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Decreased gyrification in major depressive disorderYuanchao Zhanga,b, Chunshui Yuc, Yuan Zhoub,d, Kuncheng Lic, Chong Lia,band Tianzi Jiangb Structural and functional abnormalities have been extensively reported in major depressive disorder, but possible changes in Keywords: complexity, connectivity, cortical folding, local gyrification index, cortical folding have not yet been explored in this disorder.
magnetic resonance imaging, major depressive disorder This study investigated this issue in major depressive disorder using the local gyrification index. High-resolution magnetic aDepartment of Mathematics, Zhejiang University, Hangzhou, bNational resonance imaging was performed in 18 patients with first- Laboratory of Pattern Recognition, Institute of Automation, Chinese Academyof Sciences, cDepartment of Radiology, Xuanwu Hospital of Capital Medical episode major depressive disorder and 18 age-matched and University and dCenter for Social and Economic Behavior, Institute of Psychology, sex-matched healthy individuals. The local gyrification index Chinese Academy of Sciences, Beijing, PR China was applied to detect brain areas with abnormal corticalfolding in major depressive disorder. Compared with healthy Correspondence to Professor Tianzi Jiang, PhD, National Laboratory of Pattern participants, patients with major depressive disorder showed Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing100190, PR China significantly decreased local gyrification index in the bilateral Tel: + 86 10 8261 4469; fax: + 86 10 62551993; e-mail: [email protected] mid-posterior cingulate, insula, and orbital frontal cortices, theleft anterior cingulate cortex, and the right temporal Yuanchao Zhang, Chunshui Yu, and Yuan Zhou contributed equally to this study Kluwer Health | Lippincott Williams & Wilkins.
Received 28 November 2008 accepted 30 November 2008 Major depressive disorder (MDD) is a common psychiatric Eighteen medication-naive patients with first major overwhelming feelings of sadness, guilt, and worthlessness.
depressive episode (four men and 14 women) were It is believed that depression is related to the disturbance recruited from the outpatient clinic at Xuanwu Hospital in connectivities between multiple brain regions [1].
and met the following criteria: (i) Diagnostic and Statistical This opinion is supported by abnormalities in both Manual of Mental Disorders 4th edition criteria for a major cortico–cortical connectivity revealed by disrupted white depressive episode, single episode, currently depressed, according to the structured clinical interview for revealed by gial cell pathology in MDD [3–5]. Cortical Diagnostic and Statistical Manual of mental disorders folding, which can be investigated by gyrification fourth edition; (ii) never exposure to any psychotropic measures, is thought to reflect not only cortico–cortical medication before the assessment began; (iii) age 18–60 connectivity [6] but also optimal intracortical organiza- years; (iv) no history of substance abuse or dependence, tion, with the most axonal connections in the least no family history of major psychiatric or neurological possible volume [7]. Therefore, investigating the pattern illness in first-degree relatives, not currently taking any of cortical folding in MDD patients may contribute in prescription or centrally acting medications, no serious understanding the pathogenesis of the disorder.
medical or neurological illness; and (v) satisfying thecriteria to undergo a magnetic resonance imaging (MRI) The gyrification index (GI) proposed by Zilles et al. [8] is scan based on a MRI screening questionnaire. The a quantitative measure of gyrification, but this method is patients were excluded for any axis I disorder (other rater dependent and cannot localize the exact regions than MDD) that preceded the onset of MDD. Additional with abnormal cortical folding. The local gyrification exclusion criteria were as follows: acutely suicidal or index (lGI), a three -dimensional extension of GI, is homicidal or requiring inpatient treatment, history of a newly developed, automated method for locating trauma resulting in loss of consciousness, current regionally specific changes in gyrification, and has been pregnancy, or breastfeeding. At the time of scanning, successfully used to assess gyrification of the 22q11 the depressive symptoms of the patients were rated using Deletion syndrome [9]. In this study, we use this measure to explore gyrification abnormalities in MDD.
(17.8 ± 3.6). Eighteen demographically matched healthy c 2009 Wolters Kluwer Health | Lippincott Williams & Wilkins participants (four men and 14 women) were recruited by advertisements and met the same inclusion criteria (iii–v)and the exclusion criteria as the patients. All participantstook part in this study after signing an informedconsent form approved by the Medical Research Ethics Committee of Xuanwu Hospital. The mean duration ofcurrent depressive episode of MDD patients was 6.7 ± 3.9 months. All patients were on no antidepressantmedications at the time of scanning. The two groups were statistically comparable in age (39.8 ± 9.3 years forMDD; P=0.8173) and sex composition (P=1).
Three-dimensional structural MRI scans were obtained on a3.0 Tesla magnetic resonance scanner (Trio system; Siemens Brain regions of significantly decreased local gyrification index in Magnetom scanner, Erlangen, Germany) with magnetization patients with major depressive disorder compared with well-matched prepared rapid acquisition gradient echo (MP-RAGE).
healthy participants after a correction for multiple comparisons(P < 0.05, the cluster-based random field theory correction). The color Detailed scan parameters were as follows: repetition bar indicates the cluster-wise P value after the correction for multiple time = 2000 ms, echo time = 2.6 ms, slice thickness = 1 mm, no gaps, flip angle = 91, matrix = 256 Â 224, field ofview = 256 Â 224 mm2, 1 Â 1 mm2 in-plane resolution.
clusters was set at P value of less than 0.05 after multiple Each scan was processed using FreeSurfer [10,11] (http:// surfer.nmr.mgh.harvard.edu/) to obtain the complexitymeasure (lGI). In brief, a cortical map of lGIs can be obtained in four steps [9]. First, the pial cortical surface is Only decreased lGI was found in MDD patients reconstructed in three-dimensional space. Second, an compared with healthy participants. We found nine outer surface can be obtained from the outer hull that clusters of difference with thresholds of P=0.001 tightly warps the pial surface. Third, the lGI is computed (uncorrected) and cluster size Z 50 points. These for each of the vertices of the outer surface. Fourth, clusters included the bilateral mid-posterior cingulate, a cortical map of lGIs is obtained by propagating the insula, and orbital frontal cortices, the left anterior lGI values from the outer surface mesh to the pial cingulate cortex, and the right temporal operculum. After performing multiple comparison correction using randomfield theory , we identified five significant clusters, which To compare the lGIs point by point, the establishment included the left insular/frontal operculum (cluster of point correspondence across participants in a standard size=2184 points, corrected P value=0.0039), the left surface-based coordinate system was required. Surface- medial orbital frontal cortex (cluster size=1907 points, based registration [12] was used to build an average corrected P value=0.0021), the left mid-posterior template and all of the individual reconstructed cortical cingulate cortex (cluster size=1041 points, corrected surfaces were aligned to the template. A heat kernel of P value=0.0428), the right insula/temporal operculum 10 mm width was used to smooth the lGI maps. Before (cluster size=1471 points, corrected P value=0.0113), the statistical analysis, a linear regression was performed and the right inferior frontal gyrus (cluster size=303 to remove the effects of age and sex. The residuals of the points, corrected P value=0.0444) (Fig. 1).
regression were used for statistical analysis.
In this study, we used a surface-based approach to Statistical analysis was performed at every point across all quantify the local cortical gyrification in well-matched participants in Montreal Neurological Institute space.
samples of MDD patients versus healthy participants.
Two-sample t-tests were used to test statistically We revealed decreased gyrification in MDD patients significant differences in lGIs at homologous vertices.
compared with healthy participants in certain mood- The threshold P=0.001 was used to define clusters, and only clusters with a minimum of 50 points were reported.
Then corrected cluster-wise P value was obtained using There are several possible explanations for the decreased random field theory [13]. The level of significance for Decreased gyrification in MDD Zhang et al.
A mechanical model of brain convolutional development has been used to explain abnormalities in cortical folding In conclusion, we found decreased gyrification in several during human brain development [14]. This model mood-related regions in patients with MDD compared proposes that differential growth rates of cortical layers with healthy participants. To our knowledge, this is the directly affect the degree of cortical convolutions. In fact, first study to explore the cortical folding pattern in MDD.
several previous studies have found decreased glial Further studies are needed to clarify the exact mechanism density, neuronal density, and neuronal size in several of the abnormal cortical folding in MDD.
mood-related regions such as the anterior cingulatedcortex [4] and the orbitofrontal cortex [3,5] in MDD.
Therefore, the decreased gyrification in the mood-relatedregions might be caused by disorganization of the cortical The authors thank Marie Schaer, Lei Lin, Kun Wang for architectures in these regions. Another tension-based their useful suggestions and Jiefeng Jiang, Yongfu Hao, model of cortical morphogenesis proposes that tension Professor Keith J. Worsley for their help on the artwork.
along the axons in white matter is the primary driving The authors also thank Dr Edmund F. and Dr Rhoda E.
force for cortical folding [6]. In MDD, previous diffusion Perozzi for checking the English. This work was supported by tensor imaging studies have revealed that depressive the Natural Science Foundation of China, grant no.
patients had a significantly lower fractional anisotropy 30425004, 30670601, 30870694, and 30730035, and the in the prefrontal white matter [2]. In addition, in National Key Basic Research and Development Program previous diffusion tensor imaging studies, white matter abnormalities of the anterior cingulated cortex, theprefrontal lobe, the insula, and the posterior cingulate regions have been reported in patients with geriatric Mayberg HS. Modulating dysfunctional limbic-cortical circuits in depression: depression [15–17]. According to the tension-based theory towards development of brain-based algorithms for diagnosis and optimisedtreatment. Br Med Bull 2003; 65:193–207.
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