Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-07T08:27:53.017Z Has data issue: false hasContentIssue false
  • English
  • Français

Neuroticism, depressive symptoms and white-matter integrity in the Lothian Birth Cohort 1936

Published online by Cambridge University Press:  11 July 2012

A. M. McIntosh ,
M. E. Bastin ,
M. Luciano ,
S. Muñoz Maniega ,
M. del C.Valdés Hernández ,
N. A. Royle ,
J. Hall ,
C. Murray ,
S. M. Lawrie  and
J. M. Starr
...Show all authors
A. M. McIntosh*
Affiliation:
Division of Psychiatry, University of Edinburgh, UK Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK SINAPSE (Scottish Imaging Network, A Platform for Scientific Excellence) collaboration
M. E. Bastin
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK SINAPSE (Scottish Imaging Network, A Platform for Scientific Excellence) collaboration Division of Health Sciences (Medical Physics), University of Edinburgh, UK Brain Research Imaging Centre, Division of Clinical Neurosciences, University of Edinburgh, UK
M. Luciano
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK Department of Psychology, University of Edinburgh, UK
S. Muñoz Maniega
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK SINAPSE (Scottish Imaging Network, A Platform for Scientific Excellence) collaboration Brain Research Imaging Centre, Division of Clinical Neurosciences, University of Edinburgh, UK
M. del C.Valdés Hernández
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK SINAPSE (Scottish Imaging Network, A Platform for Scientific Excellence) collaboration Brain Research Imaging Centre, Division of Clinical Neurosciences, University of Edinburgh, UK
N. A. Royle
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK SINAPSE (Scottish Imaging Network, A Platform for Scientific Excellence) collaboration Brain Research Imaging Centre, Division of Clinical Neurosciences, University of Edinburgh, UK
J. Hall
Affiliation:
Division of Psychiatry, University of Edinburgh, UK SINAPSE (Scottish Imaging Network, A Platform for Scientific Excellence) collaboration
C. Murray
Affiliation:
Department of Psychology, University of Edinburgh, UK
S. M. Lawrie
Affiliation:
Division of Psychiatry, University of Edinburgh, UK SINAPSE (Scottish Imaging Network, A Platform for Scientific Excellence) collaboration
J. M. Starr
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK Geriatric Medicine Unit, University of Edinburgh, UK
J. M. Wardlaw
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK SINAPSE (Scottish Imaging Network, A Platform for Scientific Excellence) collaboration Brain Research Imaging Centre, Division of Clinical Neurosciences, University of Edinburgh, UK
I. J. Deary
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK Department of Psychology, University of Edinburgh, UK
*
*Address for correspondence: Professor A. M. McIntosh, Division of Psychiatry, University of Edinburgh, Kennedy Tower, Royal Edinburgh Hospital, Edinburgh EH10 5HF, UK. (Email: andrew.mcintosh@ed.ac.uk)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Clinical depression is associated with reductions in white-matter integrity in several long tracts of the brain. The extent to which these findings are localized or related to depressive symptoms or personality traits linked to disease risk remains unclear.

Method

Members of the Lothian Birth Cohort 1936 (LBC936) were assessed in two waves at mean ages of 70 and 73 years. At wave 1, they underwent assessments of depressive symptoms and the personality traits of neuroticism and extraversion. Brain diffusion magnetic resonance imaging (MRI) data were obtained at the second wave and mood assessments were repeated. We tested whether depressive symptoms were related to reduced white-matter tract fractional anisotropy (FA), a measure of integrity, and then examined whether high neuroticism or low extraversion mediated this relationship.

Results

Six hundred and sixty-eight participants provided useable data. Bilateral uncinate fasciculus FA was significantly negatively associated with depressive symptoms at both waves (standardized β=0.12–0.16). Higher neuroticism and lower extraversion were also significantly associated with lower uncinate FA bilaterally (standardized β=0.09–0.15) and significantly mediated the relationship between FA and depressive symptoms.

Conclusions

Trait liability to depression and depressive symptoms are associated with reduced structural connectivity in tracts connecting the prefrontal cortex with the amygdala and anterior temporal cortex. These effects suggest that frontotemporal disconnection is linked to the etiology of depression, in part through personality trait differences.

Keywords

DepressionDTIextraversionMRIneuroticism
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 6 , June 2013 , pp. 1197 - 1206
Copyright
Copyright © Cambridge University Press 2012 

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

Anand, A, Li, Y, Wang, Y, Wu, J, Gao, S, Bukhari, L, Mathews, VP, Kalnin, A, Lowe, MJ (2005 a). Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biological Psychiatry 57, 1079–1088.CrossRefGoogle ScholarPubMed
Anand, A, Li, Y, Wang, Y, Wu, J, Gao, S, Bukhari, L, Mathews, VP, Kalnin, A, Lowe, MJ (2005 b). Antidepressant effect on connectivity of the mood-regulating circuit: an FMRI study. Neuropsychopharmacology 30, 1334–1344.CrossRefGoogle ScholarPubMed
Angst, J, Gamma, A, Endrass, J (2003). Risk factors for the bipolar and depression spectra. Acta Psychiatrica Scandinavica (Suppl.) 418, 15–19.CrossRefGoogle Scholar
Arnone, D, McIntosh, AM, Ebmeier, KP, Munafo, MR, Anderson, IM (2012). Magnetic resonance imaging studies in unipolar depression: systematic review and meta-regression analyses. European Neuropsychopharmacology 22, 1–16.CrossRefGoogle ScholarPubMed
Ball, D, Hill, L, Freeman, B, Eley, TC, Strelau, J, Riemann, R, Spinath, FM, Angleitner, A, Plomin, R (1997). The serotonin transporter gene and peer-rated neuroticism. NeuroReport 8, 1301–1304.CrossRefGoogle ScholarPubMed
Barnett, JH, Huang, J, Perlis, RH, Young, MM, Rosenbaum, JF, Nierenberg, AA, Sachs, G, Nimgaonkar, VL, Miklowitz, DJ, Smoller, JW (2011). Personality and bipolar disorder: dissecting state and trait associations between mood and personality. Psychological Medicine 41, 1593–1604.CrossRefGoogle ScholarPubMed
Baron, RM, Kenny, DA (1986). The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology 51, 1173–1182.CrossRefGoogle ScholarPubMed
Benjamini, Y, Hochberg, Y (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological) 57, 289–300.Google Scholar
Cardinal, RN, Parkinson, JA, Hall, J, Everitt, BJ (2002). Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neuroscience and Biobehavioral Reviews 26, 321–352.CrossRefGoogle ScholarPubMed
Caspi, A, Sugden, K, Moffitt, TE, Taylor, A, Craig, IW, Harrington, H, McClay, J, Mill, J, Martin, J, Braithwaite, A, Poulton, R (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386–389.CrossRefGoogle ScholarPubMed
Chaddock, CA, Barker, GJ, Marshall, N, Schulze, K, Hall, MH, Fern, A, Walshe, M, Bramon, E, Chitnis, XA, Murray, R, McDonald, C (2009). White matter microstructural impairments and genetic liability to familial bipolar I disorder. British Journal of Psychiatry 194, 527–534.CrossRefGoogle ScholarPubMed
Chepenik, LG, Raffo, M, Hampson, M, Lacadie, C, Wang, F, Jones, MM, Pittman, B, Skudlarski, P, Blumberg, HP (2010). Functional connectivity between ventral prefrontal cortex and amygdala at low frequency in the resting state in bipolar disorder. Psychiatry Research 182, 207–210.CrossRefGoogle Scholar
Clayden, JD, King, MD, Clark, CA (2009 a). Shape modelling for tract selection. Medical Image Computing and Computer-Assisted Intervention 12, 150–157.Google ScholarPubMed
Clayden, JD, Storkey, AJ, Bastin, ME (2007). A probabilistic model-based approach to consistent white matter tract segmentation. IEEE Transactions on Medical Imaging 26, 1555–1561.CrossRefGoogle ScholarPubMed
Clayden, JD, Storkey, AJ, Muñoz Maniega, S, Bastin, ME (2009 b). Reproducibility of tract segmentation between sessions using an unsupervised modelling-based approach. NeuroImage 45, 377–385.CrossRefGoogle ScholarPubMed
Costa, PT, McCrae, RR (1989). The NEO-PI/NEO-FFI Manual Supplement. Psychological Assessement Rescources: Odessa, FL.Google Scholar
Cullen, KR, Klimes-Dougan, B, Muetzel, R, Mueller, BA, Camchong, J, Houri, A, Kurma, S, Lim, KO (2010). Altered white matter microstructure in adolescents with major depression: a preliminary study. Journal of the American Academy of Child and Adolescent Psychiatry 49, 173–83e1.Google ScholarPubMed
Dalby, RB, Frandsen, J, Chakravarty, MM, Ahdidan, J, Sorensen, L, Rosenberg, R, Videbech, P, Ostergaard, L (2010). Depression severity is correlated to the integrity of white matter fiber tracts in late-onset major depression. Psychiatry Research 184, 38–48.CrossRefGoogle Scholar
Deary, IJ, Gow, AJ, Taylor, MD, Corley, J, Brett, C, Wilson, V, Campbell, H, Whalley, LJ, Visscher, PM, Porteous, DJ, Starr, JM (2007). The Lothian Birth Cohort 1936: a study to examine influences on cognitive ageing from age 11 to age 70 and beyond. BMC Geriatrics 7, 28.CrossRefGoogle ScholarPubMed
Drevets, WC, Price, JL, Simpson, JR Jr., Todd, RD, Reich, T, Vannier, M, Raichle, ME (1997). Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386, 824–827.CrossRefGoogle ScholarPubMed
Folstein, MF, Folstein, SE, McHugh, PR (1975). ‘Mini-mental state’. A practical method for grading the cognitive state of patents for the clinician. Journal of Psychiatric Research 12, 189–198.CrossRefGoogle Scholar
Huang, H, Fan, X, Williamson, DE, Rao, U (2011). White matter changes in healthy adolescents at familial risk for unipolar depression: a diffusion tensor imaging study. Neuropsychopharmacology 36, 684–691.CrossRefGoogle ScholarPubMed
Ivkovic, V, Vitart, V, Rudan, I, Janicijevic, B, Smolej-Narancic, N, Skaric-Juric, T, Barbalic, M, Polasek, O, Kolcic, I, Biloglav, Z, Visscher, PM, Hayward, C, Hastie, ND, Anderson, N, Campbell, H, Wright, AF, Rudan, P, Deary, IJ (2007). The Eysenck personality factors: psychometric structure, reliability, heritability and phenotypic and genetic correlations with psychological distress in an isolated Croatian population. Personality and Individual Differences 42, 123–133.CrossRefGoogle Scholar
Kantarci, K, Senjem, ML, Avula, R, Zhang, B, Samikoglu, AR, Weigand, SD, Przybelski, SA, Edmonson, HA, Vemuri, P, Knopman, DS, Boeve, BF, Ivnik, RJ, Smith, GE, Petersen, RC, Jack, Jr. CR (2011). Diffusion tensor imaging and cognitive function in older adults with no dementia. Neurology 77, 26–34.CrossRefGoogle ScholarPubMed
Kendler, KS, Gardner, CO (1998). Boundaries of major depression: an evaluation of DSM-IV criteria. American Journal of Psychiatry 155, 172–177.CrossRefGoogle ScholarPubMed
Kendler, KS, Gardner, CO, Prescott, CA (2002). Toward a comprehensive developmental model for major depression in women. American Journal of Psychiatry 159, 1133–1145.CrossRefGoogle Scholar
Kendler, KS, Gatz, M, Gardner, CO, Pedersen, NL (2006). Personality and major depression: a Swedish longitudinal, population-based twin study. Archives of General Psychiatry 63, 1113–1120.CrossRefGoogle ScholarPubMed
Kendler, KS, Neale, MC, Kessler, RC, Heath, AC, Eaves, LJ (1993 a). The lifetime history of major depression in women. Reliability of diagnosis and heritability. Archives of General Psychiatry 50, 863–870.CrossRefGoogle ScholarPubMed
Kendler, KS, Neale, MC, Kessler, RC, Heath, AC, Eaves, LJ (1993 b). A longitudinal twin study of personality and major depression in women. Archives of General Psychiatry 50, 853–862.CrossRefGoogle ScholarPubMed
Kendler, KS, Neale, MC, Kessler, RC, Heath, AC, Eaves, LJ (1994). The clinical characteristics of major depression as indices of the familial risk to illness. British Journal of Psychiatry 165, 66–72.CrossRefGoogle ScholarPubMed
Kumar, A, Jin, Z, Bilker, W, Udupa, J, Gottlieb, G (1998). Late-onset minor and major depression: early evidence for common neuroanatomical substrates detected by using MRI. Proceedings of the National Academy of Sciences USA 95, 7654–7658.CrossRefGoogle ScholarPubMed
Lawrie, SM, Buechel, C, Whalley, HC, Frith, CD, Friston, KJ, Johnstone, EC (2002). Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations. Biological Psychiatry 51, 1008–1011.CrossRefGoogle ScholarPubMed
Levinson, DF (2006). The genetics of depression: a review. Biological Psychiatry 60, 84–92.CrossRefGoogle ScholarPubMed
Maier, W, Minges, J, Lichtermann, D, Heun, R, Franke, P (1994). Personality variations in healthy relatives of schizophrenics. Schizophrenia Research 12, 81–88.CrossRefGoogle ScholarPubMed
Maniega, SM, Bastin, ME, McIntosh, AM, Lawrie, SM, Clayden, JD (2008). Atlas-based reference tracts improve automatic white matter segmentation with neighbourhood tractography. In Proceedings of the 16th Scientific Meeting of the ISMRM, p. 3318. International Society for Magnetic Resonance in Medicine, Berkley, CA, USA.Google Scholar
Matthews, G, Deary, IJ, Whiteman, MC (2009). Personality Traits. Cambridge University Press: Cambridge.CrossRefGoogle Scholar
McGue, M, Christensen, K (1997). Genetic and environmental contributions to depression symptomatology: evidence from Danish twins 75 years of age and older. Journal of Abnormal Psychology 106, 439–448.CrossRefGoogle ScholarPubMed
McGue, M, Christensen, K (2003). The heritability of depression symptoms in elderly Danish twins: occasion-specific versus general effects. Behavior Genetics 33, 83–93.CrossRefGoogle ScholarPubMed
Mori, S, van Zijl, P (2007). Human white matter atlas. American Journal of Psychiatry 164, 1005.CrossRefGoogle ScholarPubMed
Murray, CJL, Lopez, AD (1997). Alternative projections of mortality and disability by cause 1990–2020: Global Burden of Disease Study. Lancet 349, 1498–1504.CrossRefGoogle ScholarPubMed
Pezawas, L, Meyer-Lindenberg, A, Drabant, EM, Verchinski, BA, Munoz, KE, Kolachana, BS, Egan, MF, Mattay, VS, Hariri, AR, Weinberger, DR (2005). 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nature Neuroscience 8, 828–834.CrossRefGoogle ScholarPubMed
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry 54, 504–514.CrossRefGoogle ScholarPubMed
Sheline, YI, Price, JL, Vaishnavi, SN, Mintun, MA, Barch, DM, Epstein, AA, Wilkins, CH, Snyder, AZ, Couture, L, Schechtman, K, McKinstry, RC (2008). Regional white matter hyperintensity burden in automated segmentation distinguishes late-life depressed subjects from comparison subjects matched for vascular risk factors. American Journal of Psychiatry 165, 524–532.CrossRefGoogle ScholarPubMed
Sprooten, E, Sussmann, JE, Clugston, A, Peel, A, McKirdy, J, William, T, Moorhead, J, Anderson, S, Shand, AJ, Giles, S, Bastin, ME, Hall, J, Johnstone, EC, Lawrie, SM, McIntosh, AM (2011). White matter integrity in individuals at high genetic risk of bipolar disorder. Biological Psychiatry 70, 350–356.CrossRefGoogle ScholarPubMed
Taylor, WD, MacFall, JR, Gerig, G, Krishnan, RR (2007). Structural integrity of the uncinate fasciculus in geriatric depression: relationship with age of onset. Neuropsychiatric Disease and Treatment 3, 669–674.Google ScholarPubMed
Thornicroft, G, Sartorius, N (1993). The course and outcome of depression in different cultures: 10-year follow-up of the WHO collaborative study on the assessment of depressive disorders. Psychological Medicine 23, 1023–1032.CrossRefGoogle Scholar
van Os, J, Jones, PB (2001). Neuroticism as a risk factor for schizophrenia. Psychological Medicine 31, 1129–1134.CrossRefGoogle ScholarPubMed
Videbech, P (1997). MRI findings in patients with affective disorder: a meta-analysis. Acta Psychiatrica Scandinavica 96, 157–168.CrossRefGoogle ScholarPubMed
Videbech, P, Ravnkilde, B (2004). Hippocampal volume and depression: a meta-analysis of MRI studies. American Journal of Psychiatry 161, 1957–1966.CrossRefGoogle ScholarPubMed
Wardlaw, JM, Bastin, ME, Valdes Hernandez, MC, Muñoz Maniega, S, Royle, NA, Morris, Z, Clayden, JD, Sandeman, EM, Eadie, E, Murray, C, Starr, JM, Deary, IJ (2011). Brain ageing, cognition in youth and old age, and vascular disease in the Lothian Birth Cohort 1936: rationale, design and methodology of the imaging protocol. International Journal of Stroke 6, 547–559.CrossRefGoogle ScholarPubMed
Westlye, LT, Bjornebekk, A, Grydeland, H, Fjell, AM, Walhovd, KB (2011). Linking an anxiety-related personality trait to brain white matter microstructure: diffusion tensor imaging and harm avoidance. Archives of General Psychiatry 68, 369–377.CrossRefGoogle ScholarPubMed
Zanetti, MV, Jackowski, MP, Versace, A, Almeida, JR, Hassel, S, Duran, FL, Busatto, GF, Kupfer, DJ, Phillips, ML (2009). State-dependent microstructural white matter changes in bipolar I depression. European Archives of Psychiatry and Clinical Neuroscience 259, 316–328.CrossRefGoogle ScholarPubMed
Zigmond, AS, Snaith, RP (1983). The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica 67, 361–370.CrossRefGoogle ScholarPubMed
Supplementary material: File

McIntosh supplementary materials

McIntosh supplementary materials

Download McIntosh supplementary materials(File)
File 17 KB