Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-19T20:34:31.280Z Has data issue: false hasContentIssue false

Surface anatomical profile of the cerebral cortex in obsessive–compulsive disorder: a study of cortical thickness, folding and surface area

Published online by Cambridge University Press:  31 August 2012

Q. Fan
Affiliation:
Shanghai Mental Health Centre, Shanghai Jiao Tong University School of Medicine, Shanghai, China
L. Palaniyappan
Affiliation:
Division of Psychiatry, Institute of Mental Health, University of Nottingham, Nottingham, UK
L. Tan
Affiliation:
Radiology Department of Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
J. Wang
Affiliation:
Shanghai Mental Health Centre, Shanghai Jiao Tong University School of Medicine, Shanghai, China
X. Wang
Affiliation:
Shanghai Mental Health Centre, Shanghai Jiao Tong University School of Medicine, Shanghai, China
C. Li
Affiliation:
Shanghai Mental Health Centre, Shanghai Jiao Tong University School of Medicine, Shanghai, China
T. Zhang
Affiliation:
Shanghai Mental Health Centre, Shanghai Jiao Tong University School of Medicine, Shanghai, China
K. Jiang
Affiliation:
Shanghai Mental Health Centre, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Z. Xiao*
Affiliation:
Shanghai Mental Health Centre, Shanghai Jiao Tong University School of Medicine, Shanghai, China
P. F. Liddle
Affiliation:
Division of Psychiatry, Institute of Mental Health, University of Nottingham, Nottingham, UK
*
*Address for correspondence: Z. Xiao, M.D., Ph.D., Shanghai Mental Health Centre, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, China. (Email: xiaozeping@gmail.com)

Abstract

Background

Studying the distribution of anatomical abnormalities over the entire cortical surface can help to identify key neural circuits implicated in generating symptoms of neuropsychiatric disorders. There is a significant inconsistency among studies investigating the neuroanatomy of obsessive–compulsive disorder (OCD) because of the confounding influence of co-morbid depression and medication use and the lack of unbiased estimation of whole-brain morphometric changes. It is also unknown whether the distinct surface anatomical properties of thickness, surface area and gyrification, which collectively contribute to grey matter volume (GMV), are independently affected in OCD.

Method

The cortical maps of thickness, gyrification and surface areal change were acquired from 23 unmedicated OCD patients and 20 healthy controls using an unbiased whole-brain surface-based morphometric (SBM) method to detect regional changes in OCD. Subcortical structures were not assessed in this study.

Results

Patients showed a significant increase in the right inferior parietal cortical thickness. Significant increases in gyrification were also noted in the left insula, left middle frontal and left lateral occipital regions extending to the precuneus and right supramarginal gyrus in OCD. Areal contraction/expansion maps revealed no significant regional differences between the patients and controls. In patients, gyrification of the insula significantly predicted the symptom severity measured using Yale–Brown Obsessive–Compulsive Scale (YBOCS).

Conclusions

An alteration in the cortical surface anatomy is an important feature of OCD seen in unmedicated samples that relates to the severity of the illness. The results underscore the presence of a neurodevelopmental aberration underlying the pathophysiology of OCD.

Type
Original Articles
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

Berrios, GE (1989). Obsessive-compulsive disorder: its conceptual history in France during the 19th century. Comprehensive Psychiatry 30, 283295.CrossRefGoogle Scholar
Bora, E, Fornito, A, Pantelis, C, Yücel, M (2012). Gray matter abnormalities in major depressive disorder: a meta-analysis of voxel based morphometry studies. Journal of Affective Disorders 138, 918.CrossRefGoogle ScholarPubMed
Casanova, MF, Tillquist, CR (2008). Encephalization, emergent properties, and psychiatry: a minicolumnar perspective. The Neuroscientist 14, 101118.CrossRefGoogle ScholarPubMed
Cocchi, L, Harrison, BJ, Pujol, J, Harding, IH, Fornito, A, Pantelis, C, Yücel, M (2012). Functional alterations of large-scale brain networks related to cognitive control in obsessive-compulsive disorder. Human Brain Mapping 33, 10891106.CrossRefGoogle ScholarPubMed
Draganski, B, Gaser, C, Busch, V, Schuierer, G, Bogdahn, U, May, A (2004). Neuroplasticity: changes in grey matter induced by training. Nature 427, 311312.CrossRefGoogle ScholarPubMed
Driemeyer, J, Boyke, J, Gaser, C, Büchel, C, May, A (2008). Changes in gray matter induced by learning – revisited. PloS ONE 3, e2669.CrossRefGoogle ScholarPubMed
Du, M-Y, Wu, Q-Z, Yue, Q, Li, J, Liao, Y, Kuang, W-H, Huang, X-Q, Chan, RCK, Mechelli, A, Gong, Q-Y (2012). Voxelwise meta-analysis of gray matter reduction in major depressive disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 36, 1116.CrossRefGoogle ScholarPubMed
Dubois, J, Benders, M, Borradori-Tolsa, C, Cachia, A, Lazeyras, F, Ha-Vinh Leuchter, R, Sizonenko, SV, Warfield, SK, Mangin, JF, Huppi, PS (2008). Primary cortical folding in the human newborn: an early marker of later functional development. Brain 131, 20282041.CrossRefGoogle ScholarPubMed
Fallucca, E, MacMaster, FP, Haddad, J, Easter, P, Dick, R, May, G, Stanley, JA, Rix, C, Rosenberg, DR (2011). Distinguishing between major depressive disorder and obsessive-compulsive disorder in children by measuring regional cortical thickness. Archives of General Psychiatry 68, 527533.CrossRefGoogle ScholarPubMed
Fields, RD (2011). Imaging learning: the search for a memory trace. The Neuroscientist 17, 185196.CrossRefGoogle ScholarPubMed
Fischl, B, Dale, AM (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences USA 97, 1105011055.CrossRefGoogle ScholarPubMed
Fischl, B, Sereno, MI, Dale, AM (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195207.CrossRefGoogle Scholar
Fontenelle, LF, Harrison, BJ, Yücel, M, Pujol, J, Fujiwara, H, Pantelis, C (2009). Is there evidence of brain white-matter abnormalities in obsessive-compulsive disorder? A narrative review. Topics in Magnetic Resonance Imaging 20, 291298.CrossRefGoogle ScholarPubMed
Giedd, JN, Blumenthal, J, Jeffries, NO, Castellanos, FX, Liu, H, Zijdenbos, A, Paus, T, Evans, AC, Rapoport, JL (1999). Brain development during childhood and adolescence: a longitudinal MRI study. Nature Neuroscience 2, 861863.CrossRefGoogle ScholarPubMed
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 (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences USA 101, 81748179.CrossRefGoogle ScholarPubMed
Goldman-Rakic, PS (1980). Morphological consequences of prenatal injury to the primate brain. Progress in Brain Research 53, 119.Google Scholar
Hagler, DJ Jr., Saygin, AP, Sereno, MI (2006). Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. NeuroImage 33, 10931103.CrossRefGoogle ScholarPubMed
Haukvik, UK, Lawyer, G, Bjerkan, PS, Hartberg, CB, Jönsson, EG, McNeil, T, Agartz, I (2009). Cerebral cortical thickness and a history of obstetric complications in schizophrenia. Journal of Psychiatric Research 43, 12871293.CrossRefGoogle Scholar
Haukvik, UK, Schaer, M, Nesvåg, R, McNeil, T, Hartberg, CB, Jönsson, EG, Eliez, S, Agartz, I (2012). Cortical folding in Broca's area relates to obstetric complications in schizophrenia patients and healthy controls. Psychological Medicine 42, 13291337.CrossRefGoogle ScholarPubMed
Hilgetag, CC, Barbas, H (2006). Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Computational Biology 2, e22.CrossRefGoogle ScholarPubMed
Huyser, C, Veltman, DJ, de Haan, E, Boer, F (2009). Paediatric obsessive-compulsive disorder, a neurodevelopmental disorder? Evidence from neuroimaging. Neuroscience and Biobehavioral Reviews 33, 818830.CrossRefGoogle ScholarPubMed
Huyser, C, Veltman, DJ, Wolters, LH, de Haan, E, Boer, F (2011). Developmental aspects of error and high-conflict-related brain activity in pediatric obsessive-compulsive disorder: a fMRI study with a Flanker task before and after CBT. Journal of Child Psychology and Psychiatry, and Allied Disciplines 52, 12511260.CrossRefGoogle ScholarPubMed
Im, K, Lee, J-M, Lyttelton, O, Kim, SH, Evans, AC, Kim, SI (2008). Brain size and cortical structure in the adult human brain. Cerebral Cortex 18, 21812191.CrossRefGoogle ScholarPubMed
Jacob, S, Landeros-Weisenberger, A, Leckman, JF (2009). Autism spectrum and obsessive-compulsive disorders: OC behaviors, phenotypes and genetics. Autism Research 2, 293311.CrossRefGoogle ScholarPubMed
Joyner, AH, Roddey, JC, Bloss, CS, Bakken, TE, Rimol, LM, Melle, I, Agartz, I, Djurovic, S, Topol, EJ, Schork, NJ, Andreassen, OA, Dale, AM (2009). A common MECP2 haplotype associates with reduced cortical surface area in humans in two independent populations. Proceedings of the National Academy of Sciences USA 106, 1548315488.CrossRefGoogle ScholarPubMed
Karadag, F, Tumkaya, S, Kırtaş, D, Efe, M, Alacam, H, Oguzhanoglu, NK (2011). Neurological soft signs in obsessive compulsive disorder with good and poor insight. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35, 10741079.CrossRefGoogle ScholarPubMed
Kim, JJ, Youn, T, Lee, JM, Kim, IY, Kim, SI, Kwon, JS (2003). Morphometric abnormality of the insula in schizophrenia: a comparison with obsessive-compulsive disorder and normal control using MRI. Schizophrenia Research 60, 191198.CrossRefGoogle ScholarPubMed
la Fougère, C, Grant, S, Kostikov, A, Schirrmacher, R, Gravel, P, Schipper, HM, Reader, A, Evans, A, Thiel, A (2011). Where in-vivo imaging meets cytoarchitectonics: the relationship between cortical thickness and neuronal density measured with high-resolution [18F]flumazenil-PET. NeuroImage 56, 951960.CrossRefGoogle ScholarPubMed
Lázaro, L, Castro-Fornieles, J, Cullell, C, Andrés, S, Falcón, C, Calvo, R, Bargalló, N (2011). A voxel-based morphometric MRI study of stabilized obsessive-compulsive adolescent patients. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35, 18631869.CrossRefGoogle ScholarPubMed
Mangin, J-F, Jouvent, E, Cachia, A (2010). In-vivo measurement of cortical morphology: means and meanings. Current Opinion in Neurology 23, 359367.CrossRefGoogle ScholarPubMed
Mataix-Cols, D, Wooderson, S, Lawrence, N, Brammer, MJ, Speckens, A, Phillips, ML (2004). Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Archives of General Psychiatry 61, 564576.CrossRefGoogle ScholarPubMed
Mechelli, A, Price, CJ, Friston, KJ, Ashburner, J (2005). Voxel-based morphometry of the human brain: methods and applications. Current Medical Imaging Reviews 1, 105113.CrossRefGoogle Scholar
Menon, V, Uddin, LQ (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure and Function 214, 655667.CrossRefGoogle ScholarPubMed
Menzies, L, Achard, S, Chamberlain, SR, Fineberg, N, Chen, C-H, del Campo, N, Sahakian, BJ, Robbins, TW, Bullmore, E (2007). Neurocognitive endophenotypes of obsessive-compulsive disorder. Brain 130, 32233236.CrossRefGoogle ScholarPubMed
Menzies, L, Chamberlain, SR, Laird, AR, Thelen, SM, Sahakian, BJ, Bullmore, ET (2008 a). Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited. Neuroscience and Biobehavioral Reviews 32, 525549.CrossRefGoogle ScholarPubMed
Menzies, L, Williams, GB, Chamberlain, SR, Ooi, C, Fineberg, N, Suckling, J, Sahakian, BJ, Robbins, TW, Bullmore, ET (2008 b). White matter abnormalities in patients with obsessive-compulsive disorder and their first-degree relatives. American Journal of Psychiatry 165, 13081315.CrossRefGoogle ScholarPubMed
Nakamae, T, Narumoto, J, Sakai, Y, Nishida, S, Yamada, K, Kubota, M, Miyata, J, Fukui, K (2012). Reduced cortical thickness in non-medicated patients with obsessive-compulsive disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 37, 9095.CrossRefGoogle ScholarPubMed
Narayan, VM, Narr, KL, Phillips, OR, Thompson, PM, Toga, AW, Szeszko, PR (2008). Greater regional cortical gray matter thickness in obsessive-compulsive disorder. NeuroReport 19, 15511555.CrossRefGoogle ScholarPubMed
Palaniyappan, L, Liddle, PF (2011). Differential effects of surface area, gyrification and cortical thickness on voxel based morphometric deficits in schizophrenia. NeuroImage 60, 693699.CrossRefGoogle ScholarPubMed
Palaniyappan, L, Liddle, PF (2012 a). Aberrant cortical gyrification in schizophrenia: a surface-based morphometry study. Journal of Psychiatry and Neuroscience 37, 110119.CrossRefGoogle ScholarPubMed
Palaniyappan, L, Liddle, PF (2012 b). Does the salience network play a cardinal role in psychosis? An emerging hypothesis of insular dysfunction. Journal of Psychiatry and Neuroscience 37, 1727.CrossRefGoogle ScholarPubMed
Palaniyappan, L, Mallikarjun, P, Joseph, V, White, TP, Liddle, PF (2011 a). Folding of the prefrontal cortex in schizophrenia: regional differences in gyrification. Biological Psychiatry 69, 974979.CrossRefGoogle ScholarPubMed
Palaniyappan, L, Mallikarjun, P, Joseph, V, White, TP, Liddle, PF (2011 b). Regional contraction of brain surface area involves three large-scale networks in schizophrenia. Schizophrenia Research 129, 163168.CrossRefGoogle ScholarPubMed
Panizzon, MS, Fennema-Notestine, C, Eyler, LT, Jernigan, TL, Prom-Wormley, E, Neale, M, Jacobson, K, Lyons, MJ, Grant, MD, Franz, CE, Xian, H, Tsuang, M, Fischl, B, Seidman, L, Dale, A, Kremen, WS (2009). Distinct genetic influences on cortical surface area and cortical thickness. Cerebral Cortex 19, 27282735.CrossRefGoogle ScholarPubMed
Radua, J, van den Heuvel, OA, Surguladze, S, Mataix-Cols, D (2010). Meta-analytical comparison of voxel-based morphometry studies in obsessive-compulsive disorder vs other anxiety disorders. Archives of General Psychiatry 67, 701711.CrossRefGoogle ScholarPubMed
Radua, J, Mataix-Cols, D (2009). Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. British Journal of Psychiatry 195, 393402.CrossRefGoogle ScholarPubMed
Rakic, P (1988). Specification of cerebral cortical areas. Science 241, 170176.CrossRefGoogle ScholarPubMed
Raznahan, A, Shaw, P, Lalonde, F, Stockman, M, Wallace, GL, Greenstein, D, Clasen, L, Gogtay, N, Giedd, JN (2011). How does your cortex grow? Journal of Neuroscience 31, 71747177.CrossRefGoogle ScholarPubMed
Rotge, J-Y, Guehl, D, Dilharreguy, B, Tignol, J, Bioulac, B, Allard, M, Burbaud, P, Aouizerate, B (2009). Meta-analysis of brain volume changes in obsessive-compulsive disorder. Biological Psychiatry 65, 7583.CrossRefGoogle ScholarPubMed
Rotge, J-Y, Langbour, N, Guehl, D, Bioulac, B, Jaafari, N, Allard, M, Aouizerate, B, Burbaud, P (2010). Gray matter alterations in obsessive-compulsive disorder: an anatomic likelihood estimation meta-analysis. Neuropsychopharmacology 35, 686691.CrossRefGoogle ScholarPubMed
Roth, RM, Milovan, D, Baribeau, J, O'Connor, K (2005). Neuropsychological functioning in early- and late-onset obsessive-compulsive disorder. Journal of Neuropsychiatry and Clinical Neurosciences 17, 208213.CrossRefGoogle ScholarPubMed
Saxena, S, Brody, AL, Schwartz, JM, Baxter, LR (1998). Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder. British Journal of Psychiatry. Supplement 35, 2637.CrossRefGoogle Scholar
Schaer, M, Cuadra, MB, Tamarit, L, Lazeyras, F, Eliez, S, Thiran, J-P (2008). A surface-based approach to quantify local cortical gyrification. IEEE Transactions on Medical Imaging 27, 161170.CrossRefGoogle ScholarPubMed
Seeley, WW, Menon, V, Schatzberg, AF, Keller, J, Glover, GH, Kenna, H, Reiss, AL, Greicius, MD (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience 27, 23492356.CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, Dunbar, GC (1998). The Mini-International Neuropsychiatric Interview (MINI): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59, 2233.Google ScholarPubMed
Shim, G, Jung, WH, Choi, J-S, Jung, MH, Jang, JH, Park, J-Y, Choi, C-H, Kang, D-H, Kwon, JS (2009). Reduced cortical folding of the anterior cingulate cortex in obsessive-compulsive disorder. Journal of Psychiatry and Neuroscience 34, 443449.Google ScholarPubMed
Shin, Y-W, Yoo, SY, Lee, JK, Ha, TH, Lee, KJ, Lee, JM, Kim, IY, Kim, SI, Kwon, JS (2007). Cortical thinning in obsessive compulsive disorder. Human Brain Mapping 28, 11281135.CrossRefGoogle ScholarPubMed
Song, A, Jung, WH, Jang, JH, Kim, E, Shim, G, Park, HY, Choi, C-H, Kwon, JS (2011). Disproportionate alterations in the anterior and posterior insular cortices in obsessive-compulsive disorder. PloS ONE 6, e22361.CrossRefGoogle ScholarPubMed
Sridharan, D, Levitin, DJ, Menon, V (2008). A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proceedings of the National Academy of Sciences USA 105, 1256912574.CrossRefGoogle ScholarPubMed
Stern, ER, Fitzgerald, KD, Welsh, RC, Abelson, JL, Taylor, SF (2012 a). Resting-state functional connectivity between fronto-parietal and default mode networks in obsessive-compulsive disorder. PloS ONE 7, e36356.CrossRefGoogle ScholarPubMed
Stern, ER, Welsh, RC, Gonzalez, R, Fitzgerald, KD, Abelson, JL, Taylor, SF (2012 b). Subjective uncertainty and limbic hyperactivation in obsessive-compulsive disorder. Human Brain Mapping. Published online: 28 March 2012. doi:10.1002/hbm.22038.Google ScholarPubMed
Szeszko, PR, Ardekani, BA, Ashtari, M, Malhotra, AK, Robinson, DG, Bilder, RM, Lim, KO (2005). White matter abnormalities in obsessive-compulsive disorder: a diffusion tensor imaging study. Archives of General Psychiatry 62, 782790.CrossRefGoogle ScholarPubMed
Valente, Jr. AA, Miguel, EC, Castro, CC, Amaro, E Jr., Duran, FLS, Buchpiguel, CA, Chitnis, X, McGuire, PK, Busatto, GF (2005). Regional gray matter abnormalities in obsessive-compulsive disorder: a voxel-based morphometry study. Biological Psychiatry 58, 479487.CrossRefGoogle ScholarPubMed
van den Heuvel, OA, Remijnse, PL, Mataix-Cols, D, Vrenken, H, Groenewegen, HJ, Uylings, HB, van Balkom, AJ, Veltman, DJ (2009). The major symptom dimensions of obsessive-compulsive disorder are mediated by partially distinct neural systems. Brain 132, 853868.CrossRefGoogle ScholarPubMed
Winkler, AM, Kochunov, P, Blangero, J, Almasy, L, Zilles, K, Fox, PT, Duggirala, R, Glahn, DC (2010). Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. NeuroImage 53, 11351146.CrossRefGoogle ScholarPubMed
Wobrock, T, Gruber, O, McIntosh, AM, Kraft, S, Klinghardt, A, Scherk, H, Reith, W, Schneider-Axmann, T, Lawrie, SM, Falkai, P, Moorhead, TW (2010). Reduced prefrontal gyrification in obsessive-compulsive disorder. European Archives of Psychiatry and Clinical Neuroscience 260, 455464.CrossRefGoogle ScholarPubMed
Yoo, SY, Roh, MS, Choi, JS, Kang, DH, Ha, TH, Lee, JM, Kim, IY, Kim, SI, Kwon, JS (2008). Voxel-based morphometry study of gray matter abnormalities in obsessive-compulsive disorder. Journal of Korean Medical Science 23, 2430.CrossRefGoogle ScholarPubMed
Zarei, M, Mataix-Cols, D, Heyman, I, Hough, M, Doherty, J, Burge, L, Winmill, L, Nijhawan, S, Matthews, PM, James, A (2011). Changes in gray matter volume and white matter microstructure in adolescents with obsessive-compulsive disorder. Biological Psychiatry 70, 10831090.CrossRefGoogle ScholarPubMed
Zhang, T, Wang, J, Yang, Y, Wu, Q, Li, B, Chen, L, Yue, Q, Tang, H, Yan, C, Lui, S, Huang, X, Chan, RCK, Zang, Y, He, Y, Gong, Q (2011). Abnormal small-world architecture of top-down control networks in obsessive-compulsive disorder. Journal of Psychiatry and Neuroscience 36, 2331.CrossRefGoogle ScholarPubMed
Zilles, K, Armstrong, E, Schleicher, A, Kretschmann, H-J (1988). The human pattern of gyrification in the cerebral cortex. Anatomy and Embryology 179, 173179.CrossRefGoogle ScholarPubMed