Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-06-06T06:37:01.661Z Has data issue: false hasContentIssue false

Retinal ganglion cell axon diameter spectrum of the cat: Mean axon diameter varies according to retinal position

Published online by Cambridge University Press:  02 June 2009

Thomas Fitzgibbon
Affiliation:
Department of Clinical Ophthalmology, Sydney University, NSW, Australia
K. Funke
Affiliation:
Abteilung für Neurophysiologie, Ruhr-Universität Bochum, Federal Republic of Germany

Abstract

Axon diameters of retinal ganglion cells were measured from electron micrographs of the nerve fiber layer of the cat. Three adult retinae were examined which had mean axonal diameters of 1.18 ± 0.86 (n = 5553), 1.12 ± 0.79 (n = 7265), and 1.47 ±1.11 μm (n = 10,867). Cumulative histograms from several locations adjacent to the optic disc were unimodal (modal peaks: 0.6–0.8 μm). This unimodal distribution, however, did not reflect the regional differences in axonal diameters found throughout the retina. In many locations, especially those related to axons of the temporal retina, axon diameter distributions were clearly bimodal or even trimodal (modal peaks: 0.6–0.8, 1.4–2.1, and 3.3 μm). Measurements from one retina indicated that the mean diameters of axons arising from the area centralis and visual streak (0.94 ± 0.63 and 0.98 ± 0.68, respectively) were not significantly different from each other; however, when compared to other areas around the optic disc, the percentage of fibers with diameters between 1.5–2.0 μm was highest in the sample adjacent to the area centralis. Axons temporal to the optic disc were found to be on average larger than those nasal to the optic disc; similarly superior axons were larger than inferior axons. Axonal distributions at the retinal periphery were found to be significantly different from those at the optic disc (p ≤ 0.05) and contained a higher percentage of medium-sized axons and fewer small axons. In each of the three retinae the proportions small, medium, and large axons were respectively γ: 46; 47; 48, β: 50; 49; 48, and α: 4; 4; 4; regional differences in the proportions of each axonal class are compared to previously published ganglion cell density maps. Differences between axonal bundles within each sample location were not significantly different; however, in one retina axons in the scleral half of the fiber layer were significantly larger (P ≤ 0.01) than axons in the vitreal half of the nerve fiber layer adjacent to the optic disc. When compared to the axonal diameter distributions found within the optic nerve (Cottee et al., 1991) and optic tract (Reese et al., 1991), our data indicates that the diameter of retinal axons may increase by up to 30% along the length of the visual pathway.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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

Baker, G.E. & Stryker, M.P. (1990). Retinofugal fibres change conduction velocity and diameter between the optic nerve and tract in ferrets. Nature 344, 342345.CrossRefGoogle ScholarPubMed
Bishop, P.O., Jeremy, D. & Lance, J.W. (1953). The optic nerve. Properties of a central tract. Journal of Physiology (London) 121, 415432.CrossRefGoogle ScholarPubMed
Bishop, G.H. & Clare, M.H. (1955). Organization and distribution of fibers in the optic tract of the cat. Journal of Comparative Neurology 103, 269304.CrossRefGoogle ScholarPubMed
Bishop, G.H., Clare, M.H. & Landau, W.M. (1969). Further analysis of fiber groups in the optic tract of the cat. Experimental Neurology 24, 386399.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 240, 397419.CrossRefGoogle ScholarPubMed
Burke, W., Burne, J. A. & Martin, P. (1985). Selective block of Y optic nerve fibres in the cat and the occurrence of inhibition in the lateral geniculate nucleus. Journal of Physiology (London) 364, 8192.CrossRefGoogle Scholar
Cottee, L.J., FitzGibbon, T, Westland, K. & Burke, W. (1991). Long survival of retinal ganglion cells in the cat after selective crush of the optic nerve. European Journal of Neuroscience 3, 12451254.CrossRefGoogle ScholarPubMed
Donovan, A. (1967). The nerve fibre composition of the cat optic nerve. Journal of Anatomy 101, 111.Google ScholarPubMed
FitzGibbon, T. & Burke, W. (1989). Representation of the temporal raphe within the optic tract of the cat. Visual Neuroscience 2, 255267.CrossRefGoogle ScholarPubMed
FitzGibbon, T, Funke, K. & Eysel, U. Th. (1991). Anatomical correlations between soma size, axon diameter and intraretinal length for the alpha ganglion cells of the cat retina. Visual Neuroscience 6, 159174.CrossRefGoogle ScholarPubMed
FitzGibbon, T. & Funke, K. (1992). Axon diameter, intraretinal length and temporal compensation: Are they related? Proceedings of the Australian Neuroscience Society 3, 172.Google Scholar
FitzGibbon, T. & Reese, B.E. (1992). Position of growth cones within the nerve fibre layer of fetal ferrets. Journal of Comparative Neurology 323, 153166.CrossRefGoogle ScholarPubMed
Freeman, B. (1978). Myelin sheath thickness and conduction latency groups in the cat optic nerve. Journal of Comparative Neurology 181, 183196.CrossRefGoogle ScholarPubMed
Freidlander, M.J., Lin, C.S., Stanford, L.R. & Sherman, S.M. (1981). Morphology of functionally identified neurons in lateral geniculate nucleus of cat. Journal of Neurophysiology 46, 80129.CrossRefGoogle Scholar
Fuentes, C., Roch, G. & Marty, R. (1979). Le nerf optique du chat 1. Aspects quantitatifs chez l'animal adulte. Acta anatomica 105, 314325.CrossRefGoogle Scholar
Fukuda, Y., Hsiao, C-F., Watanabe, M. & Ito, H. (1984). Morphological correlates of physiologically identified Y-, X-, and W-cells in cat retina. Journal of Neurophysiology 52, 9991013.CrossRefGoogle Scholar
Fukuda, Y. & Stone, J. (1974). Retinal distribution and central projections of Y-, X- and W- cells of the cat's retina. Journal of Neurophysiology 37, 749772.CrossRefGoogle Scholar
Funke, K., Eysel, U.Th. & FitzGibbon, T. (1991). Contribution of NMDA and non-NMDA receptors to retinogeniculate transmission of single and repetitive visual responses in the cat. Brain Research 547, 229238.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1970). The laminar distribution of retinal fibers in the dorsal lateral geniculate nucleus of the cat: A new interpretation. Journal of Comparative Neurology 138, 339368.CrossRefGoogle Scholar
Guillery, R.W., Polley, E.H. & Torrealba, F. (1982). The arrangements of axons according to fiber diameter in the optic tract of the cat. Journal of Neuroscience 2, 714721.CrossRefGoogle ScholarPubMed
Hsiao, C-F., Watanabe, M. & Fukuda, Y. (1984). The relation between axon diameter and axonal conduction velocity of Y, X and W cells in the cat retina. Brain Research 309, 357361.CrossRefGoogle Scholar
Hughes, A. (1975). A quantitative analysis of the cat retinal ganglion cell topography. Journal of Comparative Neurology 163, 107128.CrossRefGoogle ScholarPubMed
Hughes, A. (1981). Population magnitudes and distribution of the major modal classes of cat retinal ganglion cell as estimated from HRP filling and a systematic survey of the soma diameter spectra for classical neurones. Journal of Comparative Neurology 197, 303339.CrossRefGoogle Scholar
Hughes, A. & Wässle, H. (1976). The cat optic nerve: Fiber total count and diameter spectrum. Journal of Comparative Neurology 69, 171184.CrossRefGoogle Scholar
Hughes, A., Caille, D. & Vibert, J.F. (1980). A statistical analysis and comparison of soma diameter spectra for classical neurones from different regions of the cat retinal ganglion cell layer. Pflügers Archives 388, 239242.CrossRefGoogle Scholar
Illing, R.B. & Wässle, H. (1981). The retinal projections to the thalamus in the cat: A quantitative investigation and a comparison of the retinotectal pathway. Journal of Comparative Neurology 202, 265285.CrossRefGoogle Scholar
Kalil, R. (1978). Development of the dorsal lateral geniculate nucleus in the cat. Journal of Comparative Neurology 182, 265292.CrossRefGoogle ScholarPubMed
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A golgi study. Vision Research 21, 10811114.CrossRefGoogle ScholarPubMed
Leventhal, A.G. (1982). Morphology and distribution of retinal ganglion cells projecting to different layers of the dorsal lateral geniculate nucleus in normal and Siamese cats. Journal of Neuroscience 2, 10241042.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1985). Central projections of cat retinal ganglion cells. Journal of Comparative Neurology 237, 216226.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Ault, S.J., Vitek, D.J. & Shou, T. (1988). Extrinsic determinants of retinal ganglion cell structure in the cat. Journal of Comparative Neurology 286, 170189.CrossRefGoogle Scholar
Murakami, D., Sesma, M.A. & Rowe, M.H. (1982). Characteristics of nasal and temporal retina in Siamese and normally pigmented cats: Ganglion cell composition, axon trajectory and laterality of projection. Brain Behaviour and Evolution 21, 67113.CrossRefGoogle ScholarPubMed
Naito, J. (1986). Course of retinogeniculate projection fibers in the cat optic nerve. Journal of Comparative Neurology 251, 376387.CrossRefGoogle ScholarPubMed
Ogden, T.E. (1983 a). Nerve fiber layer of the Macaque retina: Retino-topic organization. Investigative Ophthalmology and Visual Science 24, 8598.Google Scholar
Ogden, T.E. (1983 b). Nerve fiber layer of the Owl monkey retina: Ret-inotopic organization. Investigative Ophthalmology and Visual Science 24, 265269.Google ScholarPubMed
Ogden, T.E. (1984). Nerve fiber layer of the primate retina: Morpho-metric analysis. Investigative Ophthalmology and Visual Science 25, 1929.Google Scholar
Peichl, L. (1991). Alpha ganglion cells in mammalian retinae: Common properties, species differences, and some comments on other ganglion cells. Visual Neuroscience 7, 155169.CrossRefGoogle ScholarPubMed
Polyak, S.L. (1957). The Vertebrate Visual System. Chicago, Illinois: University of Chicago Press.Google Scholar
Reese, B.E. & Baker, G.E. (1990). The course of fibre diameter classes through the chiasmatic region in the ferret. European Journal of Neuroscience 2, 3449.CrossRefGoogle ScholarPubMed
Reese, B.E., Guillery, R.W., Marzi, C.A. & Tassinari, G. (1991). Position of axons in the cat's optic tract in relation to their retinal origin and chiasmatic pathway. Journal of Comparative Neurology 306, 539553.CrossRefGoogle ScholarPubMed
Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 1, 208212.CrossRefGoogle Scholar
Rowe, M.H. & Stone, J. (1976 a). Conduction velocity groupings among axons of cat retinal ganglion cells, and their relationship to retinal topography. Experimental Brain Research 25, 339357.CrossRefGoogle Scholar
Rowe, M.H. & Stone, J. (1976 b). Properties of ganglion cells in the visual streak of the cat's retina. Journal of Comparative Neurology 169, 99126.CrossRefGoogle ScholarPubMed
Stanford, L.R. (1987 a). W-cells in the cat retina: Correlated morphological and physiological evidence for two distinct classes. Journal of Neurophysiology 57, 218244.CrossRefGoogle ScholarPubMed
Stanford, L.R. (1987 b). Conduction velocity variations minimize conduction time differences among retinal ganglion cell axons. Science 238, 358360.CrossRefGoogle ScholarPubMed
Stone, J. & Fukuda, Y. (1974). The naso-temporal division of the cat's retina reexamined in terms of Y-, X- and W-cells. Journal of Comparative Neurology 155, 377394.CrossRefGoogle Scholar
Stone, J. (1978). The number and distribution of ganglion cells in the cat's retina. Journal of Comparative Neurology 180, 753772.CrossRefGoogle ScholarPubMed
Stone, J. & Holländer, H. (1971). Optic nerve axon diameters measured in the cat retina: Some functional considerations. Experimental Brain Research 13, 498503.CrossRefGoogle ScholarPubMed
Stone, J. & Campion, J.E. (1978). Estimate of the number of myelinated axons in the cat's optic nerve. Journal of Comparative Neurology 180, 799806.CrossRefGoogle ScholarPubMed
Stone, J. & Clarke, R. (1980). Correlation between soma size and dendritic morphology in cat retinal ganglion cells: Evidence of further variation in the g-cell class. Journal of Comparative Neurology 192, 211217.CrossRefGoogle Scholar
Stone, J. & Keens, J. (1980). Distribution of small and medium-sized ganglion cells in the cat's retina. Journal of Comparative Neurology 192, 235246.CrossRefGoogle ScholarPubMed
Stone, J., Leventhal, A., Watson, C.R.R., Keens, J. & Clarke, R. (1980). Gradients between nasal and temporal areas of the cat retina in the properties of retinal ganglion cells. Journal of Comparative Neurology 192, 219233.CrossRefGoogle ScholarPubMed
Taylor, S.F. & FitzGibbon, T. (1994). Are the human retinal fibre layer and optic nerve retinotopically ordered? Proceedings of the Australian Neuroscience Society 5, 212.Google Scholar
Vaney, D.I. (1980). A quantitative comparison between the ganglion cell populations and axonal outflows of the visual streak and periphery of the rabbit retina. Journal of Comparative Neurology 189, 215233.CrossRefGoogle ScholarPubMed
Wässle, H. & Illing, R.-B. (1980). The retinal projection to the superior colliculus in the cat: a quantitative study with HRP. Journal of Comparative Neurology 190, 333356.CrossRefGoogle Scholar
Wässle, H., Levick, W.R. & Cleland, B.G. (1975 a). The distribution of the alpha type ganglion cells in the cat's retina. Journal of Comparative Neurology 159, 419438.CrossRefGoogle ScholarPubMed
Wässle, H., Levick, W.R., Kirk, D.L. & Cleland, B.G. (1975 b). Axonal conduction velocity and perikaryal size. Experimental Neurology 49, 246251.CrossRefGoogle ScholarPubMed
Wässle, H., Peichl, L. & Boycott, B.B. (1981 a). Morphology and topography of on- and off-alpha cells in the cat retina. Proceedings of the Royal Society B (London) 212, 157175.Google Scholar
Wässle, H., Boycott, B.B. & Illing, R.B. (1981 b). Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations. Proceedings of the Royal Society B (London) 212, 177195.Google Scholar
Williams, R.W. & Chalupa, L.M. (1983). An analysis of axon caliber within the optic nerve of the cat: Evidence of size grouping and regional organization. Journal of Neuroscience 3, 15541564.CrossRefGoogle ScholarPubMed
Wong, R.O.L. & Hughes, A. (1987). The morphology, number, and distribution of a large population of confirmed displaced amacrine cells in the adult cat retina. Journal of Comparative Neurology 255, 159177.CrossRefGoogle ScholarPubMed