scholar
Brown, WG, Harris, TO (1978). Social Origins of Depression: a Study of Psychiatric Disorder in Women. The Free Press: New York.Google Scholar
Cohen, RA, Grieve, S, Hoth, KF, Paul, RH, Sweet, L, Tate, D, Gunstad, J, Stroud, L, McCaffery, J, Hitsman, B, Niaura, R, Clark, CR, McFarlane, A, Bryant, R, Gordon, E, Williams, LM (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry 59, 975982.Google Scholar
Cole, J, Costafreda, SG, McGuffin, P, Fu, CH (2011). Hippocampal atrophy in first episode depression: a meta-analysis of magnetic resonance imaging studies. Journal of Affective Disorders 134, 483487.CrossRefGoogle ScholarPubMed
Dale, AM, Fischl, B, Sereno, MI (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179194.Google Scholar
De Brito, SA, Viding, E, Sebastian, CL, Kelly, PA, Mechelli, A, Maris, H, McCrory, EJ (2013). Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children. Journal of Child Psychology and Psychiatry 54, 105112.CrossRefGoogle Scholar
Desikan, RS, Ségonne, F, Fischl, B, Quinn, BT, Dickerson, BC, Blacker, D, Buckner, RL, Dale, AM, Maguire, RP, Hyman, BT, Albert, MS, Killiany, RJ (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31, 968980.Google Scholar
Evans, GW, Schamberg, MA (2009). Childhood poverty, chronic stress, and adult working memory. Proceedings of the National Academy of Sciences USA 106, 65456549.CrossRefGoogle ScholarPubMed
Feeney, J, Kamiya, Y, Robertson, IH, Kenny, RA (2013). Cognitive function is preserved in older adults with a reported history of childhood sexual abuse. Journal of Traumatic Stress 26, 735743.CrossRefGoogle ScholarPubMed
First, MB, Gibbon, M, Spitzer, RL, Williams, JB, Benjamin, LS (1997). Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II) . American Psychiatric Press, Inc.: Washington, DC.Google Scholar
Fischl, B, Dale, AM (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences USA 97, 1105011055.Google Scholar
Fischl, B, Salat, DH, Busa, E, Albert, M, Dieterich, M, Haselgrove, C, van der Kouwe, A, Killiany, R, Kennedy, D, Klaveness, S, Montillo, A, Makris, N, Rosen, B, Dale, AM (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341355.Google Scholar
Fischl, B, Salat, DH, van der Kouwe, AJ, Makris, N, Segonne, F, Quinn, BT, Dale, AM (2004 a). Sequence-independent segmentation of magnetic resonance images. NeuroImage 23 (Suppl. 1), S69S84.Google Scholar
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 b). Automatically parcellating the human cerebral cortex. Cerebral Cortex 14, 1122.CrossRefGoogle ScholarPubMed
Frodl, T, Reinhold, E, Koutsouleris, N, Reiser, M, Meisenzahl, EM (2010). Interaction of childhood stress with hippocampus and prefrontal cortex volume reduction in major depression. Journal of Psychiatric Research 44, 799807.CrossRefGoogle ScholarPubMed
Gershon, A, Sudheimer, K, Tirouvanziam, R, Williams, LM, O'Hara, R (2013). The long-term impact of early adversity on late-life psychiatric disorders. Current Psychiatry Reports 15, 352.Google Scholar
Harkness, KL, Bruce, AE, Lumley, MN (2006). The role of childhood abuse and neglect in the sensitization to stressful life events in adolescent depression. Journal of Abnormal Psychology 115, 730741.Google Scholar
Herpfer, I, Hezel, H, Reichardt, W, Clark, K, Geiger, J, Gross, CM, Heyer, A, Neagu, V, Bhatia, H, Atas, HC, Fiebich, BL, Bischofberger, J, Haas, CA, Lieb, K, Normann, C (2012). Early life stress differentially modulates distinct forms of brain plasticity in young and adult mice. PLOS ONE 7, e46004.CrossRefGoogle ScholarPubMed
Jakubczyk, A, Klimkiewicz, A, Krasowska, A, Kopera, M, Slawinska-Ceran, A, Brower, KJ, Wojnar, M (2014). History of sexual abuse and suicide attempts in alcohol-dependent patients. Child Abuse and Neglect 38, 15601568.Google Scholar
Kaplow, JB, Widom, CS (2007). Age of onset of child maltreatment predicts long-term mental health outcomes. Journal of Abnormal Psychology 116, 176187.Google Scholar
Kessler, RC, Magee, WJ (1994). Childhood family violence and adult recurrent depression. Journal of Health and Social Behavior 35, 1327.Google Scholar
Krishnadas, R, Palaniyappan, L, Lang, J, McLean, J, Cavanagh, J (2014). Psychoticism and salience network morphology. Personality and Individual Differences 57, 3742.CrossRefGoogle Scholar
Luebbe, AM, Bell, DJ (2014). Positive and negative family emotional climate differentially predict youth anxiety and depression via distinct affective pathways. Journal of Abnormal Child Psychology 42, 897911.CrossRefGoogle ScholarPubMed
Lyons, DM, Parker, KJ, Katz, M, Schatzberg, AF (2009). Developmental cascades linking stress inoculation, arousal regulation, and resilience. Frontiers in Behavioral Neuroscience 3, 32.Google Scholar
MacQueen, G, Frodl, T (2011). The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research? Molecular Psychiatry 16, 252264.Google Scholar
Martins, CM, Von Werne Baes, C, Tofoli, SM, Juruena, MF (2014). Emotional abuse in childhood is a differential factor for the development of depression in adults. Journal of Nervous and Mental Disease 202, 774782.Google Scholar
McEwen, BS (2003). Early life influences on life-long patterns of behavior and health. Mental Retardation and Developmental Disabilities Research Reviews 9, 149154.Google Scholar
Miller, MD, Paradis, CF, Houck, PR, Mazumdar, S, Stack, JA, Rifai, AH, Mulsant, B, Reynolds, CF (1992). Rating chronic medical illness burden in geropsychiatric practice and research: application of the Cumulative Illness Rating Scale. Psychiatry Research 41, 237248.CrossRefGoogle ScholarPubMed
Montgomery, SA, Åsberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382389.Google Scholar
Navalta, CP, Polcari, A, Webster, DM, Boghossian, A, Teicher, MH (2006). Effects of childhood sexual abuse on neuropsychological and cognitive function in college women. Journal of Neuropsychiatry and Clinical Neurosciences 18, 4553.CrossRefGoogle ScholarPubMed
Parker, KJ, Buckmaster, CL, Justus, KR, Schatzberg, AF, Lyons, DM (2005). Mild early life stress enhances prefrontal-dependent response inhibition in monkeys. Biological Psychiatry 57, 848855.CrossRefGoogle ScholarPubMed
Parks, ED, Balon, R (1995). Autobiographical memory for childhood events: patterns of recall in psychiatric patients with a history of alleged trauma. Psychiatry 58, 199208.CrossRefGoogle ScholarPubMed
Polak, AR, Witteveen, AB, Reitsma, JB, Olff, M (2012). The role of executive function in posttraumatic stress disorder: a systematic review. Journal of Affective Disorders 141, 1121.CrossRefGoogle ScholarPubMed
Sanders, B, Becker-Lausen, E (1995). The measurement of psychological maltreatment: early data on the Child Abuse and Trauma Scale. Child Abuse and Neglect 19, 315323.Google Scholar
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, RW, Dunbar, GC (1998). The Mini-International Neuropsychiatric Inventory (M.I.N.I.): the development and validation of a structured diagnostic interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59 (Suppl. 20), 2233.Google Scholar
Sheline, YI, Pieper, CF, Barch, DM, Welsh-Bohmer, K, McKinstry, RC, MacFall, JR, D'Angelo, G, Garcia, KS, Gersing, K, Wilkins, C, Taylor, W, Steffens, DC, Krishnan, RR, Doraiswamy, PM (2010). Support for the vascular depression hypothesis in late-life depression: results of a 2-site, prospective, antidepressant treatment trial. Archives of General Psychiatry 67, 277285.Google Scholar
Sheline, YI, Sanghavi, M, Mintun, MA, Gado, MH (1999). Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. Journal of Neuroscience 19, 50345043.Google Scholar
Sheline, YI, Wang, PW, Gado, MH, Csernansky, JG, Vannier, MW (1996). Hippocampal atrophy in recurrent major depression. Proceedings of the National Academy of Sciences USA 93, 39083913.Google Scholar
Snyder, HR (2013). Major depressive disorder is associated with broad impairments on neuropsychological measures of executive function: a meta-analysis and review. Psychological Bulletin 139, 81132.Google Scholar
Teicher, MH, Anderson, CM, Polcari, A (2012). Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proceedings of the National Academy of Sciences USA 109, E563E572.Google Scholar
Tottenham, N, Hare, TA, Quinn, BT, McCarry, TW, Nurse, M, Gilhooly, T, Millner, A, Galvan, A, Davidson, MC, Eigsti, IM, Thomas, KM, Freed, PJ, Booma, ES, Gunnar, MR, Altemus, M, Aronson, J, Casey, BJ (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science 13, 4661.CrossRefGoogle ScholarPubMed
Udo, D, Anja, S, Victoria, B, Peter, Z, Thomas, L, Dominik, G, Katharina, D, Christa, H, Patricia, O, Jochen, B, Christian, L, Christian, P, Carsten, K, Volker, A, Walter, H, Thomas, S, Harald, K (2012). Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry 71, 286293.Google Scholar
van Harmelen, AL, van Tol, MJ, van der Wee, NJ, Veltman, DJ, Aleman, A, Spinhoven, P, van Buchem, MA, Zitman, FG, Penninx, BW, Elzinga, BM (2010). Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment. Biological Psychiatry 68, 832838.CrossRefGoogle ScholarPubMed
Vietze, P, Falsey, S, Sandler, H, O'Connor, S, Altemier, WA (1980). Transactional approach to prediction of child maltreatment. Infant Mental Health Journal 1, 248261.Google Scholar
Wise, LA, Zierler, S, Krieger, N, Harlow, BL (2001). Adult onset of major depressive disorder in relation to early life violent victimisation: a case–control study. Lancet 358, 881887.Google Scholar
Wu, G, Feder, A, Cohen, H, Kim, JJ, Calderon, S, Charney, DS, Mathe, AA (2013). Understanding resilience. Frontiers in Behavioral Neuroscience 7, 10.Google Scholar
Supplementary material: File

Saleh supplementary material

Tables S1-S3

Download Saleh supplementary material(File)
File 74.8 KB