Primary visual cortex volume and total neuron number are reduced in schizophrenia

Journal of Comparative Neurology

Volumn 501, Issue 2, 2007, Pages 290-301

  Dorph Petersen, Karl Anton ^a,b   Pierri, Joseph N ^a   Wu, Qiang ^c   Sampson, Allan R ^c   Lewis, David A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Disector; Fractionator; Schizophrenia; Stereology

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN WEIGHT; CELL COUNT; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HISTOLOGY; HUMAN; HUMAN TISSUE; INFORMATION PROCESSING; MALE; MENTAL DISEASE; NERVE CELL; PRIORITY JOURNAL; SCHIZOPHRENIA; VISUAL CORTEX; VISUAL NERVOUS SYSTEM;

ADULT; AGED; AGED, 80 AND OVER; CELL COUNT; FEMALE; HUMANS; MALE; MIDDLE AGED; NEURONS; POSTMORTEM CHANGES; SCHIZOPHRENIA; VISUAL CORTEX;

EID: 33846919880     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21243     Document Type: Article

References (84)

1. Algan O, Rakic P. 1997. Radiation-induced, lamina-specific deletion of neurons in the primate visual cortex. J Comp Neurol 381:335-352.
2. Andersen BB, Gundersen HJG. 1999. Pronounced loss of cell nuclei and anisotropic deformation of thick sections. J Microsc 196:69-73.
3. Andreasen NC, O'Leary DS, Flaum M, Nopoulos P, Watkins GL, Boles Ponto LL, Hichwa RD. 1997. Hypofrontality in schizophrenia: Distributed dysfunctional circuits in neuroleptic-naïve patients. Lancet 349:1730-1734.
4. APA. 1994. DSM-IV. Diagnostic and statistical manual of mental disorders, 4th edition. Washington, DC: American Psychiatric Association.
5. Ardekani BA, Nierenberg J, Hoptman MJ, Javitt DC, Lim KO. 2003. MRI study of white matter diffusion anisotropy in schizophrenia. Neuroreport 14:2025-2029.
6. Baddeley A, Dorph-Petersen K-A, Vedel Jensen EB. 2006. A note on the stereological implications of irregular spacing of sections. J Microsc 222:177-181.
7. Bogerts B, Falkai P, Haupts M, Greve B, Ernst S, Tapernon-Franz U, Heinzmann U. 1990. Post-mortem volume measurements of limbic system and basal ganglia structures in chronic schizophrenics. Initial results from a new brain collection. Schizophr Res 3:295-301.
8. Brown AS. 2006. Prenatal infection as a risk factor for schizophrenia. Schizophr Bull 32:200-202.
9. Brown AS, Schaefer CA, Wyatt RJ, Begg MD, Goetz R, Bresnahan MA, Harkavy-Friedman J, Gorman JM, Malaspina D, Susser ES. 2002. Paternal age and risk of schizophrenia in adult offspring. Am J Psychiatry 159:1528-1533.
10. Butler PD, Schechter I, Zemon V, Schwartz SG, Greenstein VC, Gordon J, Schroeder CE, Javitt DC. 2001. Dysfunction of early-stage visual processing in schizophrenia. Am J Psychiatry 158:1126-1133.
11. Butler PD, Zemon V, Schechter I, Saperstein AM, Hoptman MJ, Lim KO, Revheim N, Silipo G, Javitt DC. 2005. Early-stage visual processing and cortical amplification deficits in schizophrenia. Arch Gen Psychiatry 62:495-504.
12. Byne W, Buchsbaum MS, Kemether E, Hazlett EA, Shinwari A, Mitropoulou V, Siever LJ. 2001. Magnetic resonance imaging of the thalamic mediodorsal nucleus and pulvinar in schizophrenia and schizotypal personality disorder. Arch Gen Psychiatry 58:133-140.
13. Byne W, Buchsbaum MS, Mattiace LA, Hazlett EA, Kemether E, Elhakem SL, Purohit DP, Haroutunian V, Jones L. 2002. Postmortem assessment of thalamic nuclear volumes in subjects with schizophrenia. Am J Psychiatry 159:59-65.
14. Danos P, Baumann B, Krämer A, Bernstein H-G, Stauch R, Krell D, Falkai P, Bogerts B. 2003. Volumes of association thalamic nuclei in schizophrenia: a postmortem study. Schizophr Res 60:141-155.
15. Dehay C, Giroud P, Berland M, Killackey H, Kennedy H. 1996. Contribution of thalamic input to the specification of cytoarchitectonic cortical fields in the primate: effects of bilateral enucleation in the fetal monkey on the boundaries, dimensions, and gyrification of striate and extrastriate cortex. J Comp Neurol 367:70-89.
16. Desco M, Gispert JD, Reig S, Sanz J, Pascau J, Sarramea F, Benito C, Santos A, Palomo T, Molina V. 2003. Cerebral metabolic patterns in chronic and recent-onset schizophrenia. Psychiatry Res 122:125-135.
17. Doniger GM, Foxe JJ, Murray MM, Higgins BA, Javitt DC. 2002. Impaired visual object recognition and dorsal/ventral stream interaction in schizophrenia. Arch Gen Psychiatry 59:1011-1020.
18. Dorph-Petersen K-A, Nyengaard JR, Gundersen HJG. 2001. Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc 204:232-246.
19. Dorph-Petersen K-A, Caric D, Saghafi R, Lewis DA. 2004a. Volume and neuron number of the lateral geniculate nucleus in schizophrenia and mood disorders. Program No. 109.1. 2004 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. Online.
20. Dorph-Petersen K-A, Rosenberg R, Nyengaard JR. 2004b. Estimation of number and volume of immunohistochemically stained neurons in complex brain regions. In: Evans SM, Janson AM, Nyengaard JR, editors. Quantitative methods in neuroscience. Oxford: Oxford University Press. p 216-238.
21. Dorph-Petersen K-A, Pierri JN, Perel JM, Sun Z, Sampson AR, Lewis DA. 2005. The influence of chronic exposure to antipsychotic medications on brain size before and after tissue fixation: a comparison of haloperidol and olanzapine in macaque monkeys. Neuropsychopharmacology 30:1649-1661.
22. Foxe JJ, Murray MM, Javitt DC. 2005. Filling-in in schizophrenia: a high-density electrical mapping and source-analysis investigation of illusory contour processing. Cereb Cortex 15:1914-1927.
23. Fukuchi-Shimogori T, Grove EA. 2001. Neocortex patterning by the secreted signaling molecule FGF8. Science 294:1071-1074.
24. Gilbert AR, Rosenberg DR, Harenski K, Spencer S, Sweeney JA, Keshavan MS. 2001. Thalamic volumes in patients with first-episode schizophrenia. Am J Psychiatry 158:618-624.
25. Glantz LA, Lewis DA. 1997. Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia: regional and diagnostic specificity. Arch Gen Psychiatry 54:943-952.
26. Glantz LA, Lewis DA. 2000. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 57:65-73.
27. Green MF, Nuechterlein KH, Mintz J. 1994a. Backward masking in schizophrenia and mania. I. Specifying a mechanism. Arch Gen Psychiatry 51:939-944.
28. Green MF, Nuechterlein KH, Mintz J. 1994b. Backward masking in schizophrenia and mania. II. Specifying the visual channels. Arch Gen Psychiatry 51:945-951.
29. Grieve KL, Acuña C, Cudeiro J. 2000. The primate pulvinar nuclei: vision and action. Trends Neurosci 23:35-39.
30. Gundersen HJG. 1977. Notes on the estimation of the numerical density of arbitrary profiles: the edge effect. J Microsc 111:219-223.
31. Gundersen HJG. 1986. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsc 143:3-45.
32. Gundersen HJG, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263.
33. Gundersen HJG, Jensen EBV, Kiêu K, Nielsen J. 1999. The efficiency of systematic sampling in stereology - reconsidered. J Microsc 193:199-211.
34. Harrison PJ, Freemantle N, Geddes JR. 2003. Meta-analysis of brain weight in schizophrenia. Schizophr Res 64:25-34.
35. Hashimoto T, Bergen SE, Nguyen QL, Xu B, Monteggia LM, Pierri JN, Sun Z, Sampson AR, Lewis DA. 2005. Relationship of brain-derived neurotrophic factor and its receptor TrkB to altered inhibitory prefrontal circuitry in schizophrenia. J Neurosci 25:372-383.
36. Hedges LV, Olkin I. 1985. Statistical methods for meta-analysis. New York: Academic Press.
37. Highley JR, Walker MA, Crow TJ, Esiri MM, Harrison PJ. 2003. Low medial and lateral right pulvinar volumes in schizophrenia: a postmortem study. Am J Psychiatry 160:1177-1179.
38. Howard CV, Reed MG. 1998. Unbiased stereology. Three-dimensional measurement in microscopy. Oxford: Bios Scientific.
39. Javitt DC, Shelley A-M, Silipo G, Lieberman JA. 2000. Deficits in auditory and visual context-dependent processing in schizophrenia: defining the pattern. Arch Gen Psychiatry 57:1131-1137.
40. Kemether EM, Buchsbaum MS, Byne W, Hazlett EA, Haznedar M, Brickman AM, Platholi J, Bloom R. 2003. Magnetic resonance imaging of mediodorsal, pulvinar, and centromedian nuclei of the thalamus in patients with schizophrenia. Arch Gen Psychiatry 60:983-991.
41. Kéri S, Kelemen O, Benedek G, Janka Z. 2004. Vernier threshold in patients with schizophrenia and in their unaffected siblings. Neuropsychology 18:537-542.
42. Konopaske GT, Dorph-Petersen KA, Pierri JN, Wu Q, Sampson AR, Lewis DA. 2006. Effect of chronic exposure to antipsychotic medication on cell numbers in the parietal cortex of macaque monkeys. Neuropsychopharmacology advance online publication, 25 October 2006; doi:10.1038/sj-npp.1301233.
43. Kostovic I, Rakic P. 1984. Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining. J Neurosci 4:25-42.
44. Lesch A, Bogerts B. 1984. The diencephalon in schizophrenia: evidence for reduced thickness of the periventricular grey matter. Eur Arch Psychiatr Neurol Sci 234:212-219.
45. Leuba G, Garey LJ. 1987. Evolution of neuronal numerical density in the developing and aging human visual cortex. Hum Neurobiol 6:11-18.
46. Leuba G, Kraftsik R. 1994a. Changes in volume, surface estimate, three-dimensional shape and total number of neurons of the human primary visual cortex from midgestation until old age. Anat Embryol (Berl) 190:351-366.
47. Leuba G, Kraftsik R. 1994b. Visual cortex in Alzheimer's disease: occurrence of neuronal death and glial proliferation, and correlation with pathological hallmarks. Neurobiol Aging 15:29-43.
48. Mai JK, Ashwell KWS. 2004. Fetal development of the central nervous system. In: Paxinos G, Mai JK, editors. The human nervous system. San Diego: Elsevier Academic Press. p 49-94.
49. Müller F, O'Rahilly R. 2004. Embryonic development of the central nervous system. In: Paxinos G, Mai JK, editors. The human nervous system. San Diego: Elsevier Academic Press. p 22-48.
50. Oster S, Christoffersen P, Gundersen HJG, Nielsen JO, Pakkenberg B, Pedersen C. 1993. Cerebral atrophy in AIDS: a stereological study. Acta Neuropathol (Berl) 85:617-622.
51. Oster S, Christoffersen P, Gundersen HJG, Nielsen JO, Pedersen C, Pakkenberg B. 1995. Six billion neurons lost in AIDS. A stereological study of the neocortex. APMIS 103:525-529.
52. Oster S, Christoffersen P, Gundersen HJG, Nielsen JO, Pedersen C, Pakkenberg B. 1996. Erratum: six billion neurons lost in AIDS. A stereological study of the neocortex. APMIS 104:479.
53. Pakkenberg B. 1993. Total nerve cell number in neocortex in chronic schizophrenics and controls estimated using optical disectors. Biol Psychiatry 34:768-772.
54. Ragsdale CW, Grove EA. 2001. Patterning the mammalian cerebral cortex. Curr Opin Neurobiol 11:50-58.
55. Rakic P. 1988. Specification of cerebral cortical areas. Science 241:170-176.
56. Regeur L. 2000. Increasing loss of brain tissue with increasing dementia: a stereological study of post-mortem brains from elderly females. Eur J Neurol 7:47-54.
57. Regeur L, Jensen GB, Pakkenberg H, Evans SM, Pakkenberg B. 1994. No global neocortical nerve cell loss in brains from patients with senile dementia of Alzheimer's type. Neurobiol Aging 15:347-352.
58. Reite M, Teale P, Rojas DC, Benkers TL, Carlson J. 2003. Anomalous somatosensory cortical localization in schizophrenia. Am J Psychiatry 160:2148-2153.
59. Saccuzzo DP, Braff DL. 1981. Early information processing deficit in schizophrenia. New findings using schizophrenic subgroups and manic control subjects. Arch Gen Psychiatry 38:175-179.
60. Schechter I, Butler PD, Silipo G, Zemon V, Javitt DC. 2003. Magnocellular and parvocellular contributions to backward masking dysfunction in schizophrenia. Schizophr Res 64:91-101.
61. Schindler MK, Wang L, Selemon LD, Goldman-Rakic PS, Rakic P, Csernansky JG. 2002. Abnormalities of thalamic volume and shape detected in fetally irradiated rhesus monkeys with high dimensional brain mapping. Biol Psychiatry 51:827-837.
62. Selemon LD, Goldman-Rakic PS. 1999. The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biol Psychiatry 45:17-25.
63. 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.
64. Selemon LD, Mrzljak J, Kleinman JE, Herman MM, Goldman-Rakic PS. 2003. Regional specificity in the neuropathologic substrates of schizophrenia: a morphometric analysis of Broca's area 44 and area 9. Arch Gen Psychiatry 60:69-77.
65. Selemon LD, Wang L, Nebel MB, Csernansky JG, Goldman-Rakic PS, Rakic P. 2005. Direct and indirect effects of fetal irradiation on cortical gray and white matter volume in the macaque. Biol Psychiatry 57:83-90.
66. Šestan N, Rakic P, Donoghue MJ. 2001. Independent parcellation of the embryonic visual cortex and thalamus revealed by combinatorial Eph/ ephrin gene expression. Curr Biol 11:39-43.
67. Sharma J, Angelucci A, Sur M. 2000. Induction of visual orientation modules in auditory cortex. Nature 404:841-847.
68. Sherman SM, Guillery RW. 2002. The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc Lond B Biol Sci 357:1695-1708.
69. Shimogori T, Grove EA. 2005. Fibroblast growth factor 8 regulates neocortical guidance of area-specific thalamic innervation. J Neurosci 25:6550-6560.
70. Shipp S. 2003. The functional logic of cortico-pulvinar connections. Philos Trans R Soc Lond B Biol Sci 358:1605-1624.
71. St Clair D, Xu M, Wang P, Yu Y, Fang Y, Zhang F, Zheng X, Gu N, Feng G, Sham P, He L. 2005. Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959-1961. JAMA 294:557-562.
72. Stark AK, Uylings HBM, Sanz-Arigita E, Pakkenberg B. 2004. Glial cell loss in the anterior cingulate cortex, a subregion of the prefrontal cortex, in subjects with schizophrenia. Am J Psychiatry 161:882-888.
73. Sur M, Angelucci A, Sharma J. 1999. Rewiring cortex: the role of patterned activity in development and plasticity of neocortical circuits. J Neurobiol 41:33-43.
74. Susser ES, Lin SP. 1992. Schizophrenia after prenatal exposure to the Dutch Hunger Winter of 1944-1945. Arch Gen Psychiatry 49:983-988.
75. Susser E, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, Gorman JM. 1996. Schizophrenia after prenatal famine: further evidence. Arch Gen Psychiatry 53:25-31.
76. Sweet RA, Dorph-Petersen K-A, Lewis DA. 2005. Mapping auditory core, lateral belt, and parabelt cortices in the human superior temporal gyrus. J Comp Neurol 491:270-289.
77. Tek C, Gold J, Blaxton T, Wilk C, McMahon RP, Buchanan RW. 2002. Visual perceptual and working memory impairments in schizophrenia. Arch Gen Psychiatry 59:146-153.
78. Thune JJ, Uylings HBM, Pakkenberg B. 2001. No deficit in total number of neurons in the prefrontal cortex in schizophrenics. J Psychiatr Res 35:15-21.
79. Uylings HBM, Rajkowska G, Sanz-Arigita E, Amunts K, Zilles K. 2005. Consequences of large interindividual variability for human brain atlases: converging macroscopical imaging and microscopical neuroanatomy. Anat Embryol (Berl) 210:423-431.
80. Van Horn SC, Erişir A, Sherman SM. 2000. Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J Comp Neurol 416:509-520.
81. von Melchner L, Pallas SL, Sur M. 2000. Visual behaviour mediated by retinal projections directed to the auditory pathway. Nature 404:871-876.
82. West MJ, Slomianka L, Gundersen HJG. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
83. Woo T-U, Miller JL, Lewis DA. 1997. Schizophrenia and the parvalbumin-containing class of cortical local circuit neurons. Am J Psychiatry 154:1013-1015.
84. Wright IC, Rabe-Hesketh S, Woodruff PWR, David AS, Murray RM, Bullmore ET. 2000. Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 157:16-25.