Abstract
Fibres in the mammalian optic nerve are arranged into fascicles between which there is an extra-fascicular matrix containing connective tissue, a feature similar to that found in association with fibres in peripheral nerves, but not otherwise found in the CNS. The relationship between these major features of the nerve architecture are not known. We have addressed this question by examining the fascicular organisation of the optic nerve and the distribution of connective tissue and specific collagen types in the human. We have also examined the spatial development of connective tissue in the human nerve to determine when and from where it originates. Fibres are grouped into fascicles at all locations along the nerve, except intracranially, close to the chiasm where this pattern is lost. Relatively large fascicular numbers are found directly behind the eye and in the region of the optic canal, but decline in the mid-orbital segment of the nerve. Connective tissue is present in the extra-fascicular matrix throughout the fasciculated segment, but in many cases it does not fully encircle fascicles. The proportion of matrix occupied by connective tissue is similar along the length of the nerve (approximately 60%). Within the matrix, collagen types I, III, IV, V and VI are present throughout fasciculated regions. Staining for types V and VI appeared relatively weak compared with that for the other types. Although the collagen types in the nerve are similar to those at the lamina cribrosa and in peripheral nerves, they did not appear to be differentially distributed as in regions of the PNS. Connective tissue enters the nerve at a number of wide-spread locations early in development, consistent with the notion that it enters the nerve with the blood supply. It is present within the matrix before it is established at the lamina cribrosa.
Similar content being viewed by others
References
Albon J, Karwatowski WSS, Duance VC, Bailey AJ, Easty DL (1992) Age-related changes in the collagen matrix of the human lamina cribrosa. Invest Ophthalmol Vis Sci [Suppl] 33:1092
Albon J, Purslow PP, Duance VC, Easty DL, Karwatowski WSS (1994a) Mechanical compliance of the aging human lamina cribrosa. Invest Ophthalmol Vis Sci [Suppl] 35:1645
Albon J, Purslow P, Karwatowski WSS (1994b) Age related compliance in the lamina cribrosa in human eyes. J Biomech 27:823–854
Anderson DR, Hoyt WF (1969) Ultrastructure of intraorbital portion of human and monkey optic nerve. Arch Ophthalmol 82:506–530
Baker GE (1990) Prechiasmatic reordering of fibre diameter classes in the retinofugal pathway of ferrets. Eur J Neurosci 2:24–33
Behr C (1935) Beitrag zur Anatomie und Klinik des septalen Gewebes und des Arterieneinbaus im Sehnervenstamm. Graefes Arch Clin Exp Ophthalmol 134:227–267
Clarke E, Bearn JG (1972) The spiral bands of Fontana. Brain 95:1–20
Cobin KB, Gardner ED (1937) Decrease in the number of myelinated fibres in human spinal roots with age. Anat Rec 68:63–74
Cottrell L (1940) Histologic variation with age in apparently normal peripheral nerve trunks. Arch Neurol 43:1138–1150
Culling CFA (1963) Handbook of histopathological techniques. Butterworths, London
Dolman SL, McCormick AQ, Drance SM (1980) Aging of the optic nerve. Arch Ophthalmol 98:2053–2058
Evans A, Jeffery G (1992) The fascicular organisation of the cat optic nerve. Exp Brain Res 91:79–84
Fontana F (1781) Traité sur le Venin de la Vipère sur les Poisons Americains, vol 2. Florence
Goldbaum MH, Jeng S, Logemann R, Weinreb RN (1989) The extracellular matrix of the human optic nerve. Arch Ophthalmol 107:1225–1231
Harman AM, Jeffery G (1992) Distinctive pattern of organisation in the retinofugal pathway of a marsupial. I. Retina and optic nerve. J Comp Neurol 325:47–56
Hernadez MR (1993) Glaucoma: changes in extracellular matrix in the optic nerve head. Ann Med 25:309–315
Hernadez MR, Luo DDS, Andrzejewska W, Neufeld AH (1989) Age-related changes in the extracellular matrix of the human optic nerve head. Am J Ophthalmol 107:476–484
Hollander H, Vaaland JL (1968) A reliable staining method for semi-thin sections in experimental neuroanatomy. Brain Res 10:120–126
Jeffery G (1990) Distribution of uncrossed and crossed retinofugal axons in the cat optic nerve and their relationship to patterns of fasciculation. Vis Neurosci 5:99–104
Jonas JB, Muller-Bergh JA, Schlotzer-Schrehart UM, Naumann GOH (1990) Histomorphometry of the human optic nerve. Invest Ophthalmol Vis Sci 31:736–744
Keene DR, Sakai LY, Bachinger HP, Burgeson RE (1987) Type III collagen can be present on banding fibrils regardless of fibril diameter. I Cell Biol 105:2395–2403
Liu CS, Youl B, Moseley FI (1992) Magnetic resonance imaging of the optic nerve in extremes of gaze. Implications for the positioning of the globe for retrobulba anaesthesia. Br J Ophthalmol 76:728–733
Lorimier P, Mezin P, Labat Moleur F, Pinel N, Peyrol S, Stoebner P (1992) Ultrastructural localisation of the major components of the extracellular matrix in normal rat nerve. J Histochem Cytochem 40:859–868
Maniscalco JE, Habal MB (1978) Microanatomy of the optic canal. J Neurosurg 48:402–406
Quigley HA, Dorman-Pease ME, Brown AE (1991) Quantitative study of collagen and elastin of the optic nerve head and sclera in human and experimental monkey glaucoma. Curr Eye Res 10:877–888
Reese BE (1987) The distribution of axons according to diameter in the optic nerve and optic tract of the rat. Neuroscience 22:1015–1024
Scholes J (1991) The design of the optic nerve in the fish. Vis Neurosci 7:129–139
Shellswell GB, Restall DJ, Duance VC, Bailey AJ (1979) Identification and differential distribution of collagen types in the central peripheral nervous systems. FEBS Lett 106:305–308
Sutherland S (1965) The connective tissues of peripheral nerves. Brain 88:841–854
Tansley K (1956) Comparison of the lamina cribrosa in mammalian species with good and with indifferent vision. Br J Ophthalmol 40:178–182
Unsold R, De Groot J, Newton TH (1980) Images of the optic nerve; anatomic-CT correlation. Am J Roentgenol 135:767–773
Vitellaro-Zuccarello L, Garbelli R, Dal Pozzo Rossi V (1992) Immunocytochemical localisation of collagen types I, III, IV and fibronectin in the human dermis. Modification with ageing. Cell Tissue Res 268:505–511
Walsh and Hoyt's Clinical Neuro-Ophthalmology (1982) 4th edn, vol 1 Miller NR (ed). Williams &Wilkins, Baltimore
Wilbrand HL, Saenger A (1904) Die Neurologie des Auges. Ein Handbuch fur Nerven und Augenärzte. Bergman, Wiesbaden
Wolf E (1940) The Anatomy of the eye and orbit, 2nd edn. Lewis, London
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Jeffery, G., Evans, A., Albon, J. et al. The human optic nerve: fascicular organisation and connective tissue types along the extra-fascicular matrix. Anat Embryol 191, 491–502 (1995). https://doi.org/10.1007/BF00186739
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00186739