Stereological assessment of the dorsal anterior cingulate cortex in schizophrenia: Absence of changes in neuronal and glial densities

Neuropathology and Applied Neurobiology

Volumn 39, Issue 4, 2013, Pages 348-361

  Hoistad M ^a,b   Heinsen, H ^c   Wicinski, B ^a   Schmitz, C ^d   Hof, P R ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Swedish Council on Health Technology Assessment   (Sweden)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cytoarchitecture; Dysmyelination; Morphology; Myelin; Oligodendrocytes; White matter

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; AUTOPSY; CELL COUNT; CELL DENSITY; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); CYTOARCHITECTURE; DISEASE DURATION; ENTORHINAL CORTEX; FRONTAL CORTEX; GLIA CELL; HUMAN; HUMAN TISSUE; MALE; MYELIN DEFICIENCY; NEOCORTEX; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; OLIGODENDROGLIA; ONSET AGE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SCHIZOPHRENIA; STEREOLOGY; TRACTOGRAPHY; WHITE MATTER;

ADULT; AGE OF ONSET; CELL COUNT; CEREBRAL CORTEX; DEMYELINATING DISEASES; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; GYRUS CINGULI; HUMANS; INTERNATIONAL CLASSIFICATION OF DISEASES; MALE; MIDDLE AGED; NEUROGLIA; NEURONS; OLIGODENDROGLIA; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; YOUNG ADULT;

EID: 84875901419     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2012.01296.x     Document Type: Article

References (90)

1. Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD, Haroutunian V, Fienberg AA. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Natl Acad Sci U S A 2001; 98: 4746-51.
2. Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB, Starkey M, Webster MJ, Yolken RH, Bahn S. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 2003; 362: 798-805.
3. Dracheva S, Davis KL, Chin B, Woo DA, Schmeidler J, Haroutunian V. Myelin-associated mRNA and protein expression deficits in the anterior cingulate cortex and hippocampus in elderly schizophrenia patients. Neurobiol Dis 2006; 21: 531-40.
4. Buchsbaum MS, Friedman J, Buchsbaum BR, Chu KW, Hazlett EA, Newmark R, Schneiderman JS, Torosjan Y, Tang C, Hof PR, Stewart D, Davis KL, Gorman J. Diffusion tensor imaging in schizophrenia. Biol Psychiatry 2006; 60: 1181-7.
5. Buchsbaum MS, Tang CY, Peled S, Gudbjartsson H, Lu D, Hazlett EA, Downhill J, Haznedar M, Fallon JH, Atlas SW. MRI white matter diffusion anisotropy and PET metabolic rate in schizophrenia. Neuroreport 1998; 9: 425-30.
6. Lim KO, Hedehus M, Moseley M, de Crespigny A, Sullivan EV, Pfefferbaum A. Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging. Arch Gen Psychiatry 1999; 56: 367-74.
7. Foong J, Maier M, Barker GJ, Brocklehurst S, Miller DH, Ron MA. In vivo investigation of white matter pathology in schizophrenia with magnetisation transfer imaging. J Neurol Neurosurg Psychiatry 2000; 68: 70-4.
8. Foong J, Symms MR, Barker GJ, Maier M, Woermann FG, Miller DH, Ron MA. Neuropathological abnormalities in schizophrenia: evidence from magnetization transfer imaging. Brain 2001; 124: 882-92.
9. Kubicki M, McCarley R, Westin CF, Park HJ, Maier S, Kikinis R, Jolesz FA, Shenton ME. A review of diffusion tensor imaging studies in schizophrenia. J Psychiatr Res 2007; 41: 15-30.
10. Kubicki M, Park H, Westin CF, Nestor PG, Mulkern RV, Maier SE, Niznikiewicz M, Connor EE, Levitt JJ, Frumin M, Kikinis R, Jolesz FA, McCarley RW, Shenton ME. DTI and MTR abnormalities in schizophrenia: analysis of white matter integrity. Neuroimage 2005; 26: 1109-18.
11. Kubicki M, Westin CF, Nestor PG, Wible CG, Frumin M, Maier SE, Kikinis R, Jolesz FA, McCarley RW, Shenton ME. Cingulate fasciculus integrity disruption in schizophrenia: a magnetic resonance diffusion tensor imaging study. Biol Psychiatry 2003; 54: 1171-80.
12. Sun Z, Wang F, Cui L, Breeze J, Du X, Wang X, Cong Z, Zhang H, Li B, Hong N, Zhang D. Abnormal anterior cingulum in patients with schizophrenia: a diffusion tensor imaging study. Neuroreport 2003; 14: 1833-6.
13. Davis KL, Stewart DG, Friedman JI, Buchsbaum M, Harvey PD, Hof PR, Buxbaum J, Haroutunian V. White matter changes in schizophrenia: evidence for myelin-related dysfunction. Arch Gen Psychiatry 2003; 60: 443-56.
14. Walterfang M, Wood SJ, Velakoulis D, Pantelis C. Neuropathological, neurogenetic and neuroimaging evidence for white matter pathology in schizophrenia. Neurosci Biobehav Rev 2006; 30: 918-48.
15. Dwork AJ, Mancevski B, Rosoklija G. White matter and cognitive function in schizophrenia. Int J Neuropsychopharmacol 2007; 10: 513-36.
16. Höistad M, Segal D, Takahashi N, Sakurai T, Buxbaum JD, Hof PR. Linking white and grey matter in schizophrenia: oligodendrocyte and neuron pathology in the prefrontal cortex. Front Neuroanat 2009; 3: 9.
17. Karoutzou G, Emrich HM, Dietrich DE. The myelin-pathogenesis puzzle in schizophrenia: a literature review. Mol Psychiatry 2008; 13: 245-60.
18. Segal D, Koschnick JR, Slegers LH, Hof PR. Oligodendrocyte pathophysiology: a new view of schizophrenia. Int J Neuropsychopharmacol 2007; 10: 503-11.
19. Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR. Human cingulate cortex: surface features, flat maps, and cytoarchitecture. J Comp Neurol 1995; 359: 490-506.
20. Öngür D, Ferry AT, Price JL. Architectonic subdivision of the human orbital and medial prefrontal cortex. J Comp Neurol 2003; 460: 425-49.
21. Gittins R, Harrison PJ. A quantitative morphometric study of the human anterior cingulate cortex. Brain Res 2004; 1013: 212-22.
22. Palomero-Gallagher N, Mohlberg H, Zilles K, Vogt B. Cytology and receptor architecture of human anterior cingulate cortex. J Comp Neurol 2008; 508: 906-26.
23. Vogt BA. Structural organization of cingulate cortex: areas, neurons, and somatodendritic transmitter receptors. In Neurobiology of Cingulate Cortex and Limbic Thalamus. Ed BA Vogt. Boston: Birkhäuser, 1993; 19-70.
24. Jones EG, Powell TP. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 1970; 93: 793-820.
25. Vogt BA, Pandya DN. Cingulate cortex of the rhesus monkey: II. Cortical afferents. J Comp Neurol 1987; 262: 271-89.
26. Vogt BA, Pandya DN, Rosene DL. Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents. J Comp Neurol 1987; 262: 256-70.
27. Van Hoesen GW, Morecraft RJ, Vogt BA. Connections of the monkey cingulate cortex. In Neurobiology of Cingulate Cortex and Limbic Thalamus. Eds BA Vogt, M Gabriel. Boston: Birkhauser, 1993; 249-84.
28. Beckmann M, Johansen-Berg H, Rushworth MF. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci 2009; 29: 1175-90.
29. Barbas H, Pandya DN. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 1989; 286: 353-75.
30. Vogt BA, Finch DM, Olson CR. Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb Cortex 1992; 2: 435-43.
31. Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 2000; 4: 215-22.
32. Mohanty A, Engels AS, Herrington JD, Heller W, Ho MH, Banich MT, Webb AG, Warren SL, Miller GA. Differential engagement of anterior cingulate cortex subdivisions for cognitive and emotional function. Psychophysiology 2007; 44: 343-51.
33. Etkin A, Egner T, Kalisch R. Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 2011; 15: 85-93.
34. Beauregard M, Levesque J, Bourgouin P. Neural correlates of conscious self-regulation of emotion. J Neurosci 2001; 21: RC165.
35. Hof PR, Haroutunian V, Friedrich VL Jr, Byne W, Buitron C, Perl DP, Davis KL. Loss and altered spatial distribution of oligodendrocytes in the superior frontal gyrus in schizophrenia. Biol Psychiatry 2003; 53: 1075-85.
36. Stark AK, Uylings HB, Sanz-Arigita E, Pakkenberg B. Glial cell loss in the anterior cingulate cortex, a subregion of the prefrontal cortex, in subjects with schizophrenia. Am J Psychiatry 2004; 161: 882-8.
37. Segal D, Schmitz C, Hof PR. Spatial distribution and density of oligodendrocytes in the cingulum bundle are unaltered in schizophrenia. Acta Neuropathol 2009; 117: 385-94.
38. Benes FM. Evidence for neurodevelopment disturbances in anterior cingulate cortex of post-mortem schizophrenic brain. Schizophr Res 1991; 5: 187-8.
39. Selemon LD, Rajkowska G, Goldman-Rakic PS. Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. Arch Gen Psychiatry 1995; 52: 805-18; discussion 19-20.
40. Selemon LD, Rajkowska G, Goldman-Rakic PS. Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three-dimensional, stereologic counting method. J Comp Neurol 1998; 392: 402-12.
41. Andreasen N, Nasrallah HA, Dunn V, Olson SC, Grove WM, Ehrhardt JC, Coffman JA, Crossett JH. Structural abnormalities in the frontal system in schizophrenia. A magnetic resonance imaging study. Arch Gen Psychiatry 1986; 43: 136-44.
42. Nesvag R, Lawyer G, Varnas K, Fjell AM, Walhovd KB, Frigessi A, Jonsson EG, Agartz I. Regional thinning of the cerebral cortex in schizophrenia: effects of diagnosis, age and antipsychotic medication. Schizophr Res 2008; 98: 16-28.
43. Narr KL, Bilder RM, Toga AW, Woods RP, Rex DE, Szeszko PR, Robinson D, Sevy S, Gunduz-Bruce H, Wang YP, DeLuca H, Thompson PM. Mapping cortical thickness and gray matter concentration in first episode schizophrenia. Cereb Cortex 2005; 15: 708-19.
44. Baiano M, David A, Versace A, Churchill R, Balestrieri M, Brambilla P. Anterior cingulate volumes in schizophrenia: a systematic review and a meta-analysis of MRI studies. Schizophr Res 2007; 93: 1-12.
45. Koo MS, Levitt JJ, Salisbury DF, Nakamura M, Shenton ME, McCarley RW. A cross-sectional and longitudinal magnetic resonance imaging study of cingulate gyrus gray matter volume abnormalities in first-episode schizophrenia and first-episode affective psychosis. Arch Gen Psychiatry 2008; 65: 746-60.
46. Kreczmanski P, Heinsen H, Mantua V, Woltersdorf F, Masson T, Ulfig N, Schmidt-Kastner R, Korr H, Steinbusch HW, Hof PR, Schmitz C. Volume, neuron density and total neuron number in five subcortical regions in schizophrenia. Brain 2007; 130: 678-92.
47. Kreczmanski P, Schmidt-Kastner R, Heinsen H, Steinbusch HW, Hof PR, Schmitz C. Stereological studies of capillary length density in the frontal cortex of schizophrenics. Acta Neuropathol 2005; 109: 510-18.
48. Casanova MF, de Zeeuw L, Switala A, Kreczmanski P, Korr H, Ulfig N, Heinsen H, Steinbusch HW, Schmitz C. Mean cell spacing abnormalities in the neocortex of patients with schizophrenia. Psychiatry Res 2005; 133: 1-12.
49. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR), 4th edn. Washington, DC: APA, 2000.
50. World Health Organization. ICD-10, International Statistical Classification of Diseases and Related Health Problems, 10th revision edn. Geneva, Switzerland: WHO, 2007.
51. Heinsen H, Heinsen YL. Serial thick, frozen, gallycyanin stained sections of human central nervous system. J Histotechnol 1991; 14: 167-73.
52. Heinsen H, Beckmann H, Heinsen YL, Gallyas F, Haas S, Scharff G. Laminar neuropathology in Alzheimer's disease by a modified Gallyas impregnation. Psychiatry Res 1989; 29: 463-5.
53. Braak H, Braak E. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging 1995; 16: 271-8.
54. Heinsen H, Arzberger T, Schmitz C. Celloidin mounting (embedding without infiltration) - a new, simple and reliable method for producing serial sections of high thickness through complete human brains and its application to stereological and immunohistochemical investigations. J Chem Neuroanat 2000; 20: 49-59.
55. Heinsen H, Henn R, Eisenmenger W, Gotz M, Bohl J, Bethke B, Lockemann U, Puschel K. Quantitative investigations on the human entorhinal area: left-right asymmetry and age-related changes. Anat Embryol (Berl) 1994; 190: 181-94.
56. Schmitz C, Hof PR. Design-based stereology in neuroscience. Neuroscience 2005; 130: 813-31.
57. Barbas H, Rempel-Clower N. Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex 1997; 7: 635-46.
58. Roberts GW, Colter N, Lofthouse R, Bogerts B, Zech M, Crow TJ. Gliosis in schizophrenia: a survey. Biol Psychiatry 1986; 21: 1043-50.
59. Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW. Mapping cortical change across the human life span. Nat Neurosci 2003; 6: 309-15.
60. Selemon LD, Kleinman JE, Herman MM, Goldman-Rakic PS. Smaller frontal gray matter volume in postmortem schizophrenic brains. Am J Psychiatry 2002; 159: 1983-91.
61. Rimol LM, Hartberg CB, Nesvag R, Fennema-Notestine C, Hagler DJ Jr, Pung CJ, Jennings RG, Haukvik UK, Lange E, Nakstad PH, Melle I, Andreassen OA, Dale AM, Agartz I. Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biol Psychiatry 2010; 68: 41-50.
62. 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: 153-9.
63. Pomarol-Clotet E, Canales-Rodriguez EJ, Salvador R, Sarro S, Gomar JJ, Vila F, Ortiz-Gil J, Iturria-Medina Y, Capdevila A, McKenna PJ. Medial prefrontal cortex pathology in schizophrenia as revealed by convergent findings from multimodal imaging. Mol Psychiatry 2010; 15: 823-30.
64. Selemon LD, Goldman-Rakic PS. The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biol Psychiatry 1999; 45: 17-25.
65. Harrison PJ. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 1999; 122: 593-624.
66. Bouras C, Kövari E, Hof PR, Riederer BM, Giannakopoulos P. Anterior cingulate cortex pathology in schizophrenia and bipolar disorder. Acta Neuropathol 2001; 102: 373-9.
67. Pakkenberg B. Total nerve cell number in neocortex in chronic schizophrenics and controls estimated using optical disectors. Biol Psychiatry 1993; 34: 768-72.
68. Thune JJ, Uylings HB, Pakkenberg B. No deficit in total number of neurons in the prefrontal cortex in schizophrenics. J Psychiatr Res 2001; 35: 15-21.
69. Benes FM, McSparren J, Bird ED, SanGiovanni JP, Vincent SL. Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 1991; 48: 996-1001.
70. Benes FM, Davidson J, Bird ED. Quantitative cytoarchitectural studies of the cerebral cortex of schizophrenics. Arch Gen Psychiatry 1986; 43: 31-5.
71. Rajkowska G, Selemon LD, Goldman-Rakic PS. Neuronal and glial somal size in the prefrontal cortex: a postmortem morphometric study of schizophrenia and Huntington disease. Arch Gen Psychiatry 1998; 55: 215-24.
72. 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. Biol Psychiatry 2003; 53: 1086-98.
73. Benes FM. Emerging principles of altered neural circuitry in schizophrenia. Brain Res Rev 2000; 31: 251-69.
74. Ongur D, Drevets WC, Price JL. Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A 1998; 95: 13290-5.
75. 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. Arch Gen Psychiatry 2001; 58: 545-53.
76. Selimbeyoglu A, Parvizi J. Electrical stimulation of the human brain: perceptual and behavioral phenomena reported in the old and new literature. Front Hum Neurosci 2010; 4: 46.
77. Habel U, Chechko N, Pauly K, Koch K, Backes V, Seiferth N, Shah NJ, Stocker T, Schneider F, Kellermann T. Neural correlates of emotion recognition in schizophrenia. Schizophr Res 2010; 122: 113-23.
78. Ghashghaei HT, Hilgetag CC, Barbas H. Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 2007; 34: 905-23.
79. Davidson RJ, Pizzagalli D, Nitschke JB, Putnam K. Depression: perspectives from affective neuroscience. Annu Rev Psychol 2002; 53: 545-74.
80. Konner M. Universals of behavioral development in relation to brain myelination. In Brain Maturation and Cognitive Development. Eds KR Gibson, AC Petersen. New York: Aldine de Gruyter, 1991; 181-223.
81. Marenco S, Weinberger DR. The neurodevelopmental hypothesis of schizophrenia: following a trail of evidence from cradle to grave. Dev Psychopathol 2000; 12: 501-27.
82. Weinberger DR. Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 1987; 44: 660-9.
83. Insel TR. Rethinking schizophrenia. Nature 2010; 468: 187-93.
84. Weinberger DR, Lipska BK. Cortical maldevelopment, anti-psychotic drugs, and schizophrenia: a search for common ground. Schizophr Res 1995; 16: 87-110.
85. Skudlarski P, Jagannathan K, Anderson K, Stevens MC, Calhoun VD, Skudlarska BA, Pearlson G. Brain connectivity is not only lower but different in schizophrenia: a combined anatomical and functional approach. Biol Psychiatry 2010; 68: 61-9.
86. Fallon JH, Opole IO, Potkin SG. The neuroanatomy of schizophrenia: circuitry and neurotransmittor systems. Clin Neurosci Res 2003; 1-2: 77-107.
87. Zalesky A, Fornito A, Seal ML, Cocchi L, Westin CF, Bullmore ET, Egan GF, Pantelis C. Disrupted axonal fiber connectivity in schizophrenia. Biol Psychiatry 2011; 69: 80-9.
88. Kubicki M, Niznikiewicz M, Connor E, Nestor P, Bouix S, Dreusicke M, Kikinis R, McCarley R, Shenton M. Relationship between white matter integrity, attention, and memory in schizophrenia: a diffusion tensor imaging study. Brain Imaging Behav 2009; 3: 191-201.
89. Whitford TJ, Kubicki M, Schneiderman JS, O'Donnell LJ, King R, Alvarado JL, Khan U, Markant D, Nestor PG, Niznikiewicz M, McCarley RW, Westin CF, Shenton ME. Corpus callosum abnormalities and their association with psychotic symptoms in patients with schizophrenia. Biol Psychiatry 2010; 68: 70-7.
90. Takei K, Yamasue H, Abe O, Yamada H, Inoue H, Suga M, Muroi M, Sasaki H, Aoki S, Kasai K. Structural disruption of the dorsal cingulum bundle is associated with impaired Stroop performance in patients with schizophrenia. Schizophr Res 2009; 114: 119-27.