Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T14:57:19.307Z Has data issue: false hasContentIssue false

Three-Dimensional Morphological Characterization of Optic Nerve Fibers by Atomic Force Microscopy and by Scanning Electron Microscopy

Published online by Cambridge University Press:  07 July 2005

Mahmoud Melling
Affiliation:
Department of Anatomy, University of Vienna, Vienna, Austria
Daniela Karimian-Teherani
Affiliation:
Department of Dermatology, Medical School of Vienna, Vienna, Austria
Sascha Mostler
Affiliation:
Department of Anatomy, University of Vienna, Vienna, Austria
Sonja Hochmeister
Affiliation:
Institute of Brain Research, University of Vienna, Vienna, Austria
Get access

Abstract

A comparative study of scanning electron microscopy (SEM) and atomic force microscopy (AFM) imaging of the healthy human optic nerve was carried out to determine the similarities and the differences. In this study we compared the fine optic nerve structures as observed by SEM and AFM. The fibers of the right optic nerve of a 61-year-old man show different arrangements in transverse sections taken from the same individual 5 mm central to the optic canal and 5 mm peripheral to the optic chiasma; this difference can be recognized by light microscopy (LM), SEM, and AFM. AFM revealed such typical optic nerve fibers (taken from a point 5 mm central to the optic canal) with annular and longitudinal orientations, which were not visible by SEM in this form. By contrast, LM and SEM visualized other structures, such as pia mater and optic nerve fibers loosely arranged in bundles, none of which was visualized by AFM. The images, however, taken 5 mm peripheral from the optic chiasma show shapeless nerve fibers having a wavy course. Our results reveal that more detailed information on optic nerve morphology is obtained by exploiting the advantages of both SEM and AFM. These are the first SEM and AFM images of healthy human optic nerve fibers, containing clear representations of the three dimensions of the optic nerve.

Type
BIOLOGICAL APPLICATIONS
Copyright
© 2005 Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aragno, I., Odetti, P., Altamura, F., Cavalleri, O., & Rolandi, R. (1995). Structure of rat tail tendon collagen examined by atomic force microscope. Experientia 51, 10631067.Google Scholar
Birch, M., Brotschie, D., Roberts, N., & Grierson, I. (1997). The three-dimensional structure of the connective tissue in the lamina cribrosa of the human optic nerve head. Ophthalmology 211, 183191.Google Scholar
Bonfiglio, A., Parodi, M.T., & Tonini, G.P. (1995). Subcellular details of early events of differentiation induced by retinoic acid in human neuroblastoma cells detected by atomic force microscopy. Exp Cell Res 216, 7379.Google Scholar
Braet, F., de Zanger, R., & Wisse E. (1997). Drying cells for SEM, AFM and TEM by hexamethyldisilazane: A study on hepatic endothelial cells. J Microsc 186, 8487.Google Scholar
Braet, F., Seynaeve, C., de Zanger, R., & Wisse, E. (1998). Imaging surface and submembranous structures with the atomic force microscope: A study on living cancer cells, fibroblasts and macrophages. J Microsc 190, 328338.Google Scholar
Bumke, O. & Foerster, O. (1935). Handbuch der Neurologie. Allgemeine Neurologie I, Anatomie. Erster Band, p. 236. Berlin: Springer.
Bustamante, C. & Keller, D. (1995). Scanning force microscopy in biology. Phys Today 48, 3238.Google Scholar
Bustamante, C., Keller, D., & Yang, G. (1993). Scanning force microscopy of nucleid acids and nucleoprotein assemblies. Curr Opin Struct Biol 3, 363372.Google Scholar
Bustamante, C. & Rivetti, C. (1996). Visualizing protein–nucleic acid interactions on a large scale with the scanning force microscope. Annu Rev Biophys Biomol Struct 25, 395429.Google Scholar
Bustamante, C., Vesenka, J., Tang, C.L., Rees, W., Guthold, M., & Keller, R. (1992). Circular DNA molecules imaged in air by scanning force microscopy. Biochemistry 3, 2226.Google Scholar
Cricenti, A., de Stasio, G., Generosi, R., Perfetti, P., Ciotti, M.T., & Mercanti, D. (1995). Atomic force microscopy of neuron networks. Scanning Microsc 9, 695699.Google Scholar
De Stasio, G., Cricenti, A., Generosi, R., Mercanti, D., Ciotti, M.T., Casalbore, P., Margaritondo, G., & Perfetti, P. (1995). Neurone decapping characterization by atomic force microscope: A topological systematic analysis. Neuroreport 7, 6568.Google Scholar
El Shoura, S.M. (1993). Falciparum malaria in naturally infected human patients: IV—Ultrastructural changes in peripheral white blood cells. Ann Parasit Human Com 68, 169175.Google Scholar
Firbas, W., Gruber, H., & Mayr, R. (1995). Neuroanatomie. 2. überarbeitete Auflage, pp. 181182. Wien, München, Bern: Maudrich.
Henderson, E., Haydon, P.G., & Sakaguchi, D.S. (1992). Actin filament dynamics in living glial cells imaged by atomic force microscopy. Science 257, 19441946.Google Scholar
Hoh, J.H. & Schönenberger, C.A. (1994). Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy. J Cell Sci 107, 11051114.Google Scholar
Isrealachvili, J. (1992). Intermolecular and surface forces, p. 450. New York: Academic.
Lillehei, P.T. & Bottomley, L.A. (2000). Scanning probe microscopy. Anal Chem 72, 189R196R.Google Scholar
Matsui, I., Tanimura, M., Kobayashi, N., Sawada, T., Nagahara, N., & Akatsuka, J. (1993). Neurofibromatosis type 1 and childhood cancer. Cancer 72, 27462754.Google Scholar
Melling, M., Hochmeister, S., Blumer, R., Schilcher, K., Mostler, S., Behnam, M., Wilde, J., & Karimian-Teherani, D. (2001). Atomic force microscopy imaging of the human trigeminal ganglion. Neuroimage 14, 13481352.Google Scholar
Melling, M., Karimian-Teherani, D., Behnam, M., & Mostler, S. (2003). Morphological study of the healthy human oculomotor nerve by atomic force microscopy. NeuroImage 20, 795801.Google Scholar
Nagayama, S., Morimoto, M., Kawanata, K., Fujito, Y., Ogura, S., Abe, K., Ushiki, T., & Ito, E. (1996). AFM observation of three-dimensional fine structural changes in living neurons. Bioimages 4, 111116.Google Scholar
Nagayama, S., Tojima, T., Morimoto, M., Sasaki, S., Kawabata, K., Ushiki, T., Abe, K., & Ito, K. (1997). Practical scan speed in atomic force microscopy for live neurons in a physiological solution. Jpn J Appl Phys 36, 38773880.Google Scholar
Nesic, M., Klinger, M., Katuic, D., & Curkovic, T. (1990). Retinoblastoma. Acta Med Iug 44, 44445.Google Scholar
Oberleithner, H., Schneider, S., Larmer, J., & Henderson, R.M. (1996). Viewing the renal epithelium with the atomic force microscope. Kid Blood Pres Res 19, 142147.Google Scholar
Onken, C., Guthoff, R., & Abramo, F. (1989). Neue diagnostische Ansätze zur Abklärung des verbreiterten Nervus opticus-Vergleiche zwischen Ultraschallechographie und Kernspintomographie. Fort Ophthal 86, 352355.Google Scholar
Osada, T., Arakawa, H., Ichikawa, M., & Ikai, A. (1998). Atomic force microscopy of histological sections using a new electron beam etching method. J Microsc 189, 4349.Google Scholar
Parpura, V., Haydon, P.G., & Henderson, E. (1993). Three-dimensional imaging of living neurons and glia with the atomic force microscope. J Cell Sci 104, 427432.Google Scholar
Poletti, G., Orsini, F., Lenardi, C., & Barborini, E. (2003). A comparative study between AFM and SEM imaging on human scalp hair. J Microsc 211, 249255.Google Scholar
Radmacher, M., Tillmann, R.W., Fritz, M., & Gaub, H.E. (1992). From molecules to cells: Imaging soft samples with the atomic force microscope. Science 257, 19001905.Google Scholar
Rugar, D. & Hansma, P.K. (1990). Atomic force microscopy. Phys Today 43, 2330.Google Scholar
Sarid, D. (1991). Scanning Force Microscopy with Applications to Electric, Magnetic, and Atomic Forces, p. 253. New York: Oxford University Press.
Shroff, S.G., Saner, D.R., & Lal, R. (1995). Dynamic micromechanical properties of cultured rat atrial myocytes measured by atomic force microscopy. Am J Physiol C 269, 286292.Google Scholar
Strek, P., Strek, W., Nowogrodzka-Zagorska, M., & Pitynski, K. (1996). Angiomorphology of the retrobulbar part of the optic nerve. A scanning electron microscopy of vascular casts. Folia Morphol 55, 143150.Google Scholar
Thale, A., Tillmann, B., & Rochels, R. (1996). SEM studies of the collagen architecture of the human lamina cribrosa: Normal and pathological findings. Ophthalmology 210, 142147.Google Scholar
Thundat, T., Allison, D.P., Warmack, R.J., & Ferrel, T.L. (1992). Imaging isolated strands of DNA molecules by atomic force microscopy. Ultramicroscopy 42–44, 11011106.Google Scholar
Tojima, T., Yamane, Y., Takagi, H., Takeshita, T., Sugiyama, T., Haga, H., Kawabata, K., Ushiki, T., Abe, K., Yoshioka, T., & Ito, E. (2000). Three-dimensional characterization of interior structures of exocytotic apertures of nerve cells using atomic force microscopy. Neuroscience 101, 471481.Google Scholar
Ushiki, T. (2001). Atomic force microscopy and its related techniques in biomedicine. Ital J Anat Embryol 106, 38.Google Scholar
Ushiki, T., Hitomi, J., Ogura, S., Umemoto, T., & Shigeno, M. (1996). Atomic force microscopy in histology and cytology. Arch Histol Cytol 59, 421431.Google Scholar
Ushiki, T., Hoshi, O., Iwai, K., Kimura, E., & Shigeno, M. (2002). Arch Histol Cytol 65, 377390.
Wang, P.J., Tseng, C.L., Young, C., Liu, H.M., Chang, Y.C., Shen, Y.Z., & Lee, C.Y. (1995). Multiple sclerosis in children: Clinical, neuroimaging, and neurophysiological correlations. Zhonghua Min Guo Xiao Er Ke Yi Xue Hui Za Zhi 36, 93100.Google Scholar
Yamane, Y., Hatakeyama, D., Tojima, T., Kawabata, K., Ushiki, T., Ogura, S., Abe, K., & Ito, E. (1998). Fine surface images that reflect cytoskeletal structures in cultured glial cells by atomic force microscopy. Jpn J Appl Phys 37, 38493854.Google Scholar
Yamane, Y., Shiga, H., Haga, H., Kawabata, K., Abe, K., & Ito, E. (2000). Quantitative analyses of topography and elasticity of living and fixed astrocytes. J Electron Microsc 49, 463471.Google Scholar
Yamashina, S. & Shigeno, M. (1995). Application of atomic force microscopy to ultrastructural and histochemical studies of fixed and embedded cells. J Electron Microsc 44, 462466.Google Scholar
Zachee, P., Snauwaert, J., Vandenberghe, P., Hellemans, L., & Boogaerts, M. (1996). Imaging red blood cells with the atomic force microscope. Br J Haematol 95, 472481.Google Scholar