Changes in cortical thickness in the frontal lobes in schizophrenia are a result of thinning of pyramidal cell layers

European Archives of Psychiatry and Clinical Neuroscience

Volumn 263, Issue 1, 2013, Pages 25-39

  Williams, M R ^a   Chaudhry, R ^a   Perera, S ^a   Pearce, R K B ^a   Hirsch, S R ^a   Ansorge, O ^b   Thom, M ^c   Maier, M ^a  

^a CHARING CROSS HOSPITAL   (United Kingdom)

^b RADCLIFFE INFIRMARY   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cingulate; Cortical thickness; Frontal lobe; Pyramidal layers; Schizophrenia

Indexed keywords

EOSIN; HEMATOXYLIN;

ADULT; AGED; ARTICLE; BIPOLAR DISORDER; CINGULATE GYRUS; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); FEMALE; FRONTAL CORTEX; HUMAN; HUMAN TISSUE; MAJOR DEPRESSION; MALE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SCHIZOPHRENIA; TEMPORAL CORTEX; TEMPORAL GYRUS; TISSUE SECTION;

ADULT; AGED; AGED, 80 AND OVER; BENZOXAZINES; BIPOLAR DISORDER; COHORT STUDIES; DEPRESSIVE DISORDER, MAJOR; FEMALE; FRONTAL LOBE; HEMATOXYLIN; HUMANS; MALE; MIDDLE AGED; PSYCHIATRIC STATUS RATING SCALES; PYRAMIDAL CELLS; SCHIZOPHRENIA; SEX FACTORS;

EID: 84873288340     PISSN: 09401334     EISSN: 14338491     Source Type: Journal    
DOI: 10.1007/s00406-012-0325-8     Document Type: Article

References (71)

1. Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P (2001) The anterior cingulate cortex. The evolution of an interface between emotion and cognition. Ann N Y Acad Sci 935:107-117 (Pubitemid 32511395)
2. Baare WF, Hulshoff Pol HE, Hijman R, Mali WP, Viergever MA, Kahn RS (1999) Volumetric analysis of frontal lobe regions in schizophrenia: relation to cognitive function and symptomatology. Biol Psychiatry 45:1597-1605 (Pubitemid 29294104)
3. Barta PE, Pearlson GD, Powers RE, Richards SS, Tune LE (1990) Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry 147:1457-1462 (Pubitemid 20365432)
4. Benes FM, McSparren J, Bird ED, SanGiovanni JP, Vincent SL (1991) Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 48:996-1001
5. Benes FM, Lange N (2001) Two-dimensional versus threedimensional cell counting: a practical perspective. Trends Neurosci 24:11-17 (Pubitemid 32332892)
6. Bilder RM, Wu H, Bogerts B, Ashtari M, Robinson D, Woerner M, Lieberman JA, Degreef G (1999) Cerebral volume asymmetries in schizophrenia and mood disorders: a quantitative magnetic resonance imaging study. Int J Psychophysiol 34:197-205
7. Bogerts B (1984) Neuropathology of schizophrenia. Fortschr Neurol Psychiatr 52:428-437
8. Bogerts B (1993) Recent advances in the neuropathology of schizophrenia. Schizophr Bull 19:431-445 (Pubitemid 23183155)
9. Bogerts B (1999) The neuropathology of schizophrenic diseases: historical aspects and present knowledge. Eur Arch Psychiatry Clin Neurosci 249(Suppl 4):2-13
10. Bouras C, Kövari E, Hof PR, Riederer BM, Giannakopoulos P (2001) Anterior cingulate cortex pathology in schizophrenia and bipolar disorder. Acta Neuropathol (Berl) 102:373-379 (Pubitemid 32894708)
11. Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4:215-222 (Pubitemid 30332147)
12. Cannon TD (1996) Abnormalities of brain structure and function in schizophrenia: implications for aetiology and pathophysiology. Ann Med 28:533-539 (Pubitemid 27019551)
13. Chana G, Landau S, Beasley C, Everall IP, Cotter D (2003) 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 53:1086-1098 (Pubitemid 36695084)
14. Cotter D, Mackay D, Landau S, Kerwin R, Everall I (2001) Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Arch Gen Psychiatry 58:545-553 (Pubitemid 32523734)
15. Dickey CC, McCarley RW, Voglmaier MM, Niznikiewicz MA, Seidman LJ, Hirayasu Y, Fischer I, Teh EK, Van Rhoads R, Jakab M, Kikinis R, Jolesz FA, Shenton ME (1999) Schizotypal personality disorder and MRI abnormalities of temporal lobe grey matter. Biol Psychiatry 45:1393-1402 (Pubitemid 29457550)
16. Dierks T, Linden DE, Jandl M, Formisano E, Goebel R, Lanfermann H, Singer W (1999) Activation of Heschl's gyrus during auditory hallucinations. Neuron 22:615-621 (Pubitemid 29159859)
17. Elston GN (2003) Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb Cortex (New York, NY: 1991) 13:1124-1138 (Pubitemid 37336435)
18. Flaum M, O'Leary DS, Swayze VW, Miller DD, Arndt S, Andreasen NC (1995) Symptom dimensions and brain morphology in schizophrenia and related psychotic disorders. J Psychiatr Res 29:261-276
19. Gittins R, Harrison PJ (2004) A quantitative morphometric study of the human anterior cingulate cortex. Brain Res 1013:212-222 (Pubitemid 38757428)
20. Glantz LA, Lewis DA (2000) Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 57:65-73 (Pubitemid 30035660)
21. Glausier JR, Lewis DA (2011) Selective pyramidal cell reduction of GABA(A) receptor a1 subunit messenger RNA expression in schizophrenia. Neuropsychopharmacology 36:2103-2110
22. Goldstein JM, Seidman LJ, Santangelo S, Knapp PH, Tsuang MT (1994) Are schizophrenic men at higher risk for developmental deficits than schizophrenic women? Implications for adult neuropsychological functions. J Psychiatr Res 28:483-498
23. Love S, Louis DN, Ellison DW (eds) (2008) Greenfields neuropathology, 8th edn. Hodder-Arnold Publication, London
24. Gur RE, Cowell P, Turetsky BI, Gallacher F, Cannon T, Bilker W, Gur RC (1998) A follow-up magnetic resonance imaging study of schizophrenia. Relationship of neuroanatomical changes to clinical and neurobehavioral measures. Arch Gen Psychiatry 55:145-152 (Pubitemid 28087600)
25. Gur RE, Keshavan MS, Lawrie SM (2007) Deconstructing psychosis with human brain imaging. Schizophr Bull 33:921-931 (Pubitemid 47216648)
26. Gur RE, Cowell PE, Latshaw A, Turetsky BI, Grossman RI, Arnold SE, Bilker WB, Gur RC (2000) Reduced dorsal and orbital prefrontal grey matter volumes in schizophrenia. Arch Gen Psychiatry 57:761-768 (Pubitemid 30650111)
27. Harrison PJ (1999) The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 122:593-624 (Pubitemid 29158770)
28. Highley JR, Walker MA, Esiri MM, McDonald B, Harrison PJ, Crow TJ (2001) Schizophrenia and the frontal lobes: post-mortem stereological study of tissue volume. Br J Psychiatry 178: 337-343 (Pubitemid 32280928)
29. Hirayasu Y, Shenton ME, Salisbury DF, Kwon JS, Wible CG, Fischer IA, Yurgelun-Todd D, Zarate C, Kikinis R, Jolesz FA, McCarley RW (1999) Subgenual cingulate cortex volume in firstepisode psychosis. Am J Psychiatry 156:1091-1093 (Pubitemid 29302806)
30. Hoptman MJ, Nierenberg J, Bertisch HC, Catalano D, Ardekani BA, Branch CA, Delisi LE (2008) A DTI study of white matter microstructure in individuals at high genetic risk for schizophrenia. Schizophr Res 106:115-124
31. Job DE, Whalley HC, McConnell S, Glabus M, Johnstone EC, Lawrie SM (2002) Structural gray matter differences between first-episode schizophrenics and normal controls using voxelbased morphometry. Neuroimage 17:880-889 (Pubitemid 35317021)
32. Kalus P, Senitz D, Lauer M, Beckmann H (1999) Inhibitory cartridge synapses in the anterior cingulate cortex of schizophrenics. J Neural Transm 106:763-771 (Pubitemid 29401364)
33. Kasparek T, Prikryl R, Mikl M, Schwarz D, Ceskova E, Krupa P (2006) Prefrontal but not temporal grey matter changes in males with first-episode schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 31:151-157
34. Kasper BS, Taylor DC, Janz D, Kasper EM, Maier M, Williams MR, Crow TJ (2010) Neuropathology of epilepsy and psychosis: the contributions of J.A.N. Corsellis. Brain 133:3795-3805
35. Kopelman A, Andreasen NC, Nopoulos P (2005) Morphology of the anterior cingulate gyrus in patients with schizophrenia: relationship to typical neuroleptic exposure. Am J Psychiatry 162:1872-1878 (Pubitemid 41428616)
36. Kuperberg GR, Broome MR, McGuire PK, David AS, Eddy M, Ozawa F, Goff D, West WC, Williams SC, van der Kouwe AJ, Salat DH, Dale AM, Fischl B (2003) Regionally localized thinning of the cerebral cortex in schizophrenia. Arch Gen Psychiatry 60:878-888 (Pubitemid 37122306)
37. Law AJ, Harrison PJ (2003) The distribution and morphology of prefrontal cortex pyramidal neurons identified using anti-neurofilament antibodies SMI32, N200 and FNP7. Normative data and a comparison in subjects with schizophrenia, bipolar disorder or major depression. J Psychiatr Res 37:487-499 (Pubitemid 37238942)
38. Lawrie SM, Abukmeil SS, Chiswick A, Egan V, Santosh CG, Best JJ (1997) Qualitative cerebral morphology in schizophrenia: a magnetic resonance imaging study and systematic literature review. Schizophr Res 25:155-166 (Pubitemid 27245138)
39. Lawrie SM, Abukmeil SS (1998) Brain abnormality in schizophrenia. A systematic and quantitative review of volumetric magnetic resonance imaging studies. Br J Psychiatry 172:110-120 (Pubitemid 28097708)
40. Levin S (1984) Frontal lobe dysfunctions in schizophrenia-II. Impairments of psychological and brain functions. J Psychiatr Res 18:57-72 (Pubitemid 14173840)
41. Mah L, Zarate CA Jr, Singh J, Duan YF, Luckenbaugh DA, Manji HK, Drevets WC (2006) Regional Cerebral Glucose Metabolic Abnormalities in Bipolar II Depression. Biol Psychiatry 61:765-775
42. Maric N, Kamer T, Schneider Axmann T, Dani I, Jasovic Gasic M, Paunovic VR, Falkai P (2003) Volumetric analysis of grey matter, white matter and cerebrospinal fluid space in schizophrenia. Srp Arh Celok Lek 131:26-30
43. McCarley RW, Niznikiewicz MA, Salisbury DF, Nestor PG, O'Donnell BF, Hirayasu Y, Grunze H, Greene RW, Shenton ME (1999) Cognitive dysfunction in schizophrenia: unifying basic research and clinical aspects. Eur Arch Psychiatry Clin Neurosci 249(Suppl 4):69-82
44. Meisenzahl EM, Koutsouleris N, Bottlender R, Scheuerecker J, Jäger M, Teipel SJ, Holzinger S, Frodl T, Preuss U, Schmitt G, Burgermeister B, Reiser M, Born C, Möller HJ (2008) Structural brain alterations at different stages of schizophrenia: A voxelbased morphometric study. Schizophr Res 104:44-60
45. Mesulam M (1983) The functional anatomy and hemispheric specialization for directed attention. TINS 6:384-387
46. Narr KL, Toga AW, Szeszko P, Thompson PM, Woods RP, Robinson D, Sevy S, Wang Y, Schrock K, Bilder RM (2005) Cortical thinning in cingulate and occipital cortices in first episode schizophrenia. Biol Psychiatry 58:32-40 (Pubitemid 40909933)
47. Nohara S, Suzuki M, Kurachi M, Yamashita I, Matsui M, Seto H, Saitoh O (2000) Neural correlates of memory organization deficits in schizophrenia. A single photon emission computed tomography study with 99mTc-ethyl-cysteinate dimer during a verbal learning task. Schizophr Res 42:209-222 (Pubitemid 30216532)
48. Pakkenberg B (1987) Post-mortem study of chronic schizophrenic brains. Br J Psychiatry: J Mental Sci 151:744-752 (Pubitemid 18000085)
49. Pantelis C, Velakoulis D, McGorry PD, Wood SJ, Suckling J, Phillips LJ, Yung AR, Bullmore ET, Brewer W, Soulsby B, Desmond P, McGuire PK (2003) Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet 361:281-288 (Pubitemid 36126187)
50. Pierri JN, Volk CL, Auh S, Sampson A, Lewis DA (2001) Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry 58:466-473 (Pubitemid 32411327)
51. Posner MI, Petersen SE (1990) The attention system of the human brain. Ann Rev Neurosci 13:25-42 (Pubitemid 20100639)
52. Rajkowska G, Selemon LD, Goldman-Rakic PS (1998) Neuronal and glial somal size in the prefrontal cortex: a postmortem morphometric study of schizophrenia and Huntington disease. Arch Gen Psychiatry 55:215-224
53. Reig S, Moreno C, Moreno D, Burdalo M, Janssen J, Parellada M, Zabala A, Desco M, Arango C (2009) Progression of brain volume changes in adolescent-onset psychosis. Schizophr Bull 35:233-243
54. Rimol LM, Hartberg CB, Nesvåg 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 (2010) Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biol Psychiatry 68:41-50
55. Seidman LJ, Yurgelun-Todd D, Kremen WS, Woods BT, Goldstein JM, Faraone SV, Tsuang MT (1994) Relationship of prefrontal and temporal lobe MRI measures to neuropsychological performance in chronic schizophrenia. Biol Psychiatry 35:235-246 (Pubitemid 24118455)
56. Selemon LD, Rajkowska G, Goldman-Rakic PS (1995) Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. Arch Gen Psychiatry 52:805-818
57. Selemon LD, Rajkowska G, Goldman-Rakic PS (1998) Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three-dimensional, stereologic counting method. J Comp Neurol 392:402-412 (Pubitemid 28165894)
58. Selemon LD, Rajkowska G, Goldman-Rakic PS (1998) Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three-dimensional, stereologic counting method. J Comp Neurol. 392:402-412 (Pubitemid 28165894)
59. Shenton ME, Dickey CC, Frumin M, McCarley RW (2001) A review of MRI findings in schizophrenia. Schizophr Res 49:1-52 (Pubitemid 32451739)
60. Shenton ME, Kikinis R, Jolesz FA, Pollak SD, LeMay M, Wible CG, Hokama H, Martin J, Metcalf D, Coleman M (1992) Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. N Engl J Med 327:604-612
61. Smiley JF, Konnova K, Bleiwas C (2012) Cortical thickness, neuron density and size in the inferior parietal lobe in schizophrenia. Schizophr Res 136:43-50
62. Sullivan EV, Lim KO, Mathalon D, Marsh L, Beal DM, Harris D, Hoff AL, Faustman WO, Pfefferbaum A (1998) A profile of cortical grey matter volume deficits characteristic of schizophrenia. Cereb Cortex 8:117-124 (Pubitemid 28134394)
63. Todtenkopf MS, Vincent SL, Benes FM (2005) A cross-study meta-analysis and three-dimensional comparison of cell counting in the anterior cingulate cortex of schizophrenic and bipolar brain. Schizophr Res 73:79-89 (Pubitemid 39574682)
64. van Haren NE, Schnack HG, Cahn W, van den Heuvel MP, Lepage C, Collins L, Evans AC, Hulshoff Pol HE, Kahn RS (2011) Changes in cortical thickness during the course of illness in schizophrenia. Arch Gen Psychiatry 68:871-880
65. Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR (1995) Human cingulate cortex: surface features, flat maps, and cytoarchitecture. J Comp Neurol 359:490-506
66. Wang JF, Shao L, Sun X, Young LT (2009) Increased oxidative stress in the anterior cingulate cortex of subjects with bipolar disorder and schizophrenia. Bipolar Disord 11:523-529
67. Weickert TW, Goldberg TE, Gold JM, Bigelow LB, Egan MF, Weinberger DR (2000) Cognitive impairments in patients with schizophrenia displaying preserved and compromised intellect. Arch Gen Psychiatry 57:907-913
68. Weinberger DR, Berman KF, Zec RF (1986) Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. Arch Gen Psychiatry 43:114-124 (Pubitemid 16163530)
69. Wright IC, Rabe-Hesketh S, Woodruff PW, David AS, Murray RM, Bullmore ET (2000) Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 157:16-25 (Pubitemid 30027416)
70. Zipursky RB, Lim KO, Sullivan EV, Brown BW, Pfefferbaum A (1992) Widespread cerebral grey matter volume deficits in schizophrenia. Arch Gen Psychiatry 49:195-205
71. Zipursky RB, Seeman MV, Bury A, Langevin R, Wortzman G, Katz R (1997) Deficits in grey matter volume are present in schizophrenia but not bipolar disorder. Schizophr Res 26:85-92 (Pubitemid 27431770)