Psychiatry Research: Neuroimaging
Volume 162, Issue 2 , Pages 123-132 , 28 February 2008

Anatomical abnormalities of the anterior cingulate and paracingulate cortex in patients with bipolar I disorder

  • Alex Fornito

      Affiliations

    • Melbourne Neuropsychiatry Centre, The University of Melbourne, Melbourne, Australia
    • Department of Psychology, The University of Melbourne, Melbourne, Australia
    • Corresponding Author InformationCorresponding author. Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne, Levels 2 and 3, National Neuroscience Facility, Alan Gilbert Building, 161 Barry St., Carlton South, Vic 3053, Australia. Tel.: +61 3 8344 1800; fax: +61 3 9348 0469.
  • ,
  • Gin S. Malhi

      Affiliations

    • Department of Psychological Medicine, Northern Clinical School, The University of Sydney, Sydney, Australia
    • CADE clinic, Department of Psychiatry, Royal North Shore Hospital, Sydney, Australia
  • ,
  • Jim Lagopoulos

      Affiliations

    • Department of Psychological Medicine, Northern Clinical School, The University of Sydney, Sydney, Australia
    • CADE clinic, Department of Psychiatry, Royal North Shore Hospital, Sydney, Australia
  • ,
  • Belinda Ivanovski

      Affiliations

    • Department of Psychological Medicine, Northern Clinical School, The University of Sydney, Sydney, Australia
    • CADE clinic, Department of Psychiatry, Royal North Shore Hospital, Sydney, Australia
  • ,
  • Stephen J. Wood

      Affiliations

    • Melbourne Neuropsychiatry Centre, The University of Melbourne, Melbourne, Australia
  • ,
  • Michael M. Saling

      Affiliations

    • Department of Psychology, The University of Melbourne, Melbourne, Australia
  • ,
  • Christos Pantelis

      Affiliations

    • Melbourne Neuropsychiatry Centre, The University of Melbourne, Melbourne, Australia
    • Howard Florey Institute, The University of Melbourne, Melbourne, Australia
  • ,
  • Murat Yücel

      Affiliations

    • Melbourne Neuropsychiatry Centre, The University of Melbourne, Melbourne, Australia
    • ORYGEN Research Centre, The University of Melbourne, Melbourne, Australia

Received 20 October 2006 ,Revised 17 April 2007 ,Accepted 4 June 2007.

References 

  1. Adler CM, Levine AD, DelBello MP, Strakowski SM. Changes in gray matter volume in patients with bipolar disorder. Biological Psychiatry. 2005;58:151–157
  2. Amodio DM, Frith CD. Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience. 2006;7:268–277
  3. Atmaca M, Ozdemir H, Cetinkaya S, Parmaksiz S, Belli H, Poyraz AK, et al. Cingulate gyrus volumetry in drug free bipolar patients and patients treated with valproate or valproate and quetiapine. Journal of Psychiatric Research. 2007;41:821–827
  4. Behrens JT. Principles and procedures of exploratory data analysis. Psychological Methods. 1997;2:131–160
  5. Benes FM. Relationship of cingulate cortex to schizophrenia and other psychiatric disorders. In:  Vogt BA,  Gabriel M editor. Neurobiology of Cingulate Cortex and Limbic Thalamus: A Comprehensive Handbook. Boston: Birkhäuser; 1993;
  6. Benes FM, Vincent SL, Todtenkopf M. The density of pyramidal and nonpyramidal neurons in anterior cingulate cortex of schizophrenic and bipolar subjects. Biological Psychiatry. 2001;50:395–406
  7. Bookstein FL. “Voxel-based morphometry” should not be used with imperfectly registered images. NeuroImage. 2001;14:1454–1462
  8. Bora E, Vahip S, Gonul AS, Akdeniz F, Alkan M, Ogut M, et al. Evidence for theory of mind deficits in euthymic patients with bipolar disorder. Acta Psychiatrica Scandinavica. 2005;112:110–116
  9. Bouras C, Kovari E, Hof PR, Riederer BM, Giannakopoulos P. Anterior cingulate cortex pathology in schizophrenia and bipolar disorder. Acta Neuropathologica (Berlin). 2001;102:373–379
  10. Brambilla P, Nicoletti MA, Harenski K, Sassi RB, Mallinger AG, Frank E, et al. Anatomical MRI study of subgenual prefrontal cortex in bipolar and unipolar subjects. Neuropsychopharmacology. 2002;27:792–799
  11. Bruno SD, Barker GJ, Cercignani M, Symms M, Ron MA. A study of bipolar disorder using magnetization transfer imaging and voxel-based morphometry. Brain. 2004;127:2433–2440
  12. Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences. 2000;4:215–222
  13. Bush G, Vogt BA, Holmes J, Dale AM, Greve D, Jenike MA, et al. Dorsal anterior cingulate cortex: a role in reward-based decision making. Proceedings of the National Academy of Sciences of the United States of America. 2002;99:523–528
  14. Chana G, Landau S, Beasley C, Everall IP, Cotter D. Two-dimensional assessment of cytoarchitecture in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia: evidence for decreased neuronal somal size and increased neuronal density. Biological Psychiatry. 2003;53:1086–1098
  15. Cohen J. A power primer. Psychological Bulletin. 1992;112:155–159
  16. Cohen JD, Botvinick M, Carter CS. Anterior cingulate and prefrontal cortex: who's in control?. Nature Neuroscience. 2000;3:421–423
  17. Cotter D, Mackay D, Landau S, Kerwin R, Everall I. Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Archives of General Psychiatry. 2001;58:545–553
  18. Crum WR, Griffin LD, Hill DLG, Hawkes DJ. Zen and the art of medical image registration: correspondence, homology, and quantity. NeuroImage. 2003;20:1425–1437
  19. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis I. Segmentation and surface reconstruction. NeuroImage. 1999;9:179–194
  20. Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain. 1995;118:279–306
  21. Dickstein DP, Milham MP, Nugent AC, Drevets WC, Charney DS, Pine DS, et al. Frontotemporal alterations in pediatric bipolar disorder: results of a voxel-based morphometry study. Archives of General Psychiatry. 2005;62:734–741
  22. Drevets WC, Price JL, Simpson JR, Todd RD, Reich T, Vannier M, et al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature. 1997;386:824–827
  23. Drevets, W.C., Ongur, D., Price, J.L., 1998. Neuroimaging abnormalities in the subgenual prefrontal cortex: implications for the pathophysiology of familial mood disorders. Molecular Psychiatry 3, 220–226, 190–221.
  24. Eastwood SL, Harrison PJ. Synaptic pathology in the anterior cingulate cortex in schizophrenia and mood disorders. A review and a Western blot study of synaptophysin, GAP-43 and the complexins. Brain Research Bulletin. 2001;55:569–578
  25. Eritaia J, Wood SJ, Stuart GW, Bridle N, Dudgeon P, Maruff P, et al. An optimized method for estimating intracranial volume from magnetic resonance images. Magnetic Resonance in Medicine. 2000;44:973–977
  26. Farrow TF, Whitford TJ, Williams LM, Gomes L, Harris AW. Diagnosis-related regional gray matter loss over two years in first episode schizophrenia and bipolar disorder. Biological Psychiatry. 2005;58:713–723
  27. First MB, Spitzer RL, Gibbon M, Williams JB. Structured Clinical Interview for DSM-IV. Washington, DC: American Psychiatric Press; 1998;
  28. Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America. 2000;97:11050–11055
  29. Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis II: inflation, flattening, and a surface-based coordinate system. NeuroImage. 1999;9:195–207
  30. Fischl B, Sereno MI, Tootell RBH, Dale AM. High-resolution intersubject averaging and a coordinate system for the cortical surface. Human Brain Mapping. 1999;8:272–284
  31. Fischl B, Liu A, Dale AM. Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Transactions on Medical Imaging. 2001;20:70–80
  32. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33:341–355
  33. Fjell AM, Walhovd KB, Reinvang I, Lundervold A, Salat D, Quinn BT, et al. Selective increase of cortical thickness in high-performing elderly—structural indices of optimal cognitive aging. NeuroImage. 2006;29:984–994
  34. Fornito A, Whittle S, Wood SJ, Velakoulis D, Pantelis C, Yucel M. The influence of sulcal variability on morphometry of the human anterior cingulate and paracingulate cortex. NeuroImage. 2006;33:843–854
  35. Fornito, A., Wood, S.J., Whittle, S., Fuller, J., Adamson, C., Saling, M.M., Velakoulis, D., Pantelis, C., Yücel, M., in press-a. Variability of the paracingulate sulcus and morphometry of the medial frontal cortex: associations with cortical thickness, surface area, volume, and sulcal depth. Human Brain Mapping (Epub ahead of print).
  36. Fornito, A., Yücel, M., Wood, S.J., Adamson, C., Velakoulis, D., Saling, M.M., McGorry, P.D., Pantelis, C., in press-b. Surface-based morphometry of the anterior cingulate cortex in first episode schizophrenia. Human Brain Mapping (Epub ahead of print).
  37. Free SL, Bergin PS, Fish DR, Cook MJ, Shorvon SD, Stevens JM. Methods for normalization of hippocampal volumes measured with MR. AJNR American Journal of Neuroradiology. 1995;16:637–643
  38. Harrison PJ. The neuropathology of primary mood disorder. Brain. 2002;125:1428–1449
  39. Hirayasu Y, Shenton ME, Salisbury DF, Kwon JS, Wible CG, Fischer IA, et al. Subgenual cingulate cortex volume in first-episode psychosis. American Journal of Psychiatry. 1999;156:1091–1093
  40. Holmes CJ, Hoge R, Collins L, Woods R, Toga AW, Evans AC. Enhancement of MR images using registration for signal averaging. Journal of Computer Assisted Tomography. 1998;22:324–333
  41. Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Medical Image Analysis. 2001;5:143–156
  42. Kaur S, Sassi RB, Axelson D, Nicoletti M, Brambilla P, Monkul ES, et al. Cingulate cortex anatomical abnormalities in children and adolescents with bipolar disorder. American Journal of Psychiatry. 2005;162:1637–1643
  43. Kerr N, Dunbar RI, Bentall RP. Theory of mind deficits in bipolar affective disorder. Journal of Affective Disorders. 2003;73:253–259
  44. Kolbe S, Ma T, Liu W, Soh WS, Buyya R, Egan GF. A platform for distributed analysis of neuroimaging data on global grids. In: Proceedings of the 1st IEEE International Conference on e-Science and Grid Computing. Melbourne, Australia: IEEE CS Press; 2005;
  45. Kubicki M, Shenton ME, Salisbury DF, Hirayasu Y, Kasai K, Kikinis R, et al. Voxel-based morphometric analysis of gray matter in first episode schizophrenia. NeuroImage. 2002;17:1711–1719
  46. Lochhead RA, Parsey RV, Oquendo MA, Mann JJ. Regional brain gray matter volume differences in patients with bipolar disorder as assessed by optimized voxel-based morphometry. Biological Psychiatry. 2004;55:1154–1162
  47. Lyoo IK, Kim MJ, Stoll AL, Demopulos CM, Parow AM, Dager SR, et al. Frontal lobe gray matter density decreases in bipolar I disorder. Biological Psychiatry. 2004;55:648–651
  48. Lyoo IK, Sung YH, Dager SR, Friedman SD, Lee JY, Kim SJ, et al. Regional cerebral cortical thinning in bipolar disorder. Bipolar Disorders. 2006;8:65–74
  49. Mayberg HS, Liotti M, Brannan SK, McGinnis S, Mahurin RK, Jerabek PA, et al. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. American Journal of Psychiatry. 1999;156:675–682
  50. McDonald C, Bullmore ET, Sham PC, Chitnis X, Wickham H, Bramon E, et al. Association of genetic risks for schizophrenia and bipolar disorder with specific and generic brain structural endophenotypes. Archives of General Psychiatry. 2004;61:974–984
  51. McIntosh AM, Job DE, Moorhead TW, Harrison LK, Forrester K, Lawrie SM, et al. Voxel-based morphometry of patients with schizophrenia or bipolar disorder and their unaffected relatives. Biological Psychiatry. 2004;56:544–552
  52. Murphy FC, Rubinsztein JS, Michael A, Rogers RD, Robbins TW, Paykel ES, et al. Decision-making cognition in mania and depression. Psychological Medicine. 2001;31:679–693
  53. Nugent AC, Milham MP, Bain EE, Mah L, Cannon DM, Marrett S, et al. Cortical abnormalities in bipolar disorder investigated with MRI and voxel-based morphometry. NeuroImage. 2006;30:485–497
  54. Olley AL, Malhi GS, Bachelor J, Cahill CM, Mitchell PB, Berk M. Executive functioning and theory of mind in euthymic bipolar disorder. Bipolar Disorders. 2005;7(Suppl 5):43–52
  55. Ongur D, Drevets WC, Price JL. Glial reduction in the subgenual prefrontal cortex in mood disorders. Proceedings of the National Academy of Sciences of the United States of America. 1998;95:13290–13295
  56. Ono M, Kubik S, Abernathy CD. Atlas of the Cerebral Sulci. New York: Thieme; 1990;
  57. Paus T, Otkay N, Caramanos Z, MacDonald D, Zijdenbos A, D'Avirro D, et al. In vivo morphometry of the intrasulcal gray matter in the human cingulate, paracingulate, and superior rostral sulci: hemispheric asymmetries, gender differences and probability maps. Journal of Comparative Neurology. 1996;376:664–673
  58. Paus T, Tomaiuolo F, Otkay N, MacDonald D, Petrides M, Atlas J, et al. Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map. Cerebral Cortex. 1996;6:207–214
  59. Paus T, Collins DL, Evans AC, Leonard G, Pike B, Zijdenbos A. Maturation of white matter in the human brain: a review of magnetic resonance studies. Brain Research Bulletin. 2001;54:255–266
  60. Phillips ML, Drevets WC, Rauch SL, Lane R. Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry. 2003;54:504–514
  61. Phillips ML, Drevets WC, Rauch SL, Lane R. Neurobiology of emotion perception II: implications for major psychiatric disorders. Biological Psychiatry. 2003;54:515–528
  62. Picard N, Strick PL. Motor areas of the medial wall: a review of their location and functional activation. Cerebral Cortex. 1996;6:342–353
  63. Rakic P. Radial unit hypothesis of neocortical expansion. In:  Bock GR,  Cardew G editor. Evolutionary Developmental Biology of the Cerebral Cortex. West Sussex: John Wiley & Sons, Ltd.; 2000;p. 30–45
  64. Rettmann ME, Kraut MA, Prince JL, Resnick SM. Cross-sectional and longitudinal analyses of anatomical sulcal changes associated with aging. Cerebral Cortex. 2006;16:1584–1594
  65. Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S. The role of the medial frontal cortex in cognitive control. Science. 2004;306:443–447
  66. Rosas HD, Liu AK, Hersch S, Glessner M, Ferrante RJ, Salat DH, et al. Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology. 2002;58:695–701
  67. Sanches M, Sassi RB, Axelson D, Nicoletti M, Brambilla P, Hatch JP, et al. Subgenual prefrontal cortex of child and adolescent bipolar patients: a morphometric magnetic resonance imaging study. Psychiatry Research: Neuroimaging. 2005;138:43–49
  68. Sassi RB, Brambilla P, Hatch JP, Nicoletti MA, Mallinger AG, Frank E, et al. Reduced left anterior cingulate volumes in untreated bipolar patients. Biological Psychiatry. 2004;56:467–475
  69. Selemon LD, Goldman-Rakic PS. The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biological Psychiatry. 1999;45:17–25
  70. Sharma V, Menon R, Carr TJ, Densmore M, Mazmanian D, Williamson PC. An MRI study of subgenual prefrontal cortex in patients with familial and non-familial bipolar I disorder. Journal of Affective Disorders. 2003;77:167–171
  71. Shaw P, Greenstein D, Lerch J, Clasen L, Lenroot R, Gogtay N, et al. Intellectual ability and cortical development in children and adolescents. Nature. 2006;440:676–679
  72. Smith SM. Fast robust automated brain extraction. Human Brain Mapping. 2002;17:143–155
  73. Sowell ER, Thompson PM, Tessner KD, Toga AW. Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. Journal of Neuroscience. 2001;21:8819–8829
  74. Sowell ER, Thompson PM, Leonard CM, Welcome SE, Kan E, Toga AW. Longitudinal mapping of cortical thickness and brain growth in normal children. Journal of Neuroscience. 2004;24:8223–8231
  75. Steele JD, Lawrie SM. Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis. NeuroImage. 2004;21:868–875
  76. Van Essen DC. A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. NeuroImage. 2005;28:635–662
  77. Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR. Human cingulate cortex: surface features, flat maps, and cytoarchitecture. Journal of Comparative Neurology. 1995;359:490–506
  78. Vogt BA, Berger GR, Derbyshire SW. Structural and functional dichotomy of human midcingulate cortex. European Journal of Neuroscience. 2003;18:3134–3144
  79. Welker W. Why does cerebral cortex fissure and fold? A review of determinants of sulci an gyri. In:  Jones EG,  Peters A editor. Cerebral Cortex. New York: Plenum Press; 1990;p. 3–136
  80. Wilke M, Kowatch RA, DelBello MP, Mills NP, Holland SK. Voxel-based morphometry in adolescents with bipolar disorder: first results. Psychiatry Research: Neuroimaging. 2004;131:57–69
  81. Yücel M, Stuart GW, Maruff P, Velakoulis D, Crowe SF, Savage G, et al. Hemispheric and gender-related differences in the gross morphology of the anterior cingulate/paracingulate cortex in normal volunteers: an MRI morphometric study. Cerebral Cortex. 2001;11:17–25
  82. Zimmerman ME, DelBello MP, Getz GE, Shear PK, Strakowski SM. Anterior cingulate subregion volumes and executive function in bipolar disorder. Bipolar Disorders. 2006;8:281–288

PII: S0925-4927(07)00129-1

doi: 10.1016/j.pscychresns.2007.06.004

Psychiatry Research: Neuroimaging
Volume 162, Issue 2 , Pages 123-132 , 28 February 2008