Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-02T19:24:47.119Z Has data issue: false hasContentIssue false
  • English
  • Français

Alterations in white matter micro-integrity of the superior longitudinal fasciculus and anterior thalamic radiation of young adult patients with depression

Published online by Cambridge University Press:  06 March 2014

C.-H. Lai  and
Y.-T. Wu
C.-H. Lai
Affiliation:
Department of Psychiatry, Cheng Hsin General Hospital, Taipei City, Taiwan, ROC Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, Taipei, Taiwan, ROC
Y.-T. Wu*
Affiliation:
Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, Taipei, Taiwan, ROC Brain Research Center, National Yang-Ming University, Taipei, Taiwan, ROC
*
* Author for correspondence: Yu-Te Wu, Department of Biomedical Imaging and Radiological Sciences, National Yang Ming University, No. 155, Sec. 2, Linong Street, Taipei, 112 Taiwan, Taiwan, ROC. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

This study surveyed the characteristics of white matter (WM) micro-integrity in patients who were diagnosed with major depressive disorder (MDD) without co-morbidities.

Method

A total of 44 patients with MDD and 27 normal controls were enrolled in our study. Diffusion tensor imaging images of patients and controls were pre-processed and analysed to estimate differences in WM micro-integrity between patients and controls by performing comparisons of the values obtained from fractional anisotropy (FA). FA outputs of patients and controls were compared by a non-parametric permutation-based method with global brain volume, age and gender as covariates. In addition, the between-group differences of radial diffusivity (RD) and axial diffusivity (AD) were assessed to explain the alterations in FA values. Correlations between clinical variables (such as depression severity, anxiety severity, illness duration) and FA values were also estimated in each group and across both groups.

Results

The patients with MDD had significantly lower FA values than the controls, for the left superior longitudinal fasciculus (SLF) and the right anterior thalamic radiation (ATR). The reductions in FA values occurred in combination with elevated RD values in the bilateral SLF and decreased AD values in the bilateral ATR. FA values were negatively correlated with depression severity in the SLF and with illness duration in the right SLF and ATR.

Conclusions

MDD patients had significant alterations in the WM micro-integrity of the left SLF and the right ATR.

Keywords

Anterior thalamic radiationdepressionsuperior longitudinal fasciculuswhite matter
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 13 , October 2014 , pp. 2825 - 2832
Copyright
Copyright © Cambridge University Press 2014 

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

Aghajani, M, Veer, IM, van Lang, ND, Meens, PH, van den Bulk, BG, Rombouts, SA, Vermeiren, RR, van der Wee, NJ (2013). Altered white-matter architecture in treatment-naive adolescents with clinical depression. Psychologicl Medicine. Published online 16 12 2013 . doi:10.1017/S0033291713003000.Google Scholar
Bernal, B, Altman, N (2010). The connectivity of the superior longitudinal fasciculus: a tractography DTI study. Magnetic Resonance Imaging 28, 217–225.Google Scholar
Biesbroek, JM, Kuijf, HJ, van der Graaf, Y, Vincken, KL, Postma, A, Mali, WP, Biessels, GJ, Geerlings, MI; The SMART-MR Study Group (2013). Association between subcortical vascular lesion location and cognition: a voxel-based and tract-based lesion–symptom mapping study. The SMART-MR study. PLOS ONE 8, e60541.Google Scholar
Charlton, RA, Lamar, M, Zhang, A, Yang, S, Ajilore, O, Kumar, A (2013). White-matter tract integrity in late-life depression: associations with severity and cognition. Psychological Medicine. Published online 16 09 2013 . doi:10.1017/S0033291713001980.Google Scholar
Coenen, VA, Panksepp, J, Hurwitz, TA, Urbach, H, Madler, B (2012). Human medial forebrain bundle (MFB) and anterior thalamic radiation (ATR): imaging of two major subcortical pathways and the dynamic balance of opposite affects in understanding depression. Journal of Neuropsychiatry and Clinical Neurosciences 24, 223–236.Google Scholar
Cole, J, Chaddock, CA, Farmer, AE, Aitchison, KJ, Simmons, A, McGuffin, P, Fu, CH (2012). White matter abnormalities and illness severity in major depressive disorder. British Journal of Psychiatry 201, 33–39.Google Scholar
Dalby, RB, Chakravarty, MM, Ahdidan, J, Sorensen, L, Frandsen, J, Jonsdottir, KY, Tehrani, E, Rosenberg, R, Ostergaard, L, Videbech, P (2010 a). Localization of white-matter lesions and effect of vascular risk factors in late-onset major depression. Psychological Medicine 40, 1389–1399.Google Scholar
Dalby, RB, Frandsen, J, Chakravarty, MM, Ahdidan, J, Sorensen, L, Rosenberg, R, Videbech, P, Ostergaard, L (2010 b). Depression severity is correlated to the integrity of white matter fiber tracts in late-onset major depression. Psychiatry Research: Neuroimaging 184, 38–48.Google Scholar
de Diego-Adeliño, J, Pires, P, Gómez-Ansón, B, Serra-Blasco, M, Vives-Gilabert, Y, Puigdemont, D, Martín-Blanco, A, Alvarez, E, Pérez, V, Portella, MJ (2013). Microstructural white-matter abnormalities associated with treatment resistance, severity and duration of illness in major depression. Psychological Medicine. Published online 21 08 2013 . doi:10.1017/S003329171300158X.Google Scholar
Frodl, T, Carballedo, A, Fagan, AJ, Lisiecka, D, Ferguson, Y, Meaney, JF (2012). Effects of early-life adversity on white matter diffusivity changes in patients at risk for major depression. Journal of Psychiatry and Neuroscience 37, 37–45.Google Scholar
Guo, WB, Liu, F, Chen, JD, Xu, XJ, Wu, RR, Ma, CQ, Gao, K, Tan, CL, Sun, XL, Xiao, CQ, Chen, HF, Zhao, JP (2012). Altered white matter integrity of forebrain in treatment-resistant depression: a diffusion tensor imaging study with tract-based spatial statistics. Progress in Neuropsychopharmacology and Biological Psychiatry 38, 201–206.Google Scholar
Gutman, DA, Holtzheimer, PE, Behrens, TE, Johansen-Berg, H, Mayberg, HS (2009). A tractography analysis of two deep brain stimulation white matter targets for depression. Biological Psychiatry 65, 276–282.Google Scholar
Huang, H, Gundapuneedi, T, Rao, U (2012). White matter disruptions in adolescents exposed to childhood maltreatment and vulnerability to psychopathology. Neuropsychopharmacology 37, 2693–2701.Google Scholar
Jenkinson, M, Smith, S (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis 5, 143–156.Google Scholar
Klarborg, B, Skak Madsen, K, Vestergaard, M, Skimminge, A, Jernigan, TL, Baaré, WF (2012). Sustained attention is associated with right superior longitudinal fasciculus and superior parietal white matter microstructure in children. Human Brain Mapping 34, 3216–3232.Google Scholar
Korgaonkar, MS, Grieve, SM, Koslow, SH, Gabrieli, JD, Gordon, E, Williams, LM (2011). Loss of white matter integrity in major depressive disorder: evidence using tract-based spatial statistical analysis of diffusion tensor imaging. Human Brain Mapping 32, 2161–2171.Google Scholar
Liao, Y, Huang, X, Wu, Q, Yang, C, Kuang, W, Du, M, Lui, S, Yue, Q, Chan, RC, Kemp, GJ, Gong, Q (2013). Is depression a disconnection syndrome? Meta-analysis of diffusion tensor imaging studies in patients with MDD. Journal of Psychiatry and Neuroscience 38, 49–56.Google Scholar
Mamah, D, Conturo, TE, Harms, MP, Akbudak, E, Wang, L, McMichael, AR, Gado, MH, Barch, DM, Csernansky, JG (2010). Anterior thalamic radiation integrity in schizophrenia: a diffusion-tensor imaging study. Psychiatry Research: Neuroimaging 183, 144–150.CrossRefGoogle ScholarPubMed
McIntosh, AM, Bastin, ME, Luciano, M, Maniega, SM, Del C Valdés Hernández, M, Royle, NA, Hall, J, Murray, C, Lawrie, SM, Starr, JM, Wardlaw, JM, Deary, IJ (2013). Neuroticism, depressive symptoms and white-matter integrity in the Lothian Birth Cohort 1936. Psychological Medicine 43, 1197–1206.Google Scholar
Mettenburg, JM, Benzinger, TL, Shimony, JS, Snyder, AZ, Sheline, YI (2012). Diminished performance on neuropsychological testing in late life depression is correlated with microstructural white matter abnormalities. Neuroimage 60, 2182–2190.Google Scholar
Murphy, ML, Carballedo, A, Fagan, AJ, Morris, D, Fahey, C, Meaney, J, Frodl, T (2012). Neurotrophic tyrosine kinase polymorphism impacts white matter connections in patients with major depressive disorder. Biological Psychiatry 72, 663–670.Google Scholar
Murphy, ML, Frodl, T (2011). Meta-analysis of diffusion tensor imaging studies shows altered fractional anisotropy occurring in distinct brain areas in association with depression. Biology of Mood and Anxiety Disorders 1, 3.Google Scholar
Niida, A, Niida, R, Kuniyoshi, K, Motomura, M, Uechi, A (2013). Usefulness of visual evaluation of the anterior thalamic radiation by diffusion tensor tractography for differentiating between Alzheimer's disease and elderly major depressive disorder patients. International Journal of General Medicine 6, 189–200.Google Scholar
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9, 97–113.Google Scholar
Peng, HJ, Zheng, HR, Ning, YP, Zhang, Y, Shan, BC, Zhang, L, Yang, HC, Liu, J, Li, ZX, Zhou, JS, Zhang, ZJ, Li, LJ (2013). Abnormalities of cortical–limbic–cerebellar white matter networks may contribute to treatment-resistant depression: a diffusion tensor imaging study. BMC Psychiatry 13, 72.Google Scholar
Seok, JH, Choi, S, Lim, HK, Lee, SH, Kim, I, Ham, BJ (2013). Effect of the COMT val158met polymorphism on white matter connectivity in patients with major depressive disorder. Neuroscience Letters 545, 35–39.Google Scholar
Sexton, CE, Le Masurier, M, Allan, CL, Jenkinson, M, McDermott, L, Kalu, UG, Herrmann, LL, Bradley, KM, Mackay, CE, Ebmeier, KP (2012). Magnetic resonance imaging in late-life depression: vascular and glucocorticoid cascade hypotheses. British Journal of Psychiatry 201, 46–51.Google Scholar
Sheline, YI (2000). 3D MRI studies of neuroanatomic changes in unipolar major depression: the role of stress and medical comorbidity. Biological Psychiatry 48, 791–800.Google Scholar
Smith, SM (2002). Fast robust automated brain extraction. Human Brain Mapping 17, 143–155.Google Scholar
Smith, SM, Jenkinson, M, Woolrich, MW, Beckmann, CF, Behrens, TE, Johansen-Berg, H, Bannister, PR, De Luca, M, Drobnjak, I, Flitney, DE, Niazy, RK, Saunders, J, Vickers, J, Zhang, Y, De Stefano, N, Brady, JM, Matthews, PM (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 (Suppl. 1), S208–S219.Google Scholar
Smith, SM, Johansen-Berg, H, Jenkinson, M, Rueckert, D, Nichols, TE, Miller, KL, Robson, MD, Jones, DK, Klein, JC, Bartsch, AJ, Behrens, TE (2007). Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nature Protocols 2, 499–503.Google Scholar
Song, SK, Yoshino, J, Le, TQ, Lin, SJ, Sun, SW, Cross, AH, Armstrong, RC (2005). Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26, 132–140.Google Scholar
Spalletta, G, Fagioli, S, Caltagirone, C, Piras, F (2012). Brain microstructure of subclinical apathy phenomenology in healthy individuals. Human Brain Mapping 34, 3193–3203.CrossRefGoogle ScholarPubMed
Steffens, DC, Taylor, WD, Denny, KL, Bergman, SR, Wang, L (2011). Structural integrity of the uncinate fasciculus and resting state functional connectivity of the ventral prefrontal cortex in late life depression. PLoS One 6, e22697.Google Scholar
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 Scholar
Versace, A, Almeida, JR, Quevedo, K, Thompson, WK, Terwilliger, RA, Hassel, S, Kupfer, DJ, Phillips, ML (2010). Right orbitofrontal corticolimbic and left corticocortical white matter connectivity differentiate bipolar and unipolar depression. Biological Psychiatry 68, 560–567.Google Scholar
Vestergaard, M, Madsen, KS, Baare, WF, Skimminge, A, Ejersbo, LR, Ramsoy, TZ, Gerlach, C, Akeson, P, Paulson, OB, Jernigan, TL (2011). White matter microstructure in superior longitudinal fasciculus associated with spatial working memory performance in children. Journal of Cognitive Neuroscience 23, 2135–2146.CrossRefGoogle ScholarPubMed
Woolrich, MW, Jbabdi, S, Patenaude, B, Chappell, M, Makni, S, Behrens, T, Beckmann, C, Jenkinson, M, Smith, SM (2009). Bayesian analysis of neuroimaging data in FSL. Neuroimage 45, S173–S186.Google Scholar
Zhang, A, Leow, A, Ajilore, O, Lamar, M, Yang, S, Joseph, J, Medina, J, Zhan, L, Kumar, A (2012). Quantitative tract-specific measures of uncinate and cingulum in major depression using diffusion tensor imaging. Neuropsychopharmacology 37, 959–967.Google Scholar
Zou, K, Huang, X, Li, T, Gong, Q, Li, Z, Ou-yang, L, Deng, W, Chen, Q, Li, C, Ding, Y, Sun, X (2008). Alterations of white matter integrity in adults with major depressive disorder: a magnetic resonance imaging study. Journal of Psychiatry and Neuroscience 33, 525–530.Google Scholar