Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-22T19:38:52.445Z Has data issue: false hasContentIssue false
  • English
  • Français

Altered white-matter architecture in treatment-naive adolescents with clinical depression

Published online by Cambridge University Press:  16 December 2013

M. Aghajani ,
I. M. Veer ,
N. D. J. van Lang ,
P. H. F. Meens ,
B. G. van den Bulk ,
S. A. R. B. Rombouts ,
R. R. J. M. Vermeiren  and
N. J. van der Wee
M. Aghajani*
Affiliation:
Department of Child and Adolescent Psychiatry, Curium, Leiden University Medical Center, The Netherlands Leiden Institute for Brain and Cognition (LIBC), The Netherlands
I. M. Veer
Affiliation:
Leiden Institute for Brain and Cognition (LIBC), The Netherlands Department of Psychiatry and Psychotherapy, Division of Mind and Brain Research, Charité Universitätsmedizin, Berlin, Germany
N. D. J. van Lang
Affiliation:
Department of Child and Adolescent Psychiatry, Curium, Leiden University Medical Center, The Netherlands Leiden Institute for Brain and Cognition (LIBC), The Netherlands
P. H. F. Meens
Affiliation:
Department of Child and Adolescent Psychiatry, Curium, Leiden University Medical Center, The Netherlands
B. G. van den Bulk
Affiliation:
Department of Child and Adolescent Psychiatry, Curium, Leiden University Medical Center, The Netherlands Leiden Institute for Brain and Cognition (LIBC), The Netherlands Institute of Psychology, Leiden University, The Netherlands
S. A. R. B. Rombouts
Affiliation:
Leiden Institute for Brain and Cognition (LIBC), The Netherlands Institute of Psychology, Leiden University, The Netherlands Department of Radiology, Leiden University Medical Center, The Netherlands
R. R. J. M. Vermeiren
Affiliation:
Department of Child and Adolescent Psychiatry, Curium, Leiden University Medical Center, The Netherlands Leiden Institute for Brain and Cognition (LIBC), The Netherlands
N. J. van der Wee
Affiliation:
Leiden Institute for Brain and Cognition (LIBC), The Netherlands Department of Psychiatry, Leiden University Medical Center, The Netherlands
*
*Address for correspondence: M. Aghajani, M.Sc., Department of Child and Adolescent Psychiatry, Curium, Leiden University Medical Center, PO Box 15, 2300 AA Leiden, The Netherlands. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Depressive disorders are highly prevalent in adolescence and confer a heightened risk of recurrence in adulthood. Insight into the developmental neurocircuitry of depression could advance our understanding of depression and aid the development of effective treatment strategies. Whereas white-matter (WM) abnormalities are strongly implicated in adult depression, we still lack a firm understanding of WM architecture in adolescent depression. Using diffusion tensor imaging (DTI), we set out to investigate WM microstructure in a sample of clinically depressed adolescents relative to matched controls.

Method

We employed tract-based spatial statistics (TBSS) to examine WM microstructure in 25 treatment-naive adolescents with clinical depression relative to 21 matched controls. Using TBSS, we examined fractional anisotropy (FA), axial diffusivity (AD), radial diffusivity (RD) and mean diffusivity (MD). Threshold-free cluster enhancement (TFCE) with family-wise error (FWE) correction was used to control for multiple comparisons.

Results

Our analysis revealed abnormal WM microstructure in clinically depressed adolescents. More specifically, whole-brain analysis revealed that patients had lower FA values in the body of the corpus callosum (CC), coupled with elevated RD and MD, and preserved AD. Conversely, region-of-interest analysis revealed that patients had higher FA values in the uncinate fasciculus (UF), coupled with elevated AD, reduced RD and preserved MD.

Conclusions

In line with neurocircuitry models of depression, our findings suggest that WM abnormalities within pathways facilitating cognitive and emotional functioning are involved in the pathophysiology of depression. Importantly, our findings show that these WM abnormalities are already present early in the course of the disorder.

Keywords

Adolescentscorpus callosumdepressiondiffusion tensor imaginguncinate fasciculuswhite matter
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 11 , August 2014 , pp. 2287 - 2298
Copyright
Copyright © Cambridge University Press 2013 

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

Achenbach, TM (1991 a). Manual for the Child Behavior Checklist/4–18 and 1991 Profiles. Department of Psychiatry, University of Vermont: Burlington, VT.Google Scholar
Achenbach, TM (1991 b). Manual for the Youth Self-Report and 1991 Profiles. Department of Psychiatry, University of Vermont: Burlington, VT.Google Scholar
Alexopoulos, GS, Murphy, CF, Gunning-Dixon, FM, Latoussakis, V, Kanellopoulos, D, Klimstra, S, Lim, KO, Hoptman, MJ (2008). Microstructural white matter abnormalities and remission of geriatric depression. American Journal of Psychiatry 165, 238–244.CrossRefGoogle ScholarPubMed
Angold, A, Erkanli, A, Silberg, J, Eaves, L, Costello, EJ (2002). Depression scale scores in 8–17-year-olds: effects of age and gender. Journal of Child Psychology and Psychiatry and Allied Disciplines 43, 1052–1063.CrossRefGoogle ScholarPubMed
Ayling, E, Aghajani, M, Fouche, JP, van der Wee, N (2012). Diffusion tensor imaging in anxiety disorders. Current Psychiatry Reports 14, 197–202.CrossRefGoogle ScholarPubMed
Basser, PJ, Mattiello, J, LeBihan, D (1994). MR diffusion tensor spectroscopy and imaging. Biophysical Journal 66, 259–267.CrossRefGoogle ScholarPubMed
Benes, FM (2010). Amygdalocortical circuitry in schizophrenia: from circuits to molecules. Neuropsychopharmacology 35, 239–257.CrossRefGoogle ScholarPubMed
Bloom, JS, Hynd, GW (2005). The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition? Neuropsychology Review 15, 59–71.CrossRefGoogle ScholarPubMed
Braun, CM, Larocque, C, Daigneault, S, Montour-Proulx, I (1999). Mania, pseudomania, depression, and pseudodepression resulting from focal unilateral cortical lesions. Neuropsychiatry, Neuropsychology, and Behavioral Neurology 12, 35–51.Google ScholarPubMed
Budde, MD, Xie, M, Cross, AH, Song, SK (2009). Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis. Journal of Neuroscience 29, 2805–2813.CrossRefGoogle ScholarPubMed
Caetano, SC, Fonseca, M, Hatch, JP, Olvera, RL, Nicoletti, M, Hunter, K, Lafer, B, Pliszka, SR, Soares, JC (2007). Medial temporal lobe abnormalities in pediatric unipolar depression. Neuroscience Letters 427, 142–147.CrossRefGoogle ScholarPubMed
Casey, BJ, Jones, RM, Hare, TA (2008). The adolescent brain. Annals of the New York Academy of Sciences 1124, 111–126.CrossRefGoogle ScholarPubMed
CDC (2007). Suicide trends among youths and young adults aged 10–24 years – United States, 1990–2004. Morbidity and Mortality Weekly Report 56, 905–908.Google Scholar
Chorpita, BF, Yim, L, Moffitt, C, Umemoto, LA, Francis, SE (2000). Assessment of symptoms of DSM-IV anxiety and depression in children: a revised child anxiety and depression scale. Behaviour Research and Therapy 38, 835–855.CrossRefGoogle ScholarPubMed
Clark, C, Rodgers, B, Caldwell, T, Power, C, Stansfeld, S (2007). Childhood and adulthood psychological ill health as predictors of midlife affective and anxiety disorders: the 1958 British Birth Cohort. Archives of General Psychiatry 64, 668–678.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Costello, EJ, Angold, A, Burns, BJ, Stangl, DK, Tweed, DL, Erkanli, A, Worthman, CM (1996). The Great Smoky Mountains Study of Youth. Goals, design, methods, and the prevalence of DSM-III-R disorders. Archives of General Psychiatry 53, 1129–1136.CrossRefGoogle ScholarPubMed
Costello, EJ, Mustillo, S, Erkanli, A, Keeler, G, Angold, A (2003). Prevalence and development of psychiatric disorders in childhood and adolescence. Archives of General Psychiatry 60, 837–844.CrossRefGoogle ScholarPubMed
Cullen, KR, Gee, DG, Klimes-Dougan, B, Gabbay, V, Hulvershorn, L, Mueller, BA, Camchong, J, Bell, CJ, Houri, A, Kumra, S, Lim, KO, Castellanos, FX, Milham, MP (2009). A preliminary study of functional connectivity in comorbid adolescent depression. Neuroscience Letters 460, 227–231.CrossRefGoogle ScholarPubMed
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, 173–183.e1.Google ScholarPubMed
Davidson, RJ, Irwin, W (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Sciences 3, 11–21.CrossRefGoogle ScholarPubMed
Drevets, WC, Price, JL, Furey, ML (2008). Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Structure and Function 213, 93–118.CrossRefGoogle ScholarPubMed
Fields, RD (2008). White matter in learning, cognition and psychiatric disorders. Trends in Neurosciences 31, 361–370.CrossRefGoogle ScholarPubMed
Gazzaniga, MS (2000). Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition? Brain 123, 1293–1326.CrossRefGoogle ScholarPubMed
Guberman, C, Manassis, K (2011). Symptomatology and family functioning in children and adolescents with comorbid anxiety and depression. Journal of the Canadian Academy of Child and Adolescent Psychiatry 20, 186–195.Google ScholarPubMed
Herrmann, LL, Le Masurier, M, Ebmeier, KP (2008). White matter hyperintensities in late life depression: a systematic review. Journal of Neurology, Neurosurgery and Psychiatry 79, 619–624.CrossRefGoogle ScholarPubMed
Horsfield, MA, Jones, DK (2002). Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases – a review. NMR in Biomedicine 15, 570–577.CrossRefGoogle ScholarPubMed
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
Hubl, D, Koenig, T, Strik, W, Federspiel, A, Kreis, R, Boesch, C, Maier, SE, Schroth, G, Lovblad, K, Dierks, T (2004). Pathways that make voices: white matter changes in auditory hallucinations. Archives of General Psychiatry 61, 658–668.CrossRefGoogle ScholarPubMed
Hulvershorn, LA, Cullen, K, Anand, A (2011). Toward dysfunctional connectivity: a review of neuroimaging findings in pediatric major depressive disorder. Brain Imaging and Behavior 5, 307–328.CrossRefGoogle ScholarPubMed
Kier, EL, Staib, LH, Davis, LM, Bronen, RA (2004). MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer's loop of the optic radiation. American Journal of Neuroradiology 25, 677–691.Google ScholarPubMed
Kieseppa, T, Eerola, M, Mantyla, R, Neuvonen, T, Poutanen, VP, Luoma, K, Tuulio-Henriksson, A, Jylha, P, Mantere, O, Melartin, T, Rytsala, H, Vuorilehto, M, Isometsa, E (2010). Major depressive disorder and white matter abnormalities: a diffusion tensor imaging study with tract-based spatial statistics. Journal of Affective Disorders 120, 240–244.CrossRefGoogle ScholarPubMed
Kim, MJ, Whalen, PJ (2009). The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. Journal of Neuroscience 29, 11614–11618.CrossRefGoogle ScholarPubMed
Kochunov, P, Thompson, PM, Lancaster, JL, Bartzokis, G, Smith, S, Coyle, T, Royall, DR, Laird, A, Fox, PT (2007). Relationship between white matter fractional anisotropy and other indices of cerebral health in normal aging: tract-based spatial statistics study of aging. NeuroImage 35, 478–487.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Kovacs, M (1992). The Children's Depression Inventory (CDI) Manual . MultiHealth Systems: New York, NY.Google Scholar
Lamar, M, Charlton, RA, Morris, RG, Markus, HS (2010). The impact of subcortical white matter disease on mood in euthymic older adults: a diffusion tensor imaging study. American Journal of Geriatric Psychiatry 18, 634–642.CrossRefGoogle ScholarPubMed
Lebel, C, Gee, M, Camicioli, R, Wieler, M, Martin, W, Beaulieu, C (2012). Diffusion tensor imaging of white matter tract evolution over the lifespan. NeuroImage 60, 340–352.CrossRefGoogle ScholarPubMed
Li, F, Huang, X, Yang, Y, Li, B, Wu, Q, Zhang, T, Lui, S, Kemp, GJ, Gong, Q (2011). Microstructural brain abnormalities in patients with obsessive-compulsive disorder: diffusion-tensor MR imaging study at 3.0 T. Radiology 260, 216–223.CrossRefGoogle ScholarPubMed
Li, L, Ma, N, Li, Z, Tan, L, Liu, J, Gong, G, Shu, N, He, Z, Jiang, T, Xu, L (2007). Prefrontal white matter abnormalities in young adult with major depressive disorder: a diffusion tensor imaging study. Brain Research 1168, 124–128.CrossRefGoogle ScholarPubMed
Ma, N, Li, L, Shu, N, Liu, J, Gong, G, He, Z, Li, Z, Tan, L, Stone, WS, Zhang, Z, Xu, L, Jiang, T (2007). White matter abnormalities in first-episode, treatment-naive young adults with major depressive disorder. American Journal of Psychiatry 164, 823–826.CrossRefGoogle ScholarPubMed
Masten, CL, Eisenberger, NI, Borofsky, LA, McNealy, K, Pfeifer, JH, Dapretto, M (2011). Subgenual anterior cingulate responses to peer rejection: a marker of adolescents’ risk for depression. Development and Psychopathology 23, 283–292.CrossRefGoogle ScholarPubMed
Mayberg, HS (2003). Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. British Medical Bulletin 65, 193–207.CrossRefGoogle ScholarPubMed
Merikangas, KR, Avenevoli, S (2002). Epidemiology of mood and anxiety disorders in children and adolescents. In Textbook in Psychiatric Epidemiology (ed. Tsaung, M. T. and Tohen, M.), pp. 657–704. John Wiley & Sons, Inc.: New York.CrossRefGoogle Scholar
Montag, C, Reuter, M, Weber, B, Markett, S, Schoene-Bake, JC (2012). Individual differences in trait anxiety are associated with white matter tract integrity in the left temporal lobe in healthy males but not females. Neuroscience 217, 77–83.CrossRefGoogle Scholar
Mori, S, Wakana, S, Nagae-Poetscher, LM, van Zijl, PCM (2005). MRI Atlas of Human White Matter. Elsevier: Amsterdam, The Netherlands.Google Scholar
Murray, CJL, Salomon, JA, Mathers, C (2000). A critical examination of summary measures of population health. Bulletin of the World Health Organization 78, 981–994.Google ScholarPubMed
Nakamae, T, Narumoto, J, Shibata, K, Matsumoto, R, Kitabayashi, Y, Yoshida, T, Yamada, K, Nishimura, T, Fukui, K (2008). Alteration of fractional anisotropy and apparent diffusion coefficient in obsessive-compulsive disorder: a diffusion tensor imaging study. Progress in Neuro-Psychopharmacology and Biological Psychiatry 32, 1221–1226.CrossRefGoogle ScholarPubMed
Nobuhara, K, Okugawa, G, Sugimoto, T, Minami, T, Tamagaki, C, Takase, K, Saito, Y, Sawada, S, Kinoshita, T (2006). Frontal white matter anisotropy and symptom severity of late-life depression: a magnetic resonance diffusion tensor imaging study. Journal of Neurology, Neurosurgery and Psychiatry 77, 120–122.CrossRefGoogle ScholarPubMed
Paul, LK, Lautzenhiser, A, Brown, WS, Hart, A, Neumann, D, Spezio, M, Adolphs, R (2006). Emotional arousal in agenesis of the corpus callosum. International Journal of Psychophysiology 61, 47–56.CrossRefGoogle ScholarPubMed
Petrides, M, Pandya, DN (2002). Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. European Journal of Neuroscience 16, 291–310.CrossRefGoogle ScholarPubMed
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003 a). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry 54, 504–514.CrossRefGoogle ScholarPubMed
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003 b). Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biological Psychiatry 54, 515–528.CrossRefGoogle ScholarPubMed
Phillips, ML, Ladouceur, CD, Drevets, WC (2008). A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry 13, 833–857.CrossRefGoogle ScholarPubMed
Price, JL, Drevets, WC (2010). Neurocircuitry of mood disorders. Neuropsychopharmacology 35, 192–216.CrossRefGoogle ScholarPubMed
Rao, U, Chen, L-A (2009). Characteristics, correlates, and outcomes of childhood and adolescent depressive disorders. Dialogues in Clinical Neuroscience 11, 45–62.CrossRefGoogle ScholarPubMed
Rosso, IM, Cintron, CM, Steingard, RJ, Renshaw, PF, Young, AD, Yurgelun-Todd, DA (2005). Amygdala and hippocampus volumes in pediatric major depression. Biological Psychiatry 57, 21–26.CrossRefGoogle ScholarPubMed
Ryan, ND, Puig-Antich, J, Ambrosini, P, Rabinovich, H, Robinson, D, Nelson, B, Iyengar, S, Twomey, J (1987). The clinical picture of major depression in children and adolescents. Archives of General Psychiatry 44, 854–861.CrossRefGoogle ScholarPubMed
Seltzer, B, Pandya, DN (1986). Posterior parietal projections to the intraparietal sulcus of the rhesus monkey. Experimental Brain Research 62, 459–469.CrossRefGoogle Scholar
Sexton, CE, Mackay, CE, Ebmeier, KP (2009). A systematic review of diffusion tensor imaging studies in affective disorders. Biological Psychiatry 66, 814–823.CrossRefGoogle ScholarPubMed
Shimony, JS, Sheline, YI, D'Angelo, G, Epstein, AA, Benzinger, TL, Mintun, MA, McKinstry, RC, Snyder, AZ (2009). Diffuse microstructural abnormalities of normal-appearing white matter in late life depression: a diffusion tensor imaging study. Biological Psychiatry 66, 245–252.CrossRefGoogle ScholarPubMed
Silverman, W, Albano, A (1996). The Anxiety Disorders Interview Schedule for DSM-IV – Child and Parent Versions. Raywind Publications: San Antonio, TX.Google Scholar
Smith, SM, Jenkinson, M, Johansen-Berg, H, Rueckert, D, Nichols, TE, Mackay, CE, Watkins, KE, Ciccarelli, O, Cader, MZ, Matthews, PM, Behrens, TEJ (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31, 1487–1505.CrossRefGoogle ScholarPubMed
Smith, SM, Nichols, TE (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 44, 83–98.CrossRefGoogle ScholarPubMed
Song, SK, Sun, SW, Ramsbottom, MJ, Chang, C, Russell, J, Cross, AH (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 17, 1429–1436.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.CrossRefGoogle ScholarPubMed
Stein, JL, Wiedholz, LM, Bassett, DS, Weinberger, DR, Zink, CF, Mattay, VS, Meyer-Lindenberg, A (2007). A validated network of effective amygdala connectivity. NeuroImage 36, 736–745.CrossRefGoogle ScholarPubMed
Tamietto, M, Adenzato, M, Geminiani, G, de Gelder, B (2007). Fast recognition of social emotions takes the whole brain: interhemispheric cooperation in the absence of cerebral asymmetry. Neuropsychologia 45, 836–843.CrossRefGoogle ScholarPubMed
Thomas, KM, Drevets, WC, Dahl, RE, Ryan, ND, Birmaher, B, Eccard, CH, Axelson, D, Whalen, PJ, Casey, BJ (2001). Amygdala response to fearful faces in anxious and depressed children. Archives of General Psychiatry 58, 1057–1063.CrossRefGoogle ScholarPubMed
Thomason, ME, Thompson, PM (2011). Diffusion imaging, white matter, and psychopathology. Annual Review of Clinical Psychology 7, 63–85.CrossRefGoogle ScholarPubMed
Vataja, R, Pohjasvaara, T, Leppavuori, A, Mantyla, R, Aronen, HJ, Salonen, O, Kaste, M, Erkinjuntti, T (2001). Magnetic resonance imaging correlates of depression after ischemic stroke. Archives of General Psychiatry 58, 925–931.CrossRefGoogle ScholarPubMed
Versace, A, Almeida, JR, Hassel, S, Walsh, ND, Novelli, M, Klein, CR, Kupfer, DJ, Phillips, ML (2008). Elevated left and reduced right orbitomedial prefrontal fractional anisotropy in adults with bipolar disorder revealed by tract-based spatial statistics. Archives of General Psychiatry 65, 1041–1052.CrossRefGoogle ScholarPubMed
Von Der Heide, RJ, Skipper, LM, Klobusicky, E, Olson, IR (2013). Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. Brain 136, 1692–1707.CrossRefGoogle ScholarPubMed
Wechsler, D (1991). Manual for the Wechsler Intelligence Scale for Children – Third Edition. Psychological Corporation: San Antonio, TX.Google Scholar
Wechsler, D (1997). WAIS-III Administration and Scoring Manual. The Psychological Corporation: San Antonio, TX.Google Scholar
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
Westlye, LT, Walhovd, KB, Bjornerud, A, Due-Tonnessen, P, Fjell, AM (2009). Error-related negativity is mediated by fractional anisotropy in the posterior cingulate gyrus – a study combining diffusion tensor imaging and electrophysiology in healthy adults. Cerebral Cortex 19, 293–304.CrossRefGoogle ScholarPubMed
Wichstrom, L (1999). The emergence of gender difference in depressed mood during adolescence: the role of intensified gender socialization. Developmental Psychology 35, 232–245.CrossRefGoogle ScholarPubMed
Yang, Q, Huang, X, Hong, N, Yu, X (2007). White matter microstructural abnormalities in late-life depression. International Psychogeriatrics 19, 757–766.CrossRefGoogle ScholarPubMed
Zahn-Waxler, C, Klimes-Dougan, B, Slattery, MJ (2000). Internalizing problems of childhood and adolescence: prospects, pitfalls, and progress in understanding the development of anxiety and depression. Development and Psychopathology 12, 443–466.CrossRefGoogle ScholarPubMed
Zhu, X, Wang, X, Xiao, J, Zhong, M, Liao, J, Yao, S (2011). Altered white matter integrity in first-episode, treatment-naive young adults with major depressive disorder: a tract-based spatial statistics study. Brain Research 1369, 223–229.CrossRefGoogle ScholarPubMed
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 study. Journal of Psychiatry and Neuroscience 33, 525–530.Google Scholar
Supplementary material: File

Aghajani et al. Supplementary Material

Method

Download Aghajani et al. Supplementary Material(File)
File 41.5 KB