Psychiatry Research: Neuroimaging
Volume 183, Issue 1 , Pages 1-20 , 30 July 2010

3-D Cytoarchitectonic parcellation of human orbitofrontal cortex: Correlation with postmortem MRI

  • Harry B.M. Uylings

      Affiliations

    • Department of Anatomy & Neuroscience, VU University Medical Center, Graduate School Neurosciences Amsterdam, Amsterdam, The Netherlands
    • Departrment of Psychiatry & Neuropsychology, School for Mental Health and Neuroscience, Maastricht University, University of Maastricht, The Netherlands
    • Corresponding Author InformationCorresponding author. Dept. Anatomy & Neuroscience, VU University Medical Center, PO Box 7057, 1007 MB Amsterdam, The Netherlands. Tel.: +31 20 4448040; fax: +31 20 4448054.
    • These authors contributed equally.
  • ,
  • Ernesto J. Sanz -Arigita

      Affiliations

    • Department of Anatomy & Neuroscience, VU University Medical Center, Graduate School Neurosciences Amsterdam, Amsterdam, The Netherlands
    • Current address: Dept. Radiol., Ctr. Res. & Adv. Therap. Alzheimer's disease (CITA-AD), San Sebastian, Spain.
  • ,
  • Koos de Vos

      Affiliations

    • Netherlands Institute of Neuroscience, Royal Netherlands Academy of Sciences, Amsterdam, The Netherlands
    • Current address: Shell Int. Exploration & Production, Rijswijk, The Netherlands.
  • ,
  • Chris W. Pool

      Affiliations

    • Netherlands Institute of Neuroscience, Royal Netherlands Academy of Sciences, Amsterdam, The Netherlands
  • ,
  • Paul Evers

      Affiliations

    • Netherlands Brain Bank, Royal Netherlands Academy of Sciences, Amsterdam, The Netherlands
  • ,
  • Grazyna Rajkowska

      Affiliations

    • Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS 39216-4505, USA
    • These authors contributed equally.

Received 22 July 2009 ,Revised 15 March 2010 ,Accepted 21 April 2010.

References 

  1. Amunts K, Schleicher A, Bürgel U, Mohlberg H, Uylings HBM, Zilles K. Broca's region re-visited: cytoarchitecture and intersubject variability. Journal of Comparative Neurology. 1999;412:319–341
  2. Amunts K, Weiss PH, Mohlberg H, Pieperhoff P, Gurd J, Shah JN, et al. Analysis of the neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space — the role of Brodmann's areas 44 and 45. Neuroimage. 2004;22:42–56
  3. Barbas H. Specialized elements of orbitofrontal cortex in primates. Annals of the New York Academy of Sciences. 2007;1121:10–32
  4. Barbas H, Pandya DN. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. Journal of Comparative Neurology. 1989;286:353–375
  5. Barbas H, Zikopoulos B. Sequential and parallel circuits for emotional processing in primate orbitofrontal cortex. In:  Zald DH,  Rauch SL editor. The Orbitofrontal Cortex. Oxford: Oxford University Press; 2006;p. 57–91
  6. Barbas H, Ghasghaei HT, Rempel-Clower NL, Xiao D. Anatomic basis of functional specialization in prefrontal cortices in primates. In:  Grafman J editors. 2nd ed. Handbook of Neuropsychology. vol. 7:Amsterdam: Elsevier; 2002;p. 1–27
  7. Baxter MG, Parker A, Lindner CC, Izquierdo AD, Murray EA. Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex. Journal of Neuroscience. 2000;20:4311–4319
  8. Beck E. A cytoarchitectural investigation into the boundaries of cortical areas 13 and 14 in the human brain. Journal of Anatomy. 1949;83:147–157
  9. Blumberg HP, Stern E, Ricketts S, Martinez D, de Asis J, White T, et al. Rostral and orbital prefrontal dysfunction in the manic state of bipolar disorder. American Journal of Psychiatry. 1999;156:1986–1988
  10. Bok, S.T., 1959. Histonomy of the Cerebral Cortex. Elsevier Publ. Cy., Amsterdam.
  11. Bremner JD, Vythilingam M, Vermetten E, Nazeer A, Adil J, Khan S, et al. Reduced volume of orbitofrontal cortex in major depression. Biological Psychiatry. 2002;51:274–279
  12. Brockhaus H. Die Cyto- und Myeloarchitektonik des Cortex Claustralis und das Claustrum beim Menschen. Journal für Psychologisches Neurologie. 1940;49:249–348
  13. Brodmann K. Vergleichende Lokalisationslehre der Grosshirnrinde. Leipzig: Barth Verlag; 1909;
  14. Brodmann K. Physiologie des Gehirns. In:  Von Bruns P editors. Neue Deutsche Chirurgie. vol. 11:Stuttgart: Enke; 1914;p. 85–426
  15. Burgmans S, Van Boxtel MPJ, Vuurman EFPM, Smeets F, Gronenschild EHBM, Uylings HBM, et al. The prevalence of cortical gray matter atrophy may be overestimated in the healthy aging brain. Neuropsychology. 2009;23:541–550
  16. Carmichael ST, Price JL. Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. Journal of Comparative Neurology. 1994;346:366–402
  17. Cavada C, Company T, Tejedor J, Cruz Rizzolo RJ, Reinoso Suarez F. The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cerebral Cortex. 2000;10:220–242
  18. Caviness VS, Meyer J, Makris N, Kennedy DN. MRI-based topographic parcellation of human neocortex: an anatomically specified method with estimate of reliability. Journal of Cognitive Neuroscience. 1996;8:566–587
  19. Chiavaras MM, Petrides M. Orbitofrontal sulci of the human and macaque monkey brain. Journal of Comparative Neurology. 2000;422:35–54
  20. Cotter D, Pariante C, Rajkowska G. Glial pathology in major psychiatric disorders. In:  Agam G,  Belmaker RH,  Everall I editor. The Postmortem Brain in Psychiatric Research. Dordrecht: Kluwer Acad Publ; 2002;p. 291–324
  21. Cotter D, Hudson L, Landau S. Evidence for orbitofrontal pathology in bipolar disorder and major depression, but not in schizophrenia. Bipolar Disorders. 2005;7:358–369
  22. Crespo-Facorro B, Kim J-J, Andreasen NC, O'Leary DS, Wiser AK, Bailey JM, et al. Human frontal cortex: an MRI-based parcellation method. NeuroImage. 1999;10:500–519
  23. Crespo-Facorro B, Kim J-J, Andreasen NC, O'Leary DS, Magnotta VA. Regional frontal abnormalities in schizophrenia: a quantitative gray matter volume and cortical surface size study. Biological Psychiatry. 2000;48:110–119
  24. Croxson PL, Johansen-Berg H, Behrens TEJ, Robson MD, Pinsk MA, Gross CG, et al. Quantitative investigation of connections of the prefrontal cortex in the human and macaque using probabilistic diffusion tractography. Journal of Neuroscience. 2005;25:8854–8866
  25. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage. 2006;31:968–980
  26. Devlin JT, Poldrack RA. In praise of tedious anatomy. Neuroimage. 2007;37:1033–1041
  27. Drevets WC. Neuroimaging and neuropathological studies of depression: implications for the cognitive–emotional features of mood disorders. Current Opinion in Neurobiology. 2001;11:240–249
  28. Evers P, Uylings HBM. An optimal antigen retrieval method suitable for different antibodies on human brain tissue stored for several years in formaldehyde fixative. Journal of Neuroscience Methods. 1997;72:197–207
  29. Fischl B, Rajendran N, Busa E, Augustinack J, Hinds O, Yeo BTT, et al. Cortical folding patterns and predicting cytoarchitecture. Cerebral Cortex. 2008;18:1973–1980
  30. Fuster JM. The Prefrontal Cortex. 4th Ed. San Diego: Academic Press; 2008;
  31. Hof PR, Mufson EJ, Morrison JH. Human orbitofrontal cortex: cytoarchitecture and quantitative immunohistochemical parcellation. Journal of Comparative Neurology. 1995;359:48–68
  32. Howard MA, Roberts N, García-Fiñana M, Cowell PE. Volume estimation of prefrontal cortical subfields using MRI and stereology. Brain Research Protocols. 2003;10:125–138
  33. John JP, Wang L, Moffitt AJ, Singh HK, Gado MH, Csernansky JG. Inter-rater reliability of manual segmentation of the superior, inferior and middle frontal gyri. Psychiatry Research. 2006;148:151–163
  34. John JP, Yashavantha BS, Gado M, Veena R, Jain S, Ravishankar S, et al. A proposal for MRI-based parcellation of the frontal pole. Brain Structure & Function. 2007;212:245–253
  35. Keller SS, Crow T, Foundas A, Amunts K, Roberts N. Broca's area: nomenclature, anatomy, typology and asymmetry. Brain & Language. 2009;109:29–48
  36. Keppel G. Design and Analysis. A Researcher's Handbook. 2nd Ed. Englewood Cliffs: Prentice-Hall Inc; 1982;
  37. Kononova EP. The variability of structure of the cortex of the brain: inferior frontal gyrus of adult man. Brain Research Institute Publications. 1935;1:49–118(in Russian)
  38. Kringelbach ML. The human orbitofrontal cortex: linking reward to hedonic experience. Nature Reviews Neuroscience. 2005;6:691–702
  39. Kringelbach ML, Rolls ET. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Progress in Neurobiology. 2004;72:341–372
  40. Lacerda ALT, Hardan AY, Yorbik O, Keshavan MS. Measurement of the orbitofrontal cortex: a validation study of a new method. NeuroImage. 2003;19:665–673
  41. Lacerda ALT, Keshavan MS, Hardan AY, Yorbik O, Brambilla P, Sassi RB, et al. Anatomic evaluation of orbitofrontal cortex in major depressive disorder. Biological Psychiatry. 2004;55:353–358
  42. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, et al. Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping. 2000;10:120–131
  43. Mackey S, Petrides M. Architectonic mapping of the medial region of the human orbitofrontal cortex by density profiles. Neuroscience. 2009;159:1089–1107
  44. Man MS, Clarke HF, Roberts AC. The role of the orbitofrontal cortex and medial striatum in the regulation of prepotent responses to food rewards. Cerebral Cortex. 2009;19:899–906
  45. Merker B. Silver staining of cell bodies by means of the physical development. Journal of Neuroscience Methods. 1983;9:235–241
  46. Miguel-Hidalgo JJ, Rajkowska G. Immunohistochemistry of neural markers for the study of the laminar architecture in celloidin sections from the human cerebral cortex. Journal of Neuroscience Methods. 1999;93:69–79
  47. Miguel-Hidalgo JJ, Baucom C, Dilley G, Overholser JC, Meltzer HY, Stockmeier CA, et al. Glial fibrillary acidic protein immunoreactivity in the dorsolateral prefrontal cortex separates young from old adults with major depressive disorder. Biological Psychiatry. 2000;48:861–873
  48. Miguel-Hidalgo JJ, Wei J, Andrew M, Overholser JC, Jurjus G, Stockmeier CA, et al. Glia pathology in the prefrontal cortex in alcohol dependence with and without depressive symptoms. Biological Psychiatry. 2002;52:1121–1133
  49. Nakamura M, Nestor PG, Levitt JJ, Cohen AS, Kawashima T, Shenton ME, et al. Orbitofrontal volume deficit in schizophrenia and thought disorder. Brain. 2008;131:180–195
  50. Öngür D, Price JL. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex. 2000;10:206–219
  51. Öngür D, Ferry AT, Price JL. Architectonic subdivision of the human orbital and medial prefrontal cortex. Journal of Comparative Neurology. 2003;460:425–449
  52. Ono M, Kubik S, Abernathy CD. Atlas of the Cerebral Sulci. Stuttgart: Georg Thieme Verlag; 1990;
  53. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 5th ed. San Diego: Academic Press, Elsevier; 2005;
  54. Petrides M, Pandya DN. Comparative architectonic analysis of the human and the macaque frontal cortex. In:  Boller F,  Grafman J editor. Handbook of Neuropsychology. vol. 9:Amsterdam: Elsevier; 1994;p. 17–58
  55. Petrides M, Pandya DN. Comparative analysis of the human and macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. European Journal of Neuroscience. 2001;16:291–310
  56. Preuss TM, Goldman-Rakic PS. Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca. Journal of Comparative Neurology. 1991;310:429–474
  57. Rajkowska G, Goldman-Rakic PS. Cytoarchitectonic definition of prefrontal areas in the normal human cortex: I. Quantitative criteria for distinguishing areas 9 and 46. Cerebral Cortex. 1995;4:307–322
  58. Rajkowska G, Goldman-Rakic PS. Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46. Cerebral Cortex. 1995;4:323–337
  59. Rajkowska G, Miguel-Hidalgo JJ, Wei J, Dilley G, Pittman SD, Meltzer HY, et al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biological Psychiatry. 1999;45:1085–1098
  60. Rajkowska G, Miguel-Hidalgo JJ, Dubey P, Stockmeier CA, Krishnan RR. Prominent reduction in pyramidal neuron density in the orbitofrontal cortex of elderly depressed patients. Biological Psychiatry. 2005;58:297–306
  61. Rajkowska G, O'Dwyer G, Teleki Z, Stockmeier CA, Miguel-Hidalgo JJ. Reduction in calbindin-immunoreactive GABA interneurons in the prefrontal cortex in major depression. Neuropsychopharmacology. 2007;32:471–482
  62. Remijnse PL, Nielen MMA, Van Balkom AJLM, Cath DC, Van Oppen P, Uylings HBM, et al. Reduced OFC-striatal responsiveness on a reversal learning task in obsessive-compulsive disorder. Archives of General Psychiatry. 2006;63:1225–1236
  63. Retzius, G., 1896. Das Menschen Hirn. Teil 1 Text. Norstedt & Söner, Stockholm.
  64. Roberts AC. Primate orbitofrontal cortex and adaptive behaviour. Trends in Cognitive Science. 2006;10:83–90
  65. Roberts AC, Tomic DL, Parkinson CH, Roeling TA, Cutter DJ, Robbins TW, et al. Forebrain connectivity of the prefrontal cortex in the marmoset monkey (Callithrix jacchus): an anterograde and retrograde tract-tracing study. Journal of Comparative Neurology. 2007;502:86–112
  66. Rolls ET, Grabenhorst F. The orbitofrontal cortex and beyond: from affect to decision-making. Progress in Neurobiology. 2008;86:216–244
  67. Sarkisov SA, Filimonov IN, Kononova EP, Preobraschenskaja IS, Kukuev LA. Atlas of cytoarchitectonics of the human cerebral cortex. Moscow: Medzig; 1955;(in Russian)
  68. Schormann T, Zilles K. Three-dimensional linear and nonlinear transformations: an integration of light microscopical and MRI data. Human Brain Mapping. 1998;6:339–347
  69. Schwartz CE, Kunwar PS, Greve DN, Moran LR, Viner JC, Covino JM, et al. Structural differences in adult orbital and ventromedial prefrontal cortex predicted by infant temperament at 4months of age. Archives of General Psychiatry. 2010;67:78–84
  70. Swanson LW. Brain maps: structure of the rat brain. Amsterdam: Elsevier; 1992;
  71. Talairach J, Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain. 3-D proportioned system: an approach to cerebral imaging. Stuttgart: Thieme-Verlag; 1988;
  72. Tisserand DJ, Pruessner JC, Sanz Arigita EJ, Van Boxtel MPJ, Evans AC, Jolles J, et al. Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. NeuroImage. 2002;17:657–669
  73. Uylings HBM, Zilles K, Rajkowska G. Optimal staining methods for delineation of cortical areas and neuron counts in human brains. NeuroImage. 1999;9:439–445
  74. Uylings HBM, Rajkowska G, Sanz-Arigita E, Amunts K, Zilles K. Consequences of large interindividual variability for human brain atlases: converging macroscopical imaging and microscopical neuroanatomy. Anatomy Embryology (Berlin). 2005;210:423–431
  75. Uylings HBM, Malofeeva LI, Bogolepova IN, Jacobsen AM, Amunts K, Zilles K. No postnatal doubling of number of neurons in human Broca's area (BA 44 and 45)? A stereological study. Neuroscience. 2005;136:715–728
  76. Van den Heuvel OA, Remijnse PL, Mataix-Cols D, Vrenken H, Groenewegen HJ, Uylings HBM, et al. The major symptom dimensions of obsessive-compulsive disorder are mediated by partially distinct neural systems. Brain. 2009;132:853–868
  77. Van Hoesen GW, Parvizi J, Chu C-C. Orbitofrontal cortex pathology in Alzheimer's disease. Cerebral Cortex. 2000;10:243–251
  78. 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
  79. Völlm BA, de Araujo IE, Cowen PJ, Rolls ET, Kringelbach ML, Smith KA, et al. Methamphetamine activates reward circuitry in drug naïve human subjects. Neuropsychopharmacology. 2004;29:1715–1722
  80. Von Economo C, Koskinas GN. Die Cytoarchitektonik der Hirnrinde des Erwachsenen Menschen. Berlin: Springer Verlag; 1925;
  81. Walker EA. A cytoarchitectural study of the prefrontal area of the macaque monkey. Journal of Comparative Neurology. 1940;73:59–86

PII: S0925-4927(10)00148-4

doi: 10.1016/j.pscychresns.2010.04.012

Psychiatry Research: Neuroimaging
Volume 183, Issue 1 , Pages 1-20 , 30 July 2010