Disturbances of corticogenesis in schizophrenia: Morphological findings provide new evidence for the maldevelopmental hypothesis

Neuropsychobiology

Volumn 40, Issue 1, 1999, Pages 1-13

  Kalus, Peter ^a   Senitz, Dieter ^b   Beckmann, Helmut ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b NONE

Author keywords

Anterior cingulate cortex; Corticogenesis; Dil fluorescence staining; Golgi impregnation; Immunocytochemistry; Interneurons; Maldevelopmental hypothesis; Prefrontal cortex; Pyramidal cells; Schizophrenia

Indexed keywords

FLUORESCENT DYE;

ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CINGULATE GYRUS; GOLGI COMPLEX; HISTOLOGY; HUMAN; IMMUNOCYTOCHEMISTRY; INTERNEURON; LIMBIC SYSTEM; MORPHOLOGY; NERVE CELL; NEUROPATHOLOGY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SCHIZOPHRENIA;

EID: 0032808436     PISSN: 0302282X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000026591     Document Type: Article

References (85)

1. Alzheimer A: Beiträge zur pathologischen Anatomie der Hirnrinde und der anatomischen Grundlage einiger Psychosen. Monatsschr Psychiatr Neurol 1897;2:82-120.
2. Senitz D: Neuronale Strukturveränderungen im Neokortex bei schizophrener Psychose; in Kühne GE, Klepel J, Molcan J (eds): Neurobiologische Aspekte in der Psychiatrie. VEDA der slowakischen Akademie der Wissenschaften, Bratislava 1984, pp 374-376.
3. Senitz D: Über morphologische Befunde bei der schizophrenen Psychose, dargestellt mit der Golgi-Methode. Biologische Aspekte bei Psychosen. Z Univ Rostock 1986: 30-33.
4. Beckmann H, Jakob H: Pränatale Entwicklungsstörungen von Hirnstrukturen bei schizophrenen Psychosen. Nervenarzt 1994;65:454-463.
5. Taylor DG: Advances in the neuropathology of schizophrenia; in Den Boer JA, Westenberg HGM, Van Praag HM (eds): Advances in the Neurobiology of Schizophrenia. Chichester, Wiley, 1995, pp 111-130.
6. Jakob H, Beckmann H: Clinico-neuropathological studies of developmental disorders in the limbic system in chronic schizophrenia; in Schizophrenia: An Integrative View. XIV Congress CINP. Ric Educ Perm (Suppl) 1984;39: 81.
7. Jakob H, Beckmann H: Prenatal developmental disturbances in the limbic allocortex in schizophrenics. J Neural Transm 1986;65: 303-326.
8. Jakob H, Beckmann H: Circumscribed malformations and nerve cell alterations in the entorhinal cortex of schizophrenics. J Neural Transm (Gen Sect) 1994;98:83-106.
9. Kovelman JA, Scheibel AB: A neurohistological correlate of schizophrenia. Biol Psychiatry 1984;19:1601-1621.
10. Arnold SE, Lee VMY, Gur RE, Trojanowski JQ: Abnormal expression of two microtubule-associated proteins (MAP-2 and MAP-5) in specific subfields of hippocampal formation in schizophrenia. Proc Natl Acad Sci USA 1991; 88:10850-10854.
11. Arnold SE, Hyman BT, Van Hoesen GW, Damasio AR: Some cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia. Arch Gen Psychiatry 1991;48:625-632.
12. Degreef G, Bogerts B, Falkai P, Greve B, Lantos G, Ashtari M, Lieberman J: Increased prevalence of the cavum septum pellucidum in magnetic resonance scans and post-mortem brains of schizophrenic patients. Psychiatry Res 1992;45:1-13.
13. Barta PE, Pearlson GD, Brill LB, Royall R, McGilchrist IK, Pulver AE, Powers RE, Casanova MF, Tien AY, Frangou S, Petty RG: Planum temporale asymmetry reversal in schizophrenia: replication and relationship to gray matter abnormalities. Am J Psychiatry 1997; 154:661-667.
14. Andreasen NC, Swayze V, O'Leary DO, Nopoulos P, Cizadlo T, Harris G, Arndt S, Flaum M: Abnormalities in midline attentional circuitry in schizophrenia: Evidence from magnetic resonance and positron emission tomography. Eur Neuropsychopharmacol (Suppl) 1995:37-42.
15. Stöber G, Franzek E, Beckmann H: The role of maternal infectious diseases during pregnancy in the etiology of schizophrenia in offspring. Eur Psychiatry 1992;7:147-152.
16. Mednick SA, Huttunen MO, Machon RA: Prenatal influenza infections and adult schizophrenia. Schizophr Bull 1994;20:263-267.
17. Staudt A, Götz F, Staudt J, Dörner G: Acute and long-term effects of perinatally administered human recombinant interleukin-1β on the second layer of the entorhinal region of the gyrus parahippocampalis in rats. Neuroendocrinol Lett 1995;17:41-49.
18. Szentágothai J: Die Neuronenschaltungen der Grosshirnrinde. Verh Anat Ges 1976;70:187-215.
19. Rakic P: Intra- and extracellular control of neuronal migration: Relevance to cortical malformations; in Galaburda AM, Christen Y (eds): Normal and Abnormal Development of Cortex. Heidelberg, Springer, 1997, pp. 81-98.
20. Sotelo C, Soriano E: Finding a role for Cajal-Retzius cells in cerebral cortex development; in Galaburda AM, Christen Y (eds): Normal and Abnormal Development of Cortex. Heidelberg, Springer, 1997, pp 67-80.
21. Shatz CJ, Chun JJM, Luskin MB: The role of the subplate in the development of the mammalian telencephalon; in Peters A, Jones EG (eds): Cerebral Cortex, vol 7: Development and Maturation of Cerebral Cortex. New York, Plenum Press, 1988, pp 35-58.
22. Ghosh A, Shatz CI: Pathfinding and target selection by developing geniculocortical axons. J Neurosci 1992;12:39-55.
23. Bogerts B, Meertz E, Schönfeldt-Bausch R: Basal ganglia and limbic system pathology in schizophrenia. A morphometric study of brain volume and shrinkage. Arch Gen Psychiatry 1985;42:784-791.
24. Bogerts B, Falkai P, Haupts M, Greve B, Ernst S, Tapernon-Franz U, Heinzmann U: Post-mortem volume measurements of limbic system and basal ganglia structures in chronic schizophrenics. Initial results from a new brain collection. Schizophr Res 1990;3:295-301.
25. Heckers S, Heinsen H, Heinsen Y, Beckmann H: Limbic structures and lateral ventricle in schizophrenia. Arch Gen Psychiatry 1990;47: 1016-1022.
26. Heckers S, Heinsen H, Heinsen Y, Beckmann H: Morphometry of the parahippocampal gyrus in schizophrenics and controls. Some anatomic considerations. J Neural Transm (Gen Sect) 1990;80:151-155.
27. Benes FM, Sorensen I, Bird ED: Reduced neuronal size in posterior hippocampus of schizophrenic patients. Schizophr Bull 1991;17:597-608.
28. Christison GW, Casanova MF, Weinberger DR, Rawlings R, Kleinman JE: A quantitative investigation of hippocampal pyramidal cell size, shape, and variability of orientation in schizophrenia. Arch Gen Psychiatry 1989;46: 1027-1032.
29. Benes FM, Davidson J, Bird ED: Quantitative cytoarchitectural studies of the cerebral cortex of schizophrenics. Arch Gen Psychiatry 1986; 43:31-35.
30. Selemon LD, Rajkowska G, Goldman-Rakic PS: Abnormally high neuronal density in the schizophrenic cortex. Arch Gen Psychiatry 1995;52:805-818.
31. Heckers S, Heinsen H, Heinsen Y, Beckmann H: Cortex, white matter, and basal ganglia in schizophrenia: Volumetric postmortem study. Biol Psychiatry 1991;29:556-566.
32. Lauer M, Beckmann H: The human striatum in schizophrenia. I. Increase in overall relative striatal volume in schizophrenics. Psychiatry Res (Neuroimaging Sect) 1997;68:87-98.
33. Beckmann H, Lauer M: The human striatum in schizophrenia. II. Increased number of striatal neurons in schizophrenics. Psychiatry Res (Neuroimaging Sect) 1997;68:99-109.
34. Pakkenberg B: Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch Gen Psychiatry 1990;47:1023-1028.
35. White EL: Cortical Circuits. Boston, Birkhäuser, 1989, pp 1-223.
36. Senitz D: Über einen interkapillären Zelltyp im Hirn alter Menschen. Zbl Allg Path Pathol Anat 1978;122:423-427.
37. Supprian T, Senitz D, Beckmann H: Presentation of human neocortical neurons stained with the carbocyanine dye DiI compared to the Golgi silver impregnation technique. J Brain Res 1993;34:403-406.
38. Kalus P, Senitz D: Parvalbumin in the human anterior cingulate cortex: Morphological heterogeneity of inhibitory interneurons. Brain Res 1996;729:45-54.
39. Kalus P, Senitz D, Beckmann H: Cortical layer I changes in schizophrenia: A marker for impaired brain development? J Neural Transm 1997;104:549-559.
40. Kalus P, Senitz D, Beckmann H: Altered distribution of parvalbumin-immunoreactive local circuit neurons in the anterior cingulate cortex of schizophrenic patients. Psychiatry Res (Neuroimaging Sect) 1997;75:49-59.
41. Winkelmann E: Prinzipien synaptischer Organisation im Zentralnervensystem von Vertebraten. Regionale Strukturunterschiede unter besonderer Berücksichtigung des visuellen Systems. Z Mikrosk Anat Forsch 1982;96: 755-774.
42. Takada K, Nakamura H, Takashima S: Cortical dysplasia in Fukuyama congenital muscular dystrophy (FCMD): A Golgi and angioarchitectonic analysis. Acta Neuropathol (Berl) 1988;76:170-178.
43. Uranova NA, Vikhreva OV, Orlovskaya DD, Denisov DV: Increased numerical density of synapses in layer VI of postmortem prefrontal cortex in schizophrenia, in press.
44. Senitz D, Winkelmann E: Neuronale Strukturanomalität im orbito-frontalen Cortex bei Schizophrenien. J Brain Res 1991;32:149-158.
45. Poljakow GI: Entwicklung der Neuronen der menschlichen Grosshirnrinde. Leipzig, Thieme, 1979, pp. 1-320.
46. Belichenko P, Sourander P, Malmgren K, Nordborg C, van Essen C, Rydenhag B, Lindström S, Hedström A, Uvebrant P, Dahlström A: Dendritic morphology in epileptogenic cortex from TRPE patients, revealed by intracellular Lucifer Yellow microinjection and confocal laser scanning microscopy. Epilepsy Res 1994; 18:233-247.
47. Belichenko P, Oldfors A, Hagberg B, Dahlström A: Rett syndrome: 3-D confocal microscopy of cortical pyramidal dendrites and afferents. Neuroreport 1994;5:1509-1513.
48. Purpura DP: Dendritic differentiation in human cerebral cortex: Normal and aberrant developmental patterns; in Kreutzberg GW (ed): Advances in Neurology, vol 12: Physiology and Pathology of Dendrites. New York, Raven Press, 1975, pp 91-116.
49. Kamei A, Takashima S, Chan F, Becker LE: Abnormal dendritic development in maple syrup urine disease. Pediatr Neurol 1992;8:145-147.
50. Andressen C, Blümcke I, Celio MR: Calcium-binding proteins: Selective markers of nerve cells. Cell Tissue Res 1993;271:181-208.
51. Anderson SA, Volk DW, Lewis DA: Increased density of microtubule associated protein 2-immunoreactive neurons in the prefrontal white matter of schizophrenic subjects. Schizophr Res 1996;19:111-119.
52. Akbarian S, Bunney WE, Potkin SG, Wigal SB, Hagman JO, Sandman CA, Jones EG: Altered distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development. Arch Gen Psychiatry 1993; 50:169-177.
53. Akbarian S, Vinuela A, Kim JJ, Potkin SG, Bunney WE, Jones EG: Distorted distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase neurons in temporal lobe of schizophrenics implies anomalous cortical development. Arch Gen Psychiatry 1993;50:178-187.
54. Karson CN, Garcia-Rill E, Biedermann JA, Mrak RE, Husain MM, Skinner RD: The brain stem reticular formation in schizophrenia. Psychiatry Res (Neuroimaging Sect) 1991;40:31-48.
55. Daviss SR, Lewis DA: Local circuit neurons of the prefrontal cortex in schizophrenia: selective increase in the density of calbindin-immunore-active neurons. Psychiatry Res 1995;59:81-96.
56. Beasley CL, Reynolds GP: Parvalbumin-immunoreactive neurons are reduced in the pre-frontal cortex of schizophrenics. Schizophr Res 1997;24:349-355.
57. Ferrer I: Experimentally induced cortical malformations in rats. Child's Nerv Syst 1993;9: 403-407.
58. Evrard P, Marret S, Gressens P: Genetic and environmental determinants of neocortical development: clinical applications; in Galaburda AM, Christen Y (eds): Normal and Abnormal Development of Cortex. Berlin, Springer, 1997, pp. 165-177.
59. Huttenlocher PR: Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res 1979;163:195-205.
60. Anderson SA, Classey JD, Condé F, Lund JS, Lewis DA: Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex. Neuroscience 1995;67:7-22.
61. Moore DB, Quintero MA, Ruygrok AC, Walker DW, Heaton MB: Prenatal ethanol exposure reduces parvalbumin-immunoreactive GA-BAergic neuronal number in the adult rat cingulate cortex. Neurosci Lett 1998; 249:25-28.
62. Wang XH, Finley A, Murphy EH: Region specific changes in parvalbumin expression in rabbit neocortex following prenatal cocaine exposure. Soc Neurosci Abstr 1994;20:1319.
63. Wang XH, Jenkins AO, Choi L, Murphy EH: Altered neuronal distribution of parvalbumin in anterior cingulate cortex of rabbits exposed in utero to cocaine. Exp Brain Res 1996;112: 359-371.
64. Houser CR: GABA neurons in seizure disorders: A review of immunocytochemical studies. Neurochem Res 1991;16:295-308.
65. Arai H, Emson PC, Mountjoy CQ, Carassco LH, Heizmann CW: Loss of parvalbumin-immunoreactive neurones from cortex in Alzheimer-type dementia. Brain Res 1987;418: 164-169.
66. Guentchev M, Hainfellner J-A, Trabattoni H: Distribution of parvalbumin-immunoreactive neurons in brain correlates with hippocampal and temporal cortical pathology in Creutzfeldt-Jakob disease. J Neuropathol Exp Neurol 1997; 56:1119-1124.
67. Zhu Z-Q, Armstrong DL, Hamilton WJ, Grossman RG: Disproportionate loss of CA4 parvalbumin-immunoreactive interneurons in patients with Ammon's horn sclerosis. J Neuropathol Exp Neurol 1997;56:988-998.
68. Nimchinsky EA, Vogt BA, Morrison JH, Hof PR: Neurofilament and calcium-binding proteins in the human cingulate cortex. J Comp Neurol 1997;384:597-620.
69. Benes FM: Relationship of cingulate cortex to schizophrenia and other psychiatric disorders; in Vogt BA, Gabriel M (eds): Neurobiology of Cingulate Cortex and Limbic Thalamus. Boston, Birkhäuser, 1993, pp 581-605.
70. DeLisi LE: The genetics of schizophrenia: Past, present, and future concepts. Schizophr Res 1997;28:163-175.
71. Carlsson A: Neurocircuitries and neurotransmitter interactions in schizophrenia. Int Clin Psychopharmacol 1995;10(suppl 3):21-28.
72. Thome J, Foley P, Riederer P: Neurotrophic factors and the maldevelopmental hypothesis of schizophrenic psychoses. J Neural Transm 1998;105:85-100.
73. Holden RJ, Pakula IS, Mooney PA: A neuroimmunological model of schizophrenia and major depression: A review. Hum Psychopharmacol 1997;12:177-201.
74. Weinberger DR, Berman KF, Zec RF: Physiological dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow (rCBF) evidence. Arch Gen Psychiatry 1986;43:114-125.
75. Park S, Holzman PS: Schizophrenics show spatial working memory deficits. Arch Gen Psychiatry 1992;49:975-982.
76. Goldman-Rakic PS: Circuitry of primate pre-frontal cortex and regulation of behavior by representational memory; in Plum F, Mount-castle V (eds): Handbook of Physiology. The Nervous System: vol 5. Bethesda, American Physiological Society, 1987, pp. 373-417.
77. Fuster JM: The prefrontal cortex, mediator of temporal contingencies. Hum Neurobiol 1985; 4:169-179.
78. Dolan RJ, Fletcher P, Frith CD, Friston KJ, Frackowiak RSJ, Grasby PM: Dopaminergic modulation of impaired cognitive activation in the anterior cingulate cortex in schizophrenia. Nature 1995;378:180-182.
79. Andreasen NC, Rezai K, Alliger R, Swayze VW, Flaum M, Kirchner P, Cohen G, O'Leary DS: Hypofrontality in neuroleptic-naive patients and in patients with chronic schizophrenia. Assessment with xenon 133 single-photon emission computed tomography and the Tower of London. Arch Gen Psychiatry 1992;49:943-958.
80. Devinsky O, Morrell MJ, Vogt BA: Contributions of anterior cingulate cortex to behaviour. Brain 1995;118:279-306.
81. Lewis DA, Anderson SA: The functional architecture of the prefrontal cortex and schizophrenia. Psychol Med 1995;25:887-894.
82. Benes FM: Neurobiological investigations in cingulate cortex of schizophrenic brain. Schizophr Bull 1993;19:537-549.
83. Benes FM, McSparren J, SanGiovanni JP, Vincent SL: Deficits in small interneurons in cingulate cortex of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 1991;48: 996-1001.
84. Leonhard K: Aufteilung der endogenen Psychosen und ihre differenzierte Ätiologie. Stuttgart, Thieme, 1995.
85. Leonhard K: Biopsychologie der endogenen Psychosen. Leipzig, Hirzel, 1970.