Cortical thickness in youth with major depressive disorder

BMC Psychiatry

Frank P MacMaster²  Xiao-Ru Yang²  Lisa Marie Langevin²  Natalia Jaworska²  Normand Carrey¹  Stephanie Reynolds² 

[1] Department of Psychiatry, Dalhousie University, Halifax NS, Canada;Department of Pediatrics, University of Calgary, Behavioral Research Unit, Alberta Children’s Hospital, 2888 Shaganappi Trail NW, Calgary, AB T3B 6A8, Canada

关键词: Prefrontal cortex;    Magnetic resonance imaging;    Depression;    Cortical thickness;    Adolescence;   

Others  :  1123694
DOI  :  10.1186/1471-244X-14-83

 received in 2013-04-26, accepted in 2014-03-05,  发布年份 2014

【 摘 要 】

Background

Studies in adults with major depressive disorder (MDD) have implicated dysregulation of frontal-limbic circuits in the symptomology of this disorder. We hypothesized that the middle frontal gyrus (MFG; a core portion of the dorsolateral prefrontal cortex or DLPFC) and the anterior cingulate (caudal), regions implicated in emotive and cognitive control, would display a reduced cortical thickness in youth with MDD as compared to healthy, non-depressed adolescents.

Methods

Sixteen healthy control adolescents (17.19 ± 1.87 years; 7 males, 9 females) and thirty MDD participants (16.89 ± 2.01 years; 9 males, 21 females) underwent magnetic resonance imaging (MRI). Cortical thickness analysis was carried out using FreeSurfer software.

Results

Counter to our hypothesis, we observed thicker right and left rostral MFG in MDD adolescents as compared to controls (p = 0.004 and p = 0.005, respectively). Furthermore, the left caudal anterior cingulate cortex was thicker in MDD subjects as compared to controls (p = 0.009). In MDD subjects, there was a significant inverse correlation between age and left MFG thickness (r = -0.45, p = 0.001).

Conclusions

These results have implications for the developmental trajectory of the frontal lobe in adolescent MDD. The MFG is implicated in the frontal-limbic circuits underlying executive functioning and their interaction with affective processing. Alterations in this region are likely involved with the symptoms of MDD. Limitations include a small sample size and cross sectional design.

【 授权许可】

   
2014 Reynolds et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Nielen MM, Heslenfeld DJ, Heinen K, Van Strien JW, Witter MP, Jonker C, Veltman DJ: Distinct brain systems underlie the processing of valence and arousal of affective pictures. Brain Cogn 2009, 71(3):387-396.
• [2]Kusumakar V, MacMaster FP, Gates L, Sparkes SJ, Khan SC: Left medial temporal cytosolic choline in early onset depression. Can J Psychiatry 2001, 46(10):959-964.
• [3]Rosenberg DR, MacMaster FP, Mirza Y, Smith JM, Easter PC, Banerjee SP, Bhandari R, Boyd C, Lynch M, Rose M, Ivey J, Villafuerte RA, Moore GJ, Renshaw P: Reduced anterior cingulate glutamate in pediatric major depression: a magnetic resonance spectroscopy study. Biol Psychiatry 2005, 58(9):700-704.
• [4]MacMaster FP, Kusumakar V: Choline in pediatric depression. Mcgill J Med 2006, 9(1):24-27.
• [5]Chen HH, Rosenberg DR, MacMaster FP, Easter PC, Caetano SC, Nicoletti M, Hatch JP, Nery FG, Soares JC: Orbitofrontal cortex volumes in medication naive children with major depressive disorder: a magnetic resonance imaging study. J Child Adolesc Psychopharmacol 2008, 18(6):551-556.
• [6]MacMaster FP, Kusumakar V: Hippocampal volume in early onset depression. BMC Med 2004, 2:2. BioMed Central Full Text
• [7]MacMaster FP, Mirza Y, Szeszko PR, Kmiecik LE, Easter PC, Taormina SP, Lynch M, Rose M, Moore GJ, Rosenberg DR: Amygdala and hippocampal volumes in familial early onset major depressive disorder. Biol Psychiatry 2008, 63(4):385-390.
• [8]MacMaster FP, Moore GJ, Russell A, Mirza Y, Taormina SP, Buhagiar C, Rosenberg DR: Medial temporal N-acetyl-aspartate in pediatric major depression. Psychiatry Res 2008, 164(1):86-89.
• [9]Hulvershorn LA, Cullen K, Anand A: Toward dysfunctional connectivity: a review of neuroimaging findings in pediatric major depressive disorder. Brain Imaging Behav 2011, 5(4):307-328.
• [10]Pizzagalli DA: Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology 2011, 36(1):183-206.
• [11]Kumar A, Thomas A, Lavretsky H, Yue K, Huda A, Curran J, Venkatraman T, Estanol L, Mintz J, Mega M, Toga A: Frontal white matter biochemical abnormalities in late-life major depression detected with proton magnetic resonance spectroscopy. Am J Psychiatry 2002, 159(4):630-636.
• [12]Binesh N, Kumar A, Hwang S, Mintz J, Thomas MA: Neurochemistry of late-life major depression: a pilot two-dimensional MR spectroscopic study. J Magn Reson Imaging 2004, 20(6):1039-1045.
• [13]Farchione TR, Moore GJ, Rosenberg DR: Proton magnetic resonance spectroscopic imaging in pediatric major depression. Biol Psychiatry 2002, 52(2):86-92.
• [14]Mayberg HS, Liotti M, Brannan SK, McGinnis S, Mahurin RK, Jerabek PA, Silva JA, Tekell JL, Martin CC, Lancaster JL, Fox PT: Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 1999, 156(5):675-682.
• [15]Grimm S, Beck J, Schuepbach D, Hell D, Boesiger P, Bermpohl F, Niehaus L, Boeker H, Northoff G: Imbalance between left and right dorsolateral prefrontal cortex in major depression is linked to negative emotional judgment: an fMRI study in severe major depressive disorder. Biol Psychiatry 2008, 63(4):369-376.
• [16]Fallucca E, MacMaster FP, Haddad J, Easter P, Dick R, May G, Stanley JA, Rix C, Rosenberg DR: Distinguishing between major depressive disorder and obsessive-compulsive disorder in children by measuring regional cortical thickness. Arch Gen Psychiatry 2011, 68(5):527-533.
• [17]Abe O, Yamasue H, Kasai K, Yamada H, Aoki S, Inoue H, Takei K, Suga M, Matsuo K, Kato T, Masutani Y, Ohtomo K: Voxel-based analyses of gray/white matter volume and diffusion tensor data in major depression. Psychiatry Res 2010, 181(1):64-70.
• [18]Li CT, Lin CP, Chou KH, Chen IY, Hsieh JC, Wu CL, Lin WC, Su TP: Structural and cognitive deficits in remitting and non-remitting recurrent depression: a voxel-based morphometric study. Neuroimage 2010, 50(1):347-356.
• [19]Chang CC, Yu SC, McQuoid DR, Messer DF, Taylor WD, Singh K, Boyd BD, Krishnan KR, MacFall JR, Steffens DC, Payne ME: Reduction of dorsolateral prefrontal cortex gray matter in late-life depression. Psychiatry Res 2011, 193(1):1-6.
• [20]Khundakar A, Morris C, Oakley A, McMeekin W, Thomas AJ: Morphometric analysis of neuronal and glial cell pathology in the dorsolateral prefrontal cortex in late-life depression. Br J Psychiatry 2009, 195(2):163-169.
• [21]Peterson BS, Warner V, Bansal R, Zhu H, Hao X, Liu J, Durkin K, Adams PB, Wickramaratne P, Weissman MM: Cortical thinning in persons at increased familial risk for major depression. Proc Natl Acad Sci USA 2009, 106(15):6273-6278.
• [22]van Eijndhoven P: Changes in paralimbic cortical thickness in first episode depression. Biol Psychiatry 2012., 71(8) Supplement: 67th Annual Scientific Convention and Meeting, Late Breaking Abstracts
• [23]Giedd JN: Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci 2004, 1021:77-85.
• [24]MacMaster FP, Keshavan M, Mirza Y, Carrey N, Upadhyaya AR, El-Sheikh R, Buhagiar CJ, Taormina SP, Boyd C, Lynch M, Rose M, Ivey J, Moore GJ, Rosenberg DR: Development and sexual dimorphism of the pituitary gland. Life Sci 2007, 80(10):940-944.
• [25]Crews F, He J, Hodge C: Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 2007, 86(2):189-199.
• [26]Juraska JM, Markham JA: The cellular basis for volume changes in the rat cortex during puberty: white and gray matter. Ann N Y Acad Sci 2004, 1021:431-435.
• [27]Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF 3rd, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM: Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 2004, 101(21):8174-8179.
• [28]Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL: Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 1999, 2(10):861-863.
• [29]Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW: In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 1999, 2(10):859-861.
• [30]Makris N, Biederman J, Valera EM, Bush G, Kaiser J, Kennedy DN, Caviness VS, Faraone SV, Seidman LJ: Cortical thinning of the attention and executive function networks in adults with attention-deficit/hyperactivity disorder. Cereb Cortex 2007, 17(6):1364-1375.
• [31]Shaw P, Greenstein D, Lerch J, Clasen L, Lenroot R, Gogtay N, Evans A, Rapoport J, Giedd J: Intellectual ability and cortical development in children and adolescents. Nature 2006, 440(7084):676-679.
• [32]Lerch JP, Pruessner JC, Zijdenbos A, Hampel H, Teipel SJ, Evans AC: Focal decline of cortical thickness in Alzheimer’s disease identified by computational neuroanatomy. Cereb Cortex 2005, 15(7):995-1001.
• [33]Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N: Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 1997, 36(7):980-988.
• [34]Poznanski EO, Cook SC, Carroll BJ, Corzo H: Use of the children’s depression rating scale in an inpatient psychiatric population. J Clin Psychiatry 1983, 44(6):200-203.
• [35]Poznanski EO, Cook SC, Carroll BJ: A depression rating scale for children. Pediatrics 1979, 64(4):442-450.
• [36]Dale AM, Fischl B, Sereno MI: Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999, 9(2):179-194.
• [37]Fischl B, Dale AM: Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 2000, 97(20):11050-11055.
• [38]Fischl B, Sereno MI, Dale AM: Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 1999, 9(2):195-207.
• [39]Rothman KJ: No adjustments are needed for multiple comparisons. Epidemiology 1990, 1(1):43-46.
• [40]van Eijndhoven P, van Wingen G, Katzenbauer M, Groen W, Tepest R, Fernandez G, Buitelaar J, Tendolkar I: Paralimbic cortical thickness in first-episode depression: evidence for trait-related differences in mood regulation. Am J Psychiatry 2013, 170(12):1477-1486.
• [41]Rajkowska G, Goldman-Rakic PS: Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach coordinate system. Cereb Cortex 1995, 5(4):323-337.
• [42]Fuster JM: The Prefrontal Cortex. 4th edition. London: Academic Press; 2008.
• [43]Byrum CE, Ahearn EP, Krishnan KR: A neuroanatomic model for depression. Prog Neuropsychopharmacol Biol Psychiatry 1999, 23(2):175-193.
• [44]Kikinis Z, Fallon JH, Niznikiewicz M, Nestor P, Davidson C, Bobrow L, Pelavin PE, Fischl B, Yendiki A, McCarley RW, Kikinis R, Kubicki M, Shenton ME: Gray matter volume reduction in rostral middle frontal gyrus in patients with chronic schizophrenia. Schizophr Res 2010, 123(2–3):153-159.
• [45]Fossati P, Coyette F, Ergis AM, Allilaire JF: Influence of age and executive functioning on verbal memory of inpatients with depression. J Affect Disord 2002, 68(2–3):261-271.
• [46]Rose EJ, Ebmeier KP: Pattern of impaired working memory during major depression. J Affect Disord 2006, 90(2–3):149-161.
• [47]Matthews K, Coghill D, Rhodes S: Neuropsychological functioning in depressed adolescent girls. J Affect Disord 2008, 111(1):113-118.
• [48]Caetano SC, Fonseca M, Olvera RL, Nicoletti M, Hatch JP, Stanley JA, Hunter K, Lafer B, Pliszka SR, Soares JC: Proton spectroscopy study of the left dorsolateral prefrontal cortex in pediatric depressed patients. Neurosci Lett 2005, 384(3):321-326.
• [49]Cotter D, Mackay D, Frangou S, Hudson L, Landau S: Cell density and cortical thickness in Heschl’s gyrus in schizophrenia, major depression and bipolar disorder. Br J Psychiatry 2004, 185:258-259.
• [50]Rajkowska G, Miguel-Hidalgo JJ, Wei J, Dilley G, Pittman SD, Meltzer HY, Overholser JC, Roth BL, Stockmeier CA: Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 1999, 45(9):1085-1098.
• [51]Truong W, Minuzzi L, Soares CN, Frey BN, Evans AC, Macqueen GM, Hall GB: Changes in cortical thickness across the lifespan in major depressive disorder. Psychiatry Res 2013, 214(3):204-211.
• [52]Botvinick M, Nystrom LE, Fissell K, Carter CS, Cohen JD: Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 1999, 402(6758):179-181.
• [53]Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR: Human cingulate cortex: surface features, flat maps, and cytoarchitecture. J Comp Neurol 1995, 359(3):490-506.
• [54]Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD: Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 1998, 280(5364):747-749.
• [55]Smoski MJ, Felder J, Bizzell J, Green SR, Ernst M, Lynch TR, Dichter GS: fMRI of alterations in reward selection, anticipation, and feedback in major depressive disorder. J Affect Disord 2009, 118(1–3):69-78.
• [56]Knutson B, Bhanji JP, Cooney RE, Atlas LY, Gotlib IH: Neural responses to monetary incentives in major depression. Biol Psychiatry 2008, 63(7):686-692.
• [57]Huttenlocher PR: Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res 1979, 163(2):195-205.
• [58]Jernigan TL, Tallal P: Late childhood changes in brain morphology observable with MRI. Dev Med Child Neurol 1990, 32(5):379-385.
• [59]Thompson JR, Engelhart J, Hasso AN, Hinshaw DB Jr: Normal frontal lobe gray matter-white matter CT volume ratio in children. Neuroradiology 1985, 27(2):108-111.