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Design of Cerebellar and Nontegmental Rhombencephalic Microvascular Bed in the Sterlet, Acipenser ruthenus: A Scanning Electron Microscope and 3D Morphometry Study of Vascular Corrosion Casts

Published online by Cambridge University Press:  23 August 2006

Bernhard Stöttinger ,
Martin Klein ,
Bernd Minnich  and
Alois Lametschwandtner
Bernhard Stöttinger
Affiliation:
University of Salzburg, Department of Organismic Biology, Blood Vessel and Muscle Research Unit, Hellbrunnerstrasse 34, A-5020 Salzburg, Austria
Martin Klein
Affiliation:
University of Salzburg, Department of Organismic Biology, Blood Vessel and Muscle Research Unit, Hellbrunnerstrasse 34, A-5020 Salzburg, Austria
Bernd Minnich
Affiliation:
University of Salzburg, Department of Organismic Biology, Blood Vessel and Muscle Research Unit, Hellbrunnerstrasse 34, A-5020 Salzburg, Austria
Alois Lametschwandtner
Affiliation:
University of Salzburg, Department of Organismic Biology, Blood Vessel and Muscle Research Unit, Hellbrunnerstrasse 34, A-5020 Salzburg, Austria
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Abstract

The design of the microvasculature of cerebellum and nontegmental rhombencephalic areas was studied in eight adult Acipenser ruthenus L. by scanning electron microscopy of vascular corrosion casts and three-dimensional morphometry. Gross vascularization was described and diameters and total branching angles of parent and daughter vessels of randomly selected arterial and capillary bifurcations (respectively, venous mergings) were measured. With diameters ranging from 15.9 ± 1.9 μm (cerebellum; mean ± S.D.) to 15.9 ± 1.7 mm (nontegmental rhombencephalon; mean ± S.D.) capillaries in Acipenser were significantly (p ≥ .05) smaller than in cyclostomes (18–20 μm) but significantly thicker than in higher vertebrates and men (6–8 μm). With the exception of the area ratio β (i.e., sum of squared daugther diameters divided by squared diameter of parent vessel) of the venular mergings in the nontegmental rhombencephalon, no significant differences (p ≥ .05) existed between the two brain areas. Data showed that arteriolar and capillary bifurcations and venular mergings are optimally designed in respect to diameters of parent vessel to daughter vessels and to branching (merging) angles. Quantitative data are discussed both in respect to methodical pitfalls and the optimality principles possibly underlying the design of vascular bifurcations/mergings in selected brain areas of a nonteleost primitive actinopterygian fish.

Keywords

Acipenserbrainmicrovascularizationvascular castingsscanning electron microscopy3D morphometryoptimality principles
Type
BIOLOGICAL APPLICATIONS
Information
Microscopy and Microanalysis , Volume 12 , Issue 5 , October 2006 , pp. 376 - 389
Copyright
© 2006 Microscopy Society of America

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References

REFERENCES

Adam, H., Lametschwandtner, A., & Wimmer C. (1979). Hypothalamo-hypophysial relations in cyclostomes and amphibia. In Proceedings of the International Symposium on Neuroendocrinology, Belgrade, pp. 53–62.
Aharinejad, S. & Lametschwandtner, A. (1992). Microvascular Corrosion Casting in Scanning Electron Microscopy. Vienna: Springer-Verlag.
Albrecht, U., Lametschwandtner, A., & Adam, H. (1978). The vascularization of the anuran brain. The cerebellum. A scanning electron microscopical study of vascular corrosion casts. Acta Zool 59, 239–245.Google Scholar
Albrecht, U., Lametschwandtner, A., & Adam, H. (1980). The vascularization of the anuran brain. The rhombencephalon and the medulla spinalis. Acta Zool 61, 239–246.Google Scholar
Bennett, S.H., Eldridge, M.W., Zaghi, D., Zaghi, S.E., Milstein, J.M., & Goetzman, B.W. (2000). Form and function of fetal and neonatal pulmonary arterial bifurcations. Am J Physiol Heart Circ Physiol 279, H3047–H3057.Google Scholar
Boero, J.A., Ascher, J., Arregui, A., Rovainen, C., & Woolsey, T.A. (1999). Increased brain capillaries in chronic hypoxia. J Appl Physiol 86, 1211–1219.Google Scholar
Cecon, S., Minnich, B., & Lametschwandtner, A. (2002). Vascularization of the brains of the Atlantic and Pacific hagfishes, Myxine glutinosa and Eptatretus stouti: A scanning electron microscope study of vascular corrosion casts. J Morphol 253, 51–63.Google Scholar
Craigie, E.H. (1921). The vascularity of the cerebral cortex of the albino rat. J Comp Neurol 33, 193–212.Google Scholar
Craigie, E.H. (1931). The vascularity of parts of the spinal chord, brain stem, and cerebellum of the wild Norway rat (Rattus norvegicus) in comparison with that in the domesticated albino. J Comp Neurol 53, 309–318.Google Scholar
Craigie, E.H. (1938). The blood vessels of the brain substance in some amphibians. Proc Am Phil Soc 78, 615–649.Google Scholar
Craigie, E.H. (1941). Vascularization in the brains of reptiles. I. The painted turtle, Chrysemys picta marinata agassiz. J Comp Neurol 74, 247–264.Google Scholar
Dawson, T.H. (2005). Modeling of vascular networks. J Exp Biol 208, 1687–1694.Google Scholar
Demme, R. (1860). Das arterielle Gefäßsystem von Acipenser ruthenus. Inaug.-Diss. Wien.
Duvernoy, H.M., Delon, S., & Vannson, J.L. (1981). Cortical blood vessels of the human brain. Brain Res Bull 7, 519–579.Google Scholar
Duvernoy, H.M., Delon, S., & Vannson, J.L. (1983). The vascularization of the human cerebellar cortex. Brain Res Bull 11, 419–480.Google Scholar
Gössl, M., Malyar, N.M., Rosol, M., Beighley, P.E., & Ritman, E.L. (2003a). Impact of coronary vasa vasorum functional structure on coronary vessel wall perfusion structure. Am J Physiol Heart Circ Physiol 285, H2019–H2026.Google Scholar
Gössl, M., Rosol, M., Malyar, N.M., Fitzpatrick, L.A., Beighley, P.E., Zamir, M., & Ritman, E.L. (2003b). Functional anatomy and hemodynamic characteristics of vasa vasorum in the walls of porcine coronary arteries. Anat Rec 272A, 526–537.Google Scholar
Gössl, M., Zamir, M., & Ritman, E.L. (2004). Vasa vasorum growth in the coronary arteries of newborn pigs. Anat Embryol 208, 351–357.Google Scholar
Grodzinski, M.Z. (1948). The blood vessels in the brain of the sturgeon (Acipenser ruthenus L.). Bull Int Acad Polonaise Sci Lettres, B, 1–6 Bll, 61–81.Google Scholar
Hodde, K.Z. (1983). Veins of the rat brain. In The Cerebral Veins. An Experimental and Clinical Update, Auer, L.M. & Loew, F. (Eds.), pp. 85–92. New York, Berlin, Heidelberg: Springer.
Kamiya, A. & Togawa, T. (1972). Optimal branching structure of the vascular tree. Bull Math Biophys 34, 431–438.Google Scholar
Kamiya, A., Togawa, T., & Yamamoto, A. (1974). Theoretical relationship between the optimal models of the vascular tree. Bull Math Biol 36, 311–323.Google Scholar
Klein, M. (1994). Vascularization of the brain of the sterlet Acipenser ruthenus with particular emphasis on the microvascularization of the olfactory bulb. Diploma thesis. Salzburg.
Kleiter, N. & Lametschwandtner, A. (1995). The microvascularization of the cerebellum in the turtle, Pseudemys scripta elegans. A scanning electron microscope study, including stereological measurements. Anat Embryol 191, 145–153.Google Scholar
Kotrschal, K., Krautgartner, W., Lametschwandtner, A., & Adam, H. (1987a). The fine structure of neurohemal regions within the diencephalic floor of Acipenser ruthenus (Chondrostei). Wiss. Z. Karl-Marx-Univ. Leipzig, Math-Naturwiss R 36, 118–119.Google Scholar
Kotrschal, K., Krautgartner, W., Lametschwandtner, A., & Adam, H. (1987b). Brain ventricles and ependyma in the ray-finned fishes. Wiss. Z. Karl-Marx-Univ. Leipzig, Math-Naturwiss R 36, 64–66.Google Scholar
Kotrschal, K., Lametschwandtner, A., & Adam, H. (1985). Fine structure and vascular supply of the median emenence (ME) in Acipenser ruthenus (Chondrostei). J Hirnforsch 26, 333–351.Google Scholar
LaBarbera, M. (1990). Principles of design of fluid transport systems in zoology. Science 249, 992–1000.Google Scholar
Lametschwandtner, A. (1982). Das Gefäβbett des Gehirns und der Hypophyse von Myxine glutinosa L. (Cyclostomata, Myxinoides) und Bufo bufo (L.) (Amphibia, Anura). Eine rasterelektronenmikroskopische Untersuchung an Gefäßausgusspräparaten (Korrosionspräparaten). Mikroskopie 39, 35–42.Google Scholar
Lametschwandtner, A., Albrecht, U., & Adam, H. (1979a). The vascularization of the anuran brain. The choroid plexus of the fourth ventricle. A scanning electron microscopical study of the vascular corrosion casts. Acta Zool 59, 229–237.Google Scholar
Lametschwandtner, A., Albrecht, U., & Adam, H. (1979b). The vascularization of the anuran brain. The mesencephalon. A scanning electron microscopical study of vascular corrosion casts. Acta Zool 60, 89–92.Google Scholar
Lametschwandtner, A., Albrecht, U., & Adam, H. (1980a). The vascularization of the anuran brain. Olfactory bulb and telencephalon. A scanning electron microscopical study of vascular corrosion casts. Acta Zool 61, 225–238.Google Scholar
Lametschwandtner, A., Lametschwandtner, U., & Weiger, T. (1990). Scanning electron microscopy of vascular corrosion casts—Technique and applications: Updated review. Scan Microsc 4, 889–940.Google Scholar
Lametschwandtner, A., Miodonski, A., & Simonsberger, P. (1980b). On the prevention of specimen charging in scanning electron microscopy of vascular corrosion casts by attaching conductive bridges. Mikroskopie 36, 270–273.Google Scholar
Lametschwandtner, A. & Simonsberger, P. (1975). Light and scanning microcopial studies of the hypothalamo-adenohypophysial portal vessels of the toad Bufo bufo (L.). Cell Tiss Res 162, 131–139.Google Scholar
Lametschwandtner, A., Simonsberger, P., & Adam, H. (1977a). The vascularization of the neural stalk and the pars nervosa of the hypophysis in the toad Bufo bufo (L.) (Amphibia, Anura). A comparative light microscopical and scanning electron microscopical study. Cell Tiss Res 180, 433–442.Google Scholar
Lametschwandtner, A., Simonsberger, P., & Adam, H. (1977b). Vascularization of the pars intermedia of the hypophysis in the toad, Bufo bufo (L.) (Amphibia, Anura). A comparative light microscopical and scanning electron microscopical study. II. Cell Tiss Res 179, 11–16.Google Scholar
Malkusch, W., Konerding, M.A., Klapthor, B., & Bruch, J. (1995). A simple and accurate method for 3-D measurements in microcorrosion casts illustrated with tumour vascularization. Anal Cell Pathol 9, 69–81.Google Scholar
Minnich, B., Bartel, H., & Lametschwandtner, A. (2001). Quantitative microvascular corrosion casting by 2D- and 3D-morphometry. Ital J Anat Embryol 106(Suppl 1), 213–220.Google Scholar
Minnich, B., Bartel, H., & Lametschwandtner, A. (2002). How a highly complex three-dimensional network of blood vessels regresses: The gill blood vascular system of tadpoles of Xenopus during metamorphosis. A SEM study on microvascular corrosion casts. Microvasc Res 64, 425–437.Google Scholar
Minnich, B., Leeb, H., Bernroider, E.W., & Lametschwandtner, A. (1999). Three-dimensional morphometry in scanning electron microscopy: A technique for accurate dimensional and angular measurements of microstructures using stereopaired digitized images and digital image analysis. J Microsc 195, 23–33.Google Scholar
Miodonski, A., Pobrowska, A.J., & Friedhuber De Grubenthal, A. (1979). SEM study of the choroid plexus of the lateral ventricle in the rat. Anat Embryol 155, 323–331.Google Scholar
Murakami, T. (1971). Application of the scanning electron microscope to the study of the fine distribution of blood vessels. Arch Histol Jap 32, 445–454.Google Scholar
Murray, C.D. (1926a). The physiological principle of minimum work applied to the angle of branching arteries. J Gen Physiol 9, 835–841.Google Scholar
Murray, C.D. (1926b). The physiological principle of minimum work. I. The vascular system and the cost of blood volume. Proc Natl Acad Sci USA 12, 207–214.Google Scholar
Neumaier, C. & Lametschwandtner, A. (1994). The vascularization of the pituitary gland in the chicken (Gallus domesticus). A scanning electron microscope study of vascular corrosion casts. Arch Histol Cytol 57, 213–233.Google Scholar
Pfeifer, R.A. (1930). Grundlegende Untersuchungen für die Angioarchitektur des menschlichen Gehirns. Berlin: Springer.
Rashevsky, N. (1973). The principle of adequate design. In Foundations of Mathematical Biology, R. Rosen, (Ed.), vol. 3, pp. 158–167. New York: Academic Press, Inc.
Sherman, T.F., Popel, A.S., Koller, A., & Johnson, P.C. (1989). The cost of departure from optimal radii in microvascular networks. J Theor Biol 136, 245–265.Google Scholar
Splechtna, H. (1973). Die Kopfgefäße des Sterlets (Acipenser ruthenus L.) (Acipenseridae, Chondrostei). Gegenbaurs Morph Jahrb 119, 401–421.Google Scholar
Taguchi, Y., Takashima, S., Sasahara, E., Inoue, H., & Ohtani, O. (2004). Morphological changes in capillaries in the ischemic brain in Wistar rats. Arch Histol Cytol 67, 253–261.Google Scholar
Teo, E.H., Carati, C., Firth, B.T., Barbour, R.A., & Gannon, B. (1993). Vascularization of the pineal complex in the lizard Tiliqua rugosa. Anat Rec 236, 521–536.Google Scholar
Weiger, T. & Lametschwandtner, A. (1988a). The vascularization of the choroid plexus of the lateral ventricle of the turtle Pseudemys scripta elegans (Reptilia). J Zool Lond 241, 457–468.Google Scholar
Weiger, T., Lametschwandtner, A., Hodde, K., & Adam, H. (1986a). The angioarchitecure of the choroid plexus of the lateral ventricle of the rabbit. A scanning electron microscopic study of vascular corrosion casts. Brain Res 378, 285–296.Google Scholar
Weiger, T., Lametschwandtner, A., Kotrschal, K., & Krautgartner, W.D. (1988b). Vascularization of the telencephalic choroid plexus of a ganoid fish (Acipenser rutheus L.). Am J Anat 182, 33–41.Google Scholar
Weiger, T., Lametschwandtner, A., & Stockmayer, P. (1986b). Technical parameters of plastics (Mercox CL-2B and various methylmetacrylates) used in scanning electron microscopy of vascular corrosion casts. Scan Electron Microsc, 243–252.
Woldenberg, M.J. & Horsefield, K. (1983). Finding the optimal lengths for three branches at a junction. J Theor Biol 104, 301–318.Google Scholar
Zamir, M. (1976a). The role of shear forces in arterial branching. J Gen Physiol 67, 213–222.Google Scholar
Zamir, M. (1976b). Optimality principles in arterial branching. J Theor Biol 62, 227–251.Google Scholar
Zamir, M. (1978). Nonsymmetrical bifurcations in arterial branching. J Gen Physiol 72, 837–845.Google Scholar
Zamir, M. (1986). Cost analysis of arterial branching in the cardiovascular systems of man and animal. J Theor Biol 120, 111–123.Google Scholar
Zamir, M. (1988). The branching structure of arterial trees. Comments Theor Biol 1, 15–37.Google Scholar
Zamir, M. & Bigelow, D.C. (1984). Cost of departure in arterial branching. J Theor Biol 109, 401–409.Google Scholar
Zamir, M., Medeiros, J.A., & Cunningham, T.K. (1979). Arterial bifurcations in the human retina. J Gen Physiol 74, 537–548.Google Scholar
Zamir, M., Wrigley, S.M., & Langille, B.L. (1983). Arterial bifurcations in the cardiovascular system of a rat. J Gen Physiol 81, 325–335.Google Scholar