Abstract
We demonstrate here for the first time the formation of vascular anastomoses in the human neocortex. The orbitofrontal cortex (OFC) of the perinatal human brain is structurally immature, so that the maturation of neurons, neuroglia and intracortical capillaries can be conveniently studied by comparison with these elements in motor and striatal cortex of the same brain. In OFC of the perinatal human brain, indication of prominent anastomosis formation in the upper layers (lamina II and III) is observed. Golgi silver impregnation and electron microscopic techniques were employed to demonstrate individual stages of vascular anastomosis development. Along with capillary angiogenesis, vascular anastomosis formation is of major importance for the ontogenesis of neuronal and glial elements of the CNS, particularly with respect to optimal metabolic support of structural elements of the mature brain. In the neocortex of the adult human brain, a characteristic three-dimensional capillary angioarchitecture is observed, contrasting with the two-dimensional arrangement in the immature perinatal cortex. Abnormal OFC angioarchitecture was also found in 14% of histomorphologically investigated brains from persons with endogenous psychoses. For the pathogenesis of functional disorders of the human brain, including endogenous psychoses, knowledge about the processes of structural maturation of neurons and neuroglia, but also of capillary architecture, is essential.
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References
Bär T, Wolff JR (1972) The formation of capillary basement membranes. Internal vascularization of the rat's cerebral cortex. Z Zellforsch 132:231–248
Beckmann H, Senitz D (2002) Development malformations in cerebral structures in "endogenous psychosis". J Neural Transm 109:421–431
Damska M (1995) The vascularization of the developing human brain. Folia Neuropath 33:189–193
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137A–138A
Kedzia A, Rybaczuk M, Andrzejak R (2002) Fractal dimensions of human brain cortex vessels during the fetal period. Med Sci Monit 8: MT46–MT51
Koenderink MJT, Uylings HBM (1995) Postnatal maturation of layer V pyramidal neurons in the human prefrontal cortex. A quantitative Golgi analysis. Brain Res 678:233–243
Marin-Padilla M (1970) Prenatal and early postnatal ontogenesis of the human motor cortex. A Golgi study. I. The sequential development of the cortical layers. Brain Res 23:167–183
Marin-Padilla M (1985) Early vascularization of the embryonic cerebral cortex: golgi and electron microscopic studies. J Comp Neurol 241:237–249
Marin-Padilla M (1988) Embryonic vascularization of the mammalian cerebral cortex. In: Peters A, Jones EG (eds) Cerebral cortex: vol 7. Development and maturation of cerebral cortex. Plenum Press, New York pp 479–509
Pfeiffer A (1928) Die Angioarchitektonik des Kortex. Deutike, Leipzig
Scharf JH (1973) Forderungen an ein Modell für das intrauterine Wachstum am Beispiel Homo sapiens. Zool Jahrb Anat 90:454–482
Schierhorn H (1978) Die postnatale Entwicklung der Lamina V-Pyramidenzellen im sensomotorischen Cortex der Albinoratte. Gegenbaurs Morph Jahrb, Leipzig 124:1–42
Senitz D (1978) Über einen interkapillären Zelltyp im Hirn alter Menschen. Zbl Allg Path Pathol Anat 122:423–427
Senitz D (1981) Über strukturelle Veränderungen kortikaler Pyramidenzellen bei klinisch festgestellter Oligophrenie. Eine Golgi -Studie. Zbl Allg Path Pathol Anat 125:3–11
Senitz D (1985) The angioarchitecture of the human neocortex: normal and aberrant developmental pattern. Zbl Allg Path Pathol Anat 130:233
Senitz D (1986) Neuronenstruktur bei chronischem Alkoholismus. Eine Golgi-Studie am menschlichen Hirn. Wiss Z Friedrich-Schiller-Univ Jena Naturwiss R 35:195–202
Senitz D (1991) Neuronenveränderungen im cerebralen Cortex bei Patienten mit Alzheimer Krankheit im Vergleich zur milden Demenz und zum normalen Altern. Math Nat Wiss R 39:538–545
Senitz D (1994) Unusual morphological alterations of the radial glia cells in human perinatal neocortex. J Brain Res 35:130–132
Senitz D, Winkelmann E (1991) Neuronale Struktur-Anomalie im orbito-frontalen Cortex bei Schizophrenen. J Horsch 32:149–158
Senitz D, Kalus P, Beckmann H (1995) Two developmental stains of protoplasmatic astrocytes in the human neocortex. A Golgi-, DiI-, and confocal microscopic study. Clin Neuropath 14:286
Senitz D, Kalus P, Lauer M, Beckmann H (2000) The neuromorphology of schizophrenic psychoses. In: Franzek E, Ungvari GS, Rüther E, Beckmann H (eds) Progress in differentiated psychopathology. WKL Society, Hong Kong, pp 168–190
Streeter GL (1918) The developmental alterations in the vascular systems of the brain in the human embryo. Contrib Embryol Carnegie Inst 8:5–38
Wolff JR (1978) Ontogenetic aspects of cortical architecture: lamination. In: Brazier MAB, Petsche H (eds) Architectonics of the cerebral cortex. Raven Press, New York, pp 159–173
Wolff J R, Goerz C, Bär T, Guldner F H (1975) Common morphogenetic aspects of various organotypic microvascular patterns. Microvasc Res 10:373–395
Acknowledgements
This work was supported by the Alfred Golombek Foundation. We express our gratitude to Marion Winnig for her excellent technical assistance. Dr. Werner Ruhmann from "IMATEC Bildanalysesysteme", who installed and maintained the image analysis system; we want to thank him for his constant availability when questions concerning the system arose. Special thanks also to Renate Huttner and Dr. Paul Foley for their careful proof-reading of the manuscript.
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Senitz, D., Benninghoff, J. Histomorphology of angiogenesis in human perinatal orbitofrontal cortex: a Golgi and electron microscopic study of anastomosis formation. Anat Embryol 206, 479–485 (2003). https://doi.org/10.1007/s00429-003-0319-4
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DOI: https://doi.org/10.1007/s00429-003-0319-4