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Soma and axon diameter distributions and central projections of ferret retinal ganglion cells

Published online by Cambridge University Press:  02 June 2009

T. Fitzgibbon ,
R. J. Wingate  and
I. D. Thompson
T. Fitzgibbon
Affiliation:
Department of Clinical Ophthalmology, Sydney University, Australia
R. J. Wingate
Affiliation:
University Laboratory of Physiology, University of Oxford, Oxford, UK
I. D. Thompson
Affiliation:
University Laboratory of Physiology, University of Oxford, Oxford, UK
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Abstract

Using a combination of retrograde horseradish peroxidase (HRP) labelling, silver staining, and electron microscopy, we have assessed the relationship between retinal ganglion cell soma size and axon diameter in the adult ferret (Mustela putorius furo). Retinal ganglion cells were labelled following injections of HRP into the lateral geniculate nucleus (LGN), superior colliculus (SC), or LGN+SC. The soma size distributions following LGN, SC, or LGN+SC injections were all unimodal showing considerable overlap between different cell classes. This was confirmed for alpha cells, identified on the basis of dendritic filling or from neurofibrillar-stained retinae. Analysis of the soma size and axon diameters of a population of heavily labelled retinal ganglion cells showed a significant correlation between the two. However, the overall distribution of intraretinal axon diameter was bimodal with an extended tail. Analysis of the ganglion cell distributions in the adult ferret indicates that beta cells comprise about 50.5–55%, gamma 42.5–47%, and alpha 2.5% of the ganglion cell population. This implies that the proportion of gamma, beta, alpha cells in both cat and ferret retina is highly conserved despite differences in visual specialization in the two species.

Keywords

HRPElectron microscopyLGNSCSoma-axon correlation
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 4 , July 1996 , pp. 773 - 786
Copyright
Copyright © Cambridge University Press 1996

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References

Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Baker, G.E. (1990). Prechiasmatic reordering of fibre diameter classes in the retinofugal pathway of ferrets. European Journal of Neuroscience 2, 24–33.CrossRefGoogle ScholarPubMed
Baker, G.E. & Stryker, M.P. (1990). Retinofugal fibres change conduction velocity and diameter between the optic nerve and tract in ferrets. Nature 344, 342–345.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, 386–399.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, 397–419.CrossRefGoogle ScholarPubMed
Chalupa, L.M. & Dreher, B. (1991). High precision systems require high precision “blue prints”: A new view regarding the formation of connections in the mammalian visual system. Journal of Cognitive Neuroscience 3, 209–219.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, 1245–1254.CrossRefGoogle ScholarPubMed
Cucchiaro, J.B. (1991). Early development of the retinal line of decussation in normal and albino ferrets. Journal of Comparative Neurology 312, 193–206.CrossRefGoogle ScholarPubMed
Donovan, A. (1967). The nerve fibre composition of the cat optic nerve. Journal of Anatomy 101, 1–11.Google ScholarPubMed
Dräger, U.C. & Olsen, J.F. (1980). Origins of crossed and uncrossed retinal projections in pigmented and albino mice. Journal of Comparative Neurology 191, 383–412.CrossRefGoogle ScholarPubMed
FitzGibbon, T. (1982). A simple method of obtaining retinal wholemounts. Vision Research 22, 1221–1223.CrossRefGoogle Scholar
FitzGibbon, T. & Funke, K. (1994). Retinal ganglion cell axon diameter spectrum in the cat: Mean diameter varies according to retinal position. Visual Neuroscience 11, 425–439.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, 159–174.CrossRefGoogle ScholarPubMed
Freeman, B. (1978). Myelin sheath thickness and conduction latency groups in the cat optic nerve. Journal of Comparative Neurology 181, 183–196.CrossRefGoogle ScholarPubMed
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, 749–772.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, 999–1013.CrossRefGoogle Scholar
Henderson, Z. (1985). Distribution of ganglion cells in the retina of adult pigmented ferret. Brain Research 358, 221–228.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, 357–361.CrossRefGoogle Scholar
Hughes, A. (1975). A quantitative analysis of the cat retinal ganglion cell topography. Journal of Comparative Neurology 163, 107–128.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, 303–339.CrossRefGoogle Scholar
Hughes, A. & Wässle, H. (1976). The cat optic nerve: Fiber total count and diameter spectrum. Journal of Comparative Neurology 69, 171–184.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 Archive 388, 239–242.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, 265–285.CrossRefGoogle Scholar
Kirby, M., Clift-Forsberg, L., Wilson, P.D. & Rapisardi, S.C. (1982). Quantitative analysis of the optic nerve of the North American opossum (Didelphis virginiana): An electron microscope study. Journal of Comparative Neurology 211, 318–327.CrossRefGoogle Scholar
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, 1025–1042.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1985). Central projections of cat retinal ganglion cells. Journal of Comparative Neurology 237, 216–226.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, 170–189.CrossRefGoogle Scholar
Morgan, J.E., Henderson, Z. & Thompson, I.D. (1987). Retinal decussation patterns in pigmented and albino ferrets. Neuroscience 20, 519–535.CrossRefGoogle ScholarPubMed
Moriya, T. & Yamadori, T. (1993). Correlative study of the morphology and central connections of ipsilaterally projecting retinal ganglion cells in the albino rat. Experimental Eye Research 56, 79–83.CrossRefGoogle ScholarPubMed
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, Behavior, and Evolution 21, 67–113.Google ScholarPubMed
Ogden, T.E. (1984). Nerve fiber layer of the primate retina: Morpho-metric analysis. Investigative Ophthalmology and Visual Science 25, 19–29.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, 155–169.CrossRefGoogle ScholarPubMed
Peichl, L., Ott, H. & Boycott, B.B. (1987). Alpha ganglion cells in mammalian retinae. Proceedings of the Royal Society B (London) 231, 169–197.Google ScholarPubMed
Rapaport, D.H., Wilson, P.D. & Rowe, M.H. (1981). The distribution of ganglion cells in the retina of the North American opossum (Didelphis virginiana). Journal of Comparative Neurology 199, 465–480.CrossRefGoogle ScholarPubMed
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, 34–49.CrossRefGoogle ScholarPubMed
Reese, B.E., Thompson, W.F. & Peduzzi, J.D. (1994). Birthdates of neurons in the retinal ganglion cell layer of the ferret. Journal of Comparative Neurology 341, 464–475.CrossRefGoogle ScholarPubMed
Rowe, M.H., Wilson, P.D. & Rapaport, D.H. (1981). Conduction velocity groups in the optic nerve of the North American opossum (Didelphis virginiana): Retinal origins and central projections. Journal of Comparative Neurology 199, 481–493.CrossRefGoogle ScholarPubMed
Sanchez, R.M., Dunkelberger, G.R. & Quigley, H.A. (1986). The number and diameter distribution of axons in the monkey optic nerve. Investigative Ophthalmology and Visual Science 27, 1342–1350.Google ScholarPubMed
Silveira, L.C.L. & Perry, V.H. (1990). A neurofibrillar staining method for retina and skin: A simple modification for improved staining and reliability. Journal of Neuroscience Methods 33, 11–21.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, 218–244.CrossRefGoogle ScholarPubMed
Stanford, L.R. (1987 b). Conduction velocity variations minimize conduction time differences among retinal ganglion cell axons. Science 238, 358–360.CrossRefGoogle ScholarPubMed
Stein, J.J. & Berson, D.M. (1995). On the distribution of gamma cells in the cat retina. Visual Neuroscience 12, 687–700.CrossRefGoogle ScholarPubMed
Stone, J. & Holländer, H. (1971). Optic nerve axon diameters measured in the cat retina: some functional considerations. Experimental Brain Research 13, 498–503.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, 377–394.CrossRefGoogle Scholar
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, 211–217.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, 235–246.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, 219–233.CrossRefGoogle ScholarPubMed
Thompson, I.D. (1991). Considering the evolution of vertebrate retina. In The Encyclopedia of Visual Function and Dysfunction. Vol. 2: Evolution of the Eye and Visual System, ed. Cronly-Dillon, J.R. & Gregory, R.L., pp. 136–151Macmillan Press.Google Scholar
Thompson, I.D., Jefferey, G., Morgan, J.E. & Baker, G. (1991). Albino gene dosage and retinal decussation patterns in the pigmented ferret. Visual Neuroscience 6, 393–398.CrossRefGoogle ScholarPubMed
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, 215–233.CrossRefGoogle ScholarPubMed
Vaney, D.I. & Hughes, A. (1976). The rabbit optic nerve: Fibre diameter spectrum, fibre count, and comparison with a retinal ganglion cell count. Journal of Comparative Neurology 170, 241–252.CrossRefGoogle ScholarPubMed
Vitek, D.J., Schall, J.D. & Leventhal, A.G. (1985). Morphology, central projections, and dendritic field orientation of retinal ganglion cells in the ferret. Journal of Comparative Neurology 241, 1–11.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, 333–356.CrossRefGoogle Scholar
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, 157–175.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, 177–195.Google 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, 419–438.CrossRefGoogle ScholarPubMed
Wässle, H., Levick, W.R., Kirk, D.L. & Cleland, B.G. (1975 b). Axonal conduction velocity and perikaryal size. Experimental Neurology 49, 246–251.CrossRefGoogle ScholarPubMed
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, 1554–1564.CrossRefGoogle ScholarPubMed
Wingate, R.J.T. & Thompson, I.D. (1995). Axonal target choice and dendritic development of beta retinal ganglion cells in the ferret. European Journal of Neuroscience 7, 723–731.CrossRefGoogle ScholarPubMed
Wingate, R.J.T., FitzGibbon, T. & Thompson, I.D. (1992). Lucifer yellow, retrograde tracers and fractal analysis characterise adult ferret retinal ganglion cells. Journal of Comparative Neurology 323, 449–474.CrossRefGoogle ScholarPubMed