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Ultrastructural study of the optic nerve in blind mole-rats (Spalacidae, Spalax)

Published online by Cambridge University Press:  02 June 2009

M. Herbin
Affiliation:
Neuromorphologie, Développement, Evolution, I.N.S.E.R.M. U-106, Hôpital de la Salpêtrière, 75651 Paris, France Laboratoire d'Anatomie Comparée, Museum National d'Histoire Naturelle, 75005 Paris, France
J.-P. Rio
Affiliation:
Neuromorphologie, Développement, Evolution, I.N.S.E.R.M. U-106, Hôpital de la Salpêtrière, 75651 Paris, France
J. RepéRant
Affiliation:
Neuromorphologie, Développement, Evolution, I.N.S.E.R.M. U-106, Hôpital de la Salpêtrière, 75651 Paris, France Laboratoire d'Anatomie Comparée, Museum National d'Histoire Naturelle, 75005 Paris, France
H.M. Cooper
Affiliation:
Cerveau et Vision, I.N.S.E.R.M. U-371, 69500 Bron, France
E. Nevo
Affiliation:
Evolution Institute of Haifa, Israel
M. Lemire
Affiliation:
Laboratoire d'Anatomie Comparée, Museum National d'Histoire Naturelle, 75005 Paris, France

Abstract

The optic nerve in two species of subterranean mole-rats (Spalacidae) has been examined at the ultrastructural level. The axial length of the eye and the diameter of the optic nerve are 1.9 mm and 52.5 μm in Spalax leucodon, and 0.7 mm and 80.8 μm in Spalax ehrenbergi, respectively. An anti-glial fibrillary acidic protein postembedding procedure was used to distinguish glial cell processes from axons. In both species, the optic nerve is composed exclusively of unmyelinated axons and a spatial distribution gradient according to the size or the density of fibers is lacking. The optic nerve of S. leucodon contains 1790 fibers ranging in diameter from 0.07–2.30 μm (mean = 0.57 μm), whereas in S. ehrenbergi, only 928 fibers, with diameters of 0.04–1.77 μm (mean = 0.53 μm) are observed. In S. ehrenbergi, a higher proportion of glial tissue is present and the fascicular organization of optic fibers is less obvious. Distribution gradients according to size frequency or density of fibers in the optic nerve are absent in both species. Comparison with other mammals suggests that although ocular regression in microphthalmic species is correlated with a significant decrease in the total number of optic fibers and the relative proportion of myelinated fibers, no difference in the absolute size range of unmyelinated axons is observed. The total absence of myelinated fibers in Spalax may be related to the subcutaneous location of the eyes. The unique presence of unmyelinated fibers in the optic nerve is discussed in relation to the possible conservation of a single class of W-like ganglion cells in the retina, in relation to photoperiodic perception.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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References

Bettica, A. & Johnson, A.B. (1990). Ultrastructural immunogold labeling of glial filaments in osmicated and unosmicated epoxy-embedded tissue. Journal of Histochemistry and Cytochemistry 38, 103109.CrossRefGoogle ScholarPubMed
Brace, C.L. (1963). Structural reduction in evolution. American Naturalist 97, 3949.CrossRefGoogle Scholar
Braekevelt, C.R., Beazley, L.D., Dunlop, S.A. & Darby, J.E. (1986). Numbers of axons in the optic nerve and of the retinal cells during development in the marsupial Setonix brachyurus. Developmental Brain Research 25, 117125.Google Scholar
Branis, M. (1985). Optic nerve in shrews (Insectivora, Soricidae). In Vertebrate Morphology, ed. Duncker, & Fleischer, , pp. 715718. Stuttgart: Gustav Fisher Verlag.Google Scholar
Bremiller, R., Terkel, J., Schabtach, E. & Pickard, G.E. (1986). The subterranean mole rat: An analysis of the subdermal eye. Society for Neuroscience Abstracts 12, 292.15.Google Scholar
Bronchti, G., Rado, R., Terkel, J. & Wollberg, Z. (1991). Retinal projections in the blind mole rat: A WGA-HRP tracing study of a natural degeneration. Developmental Brain Research 58, 159170.CrossRefGoogle ScholarPubMed
Bruesch, S.R. & Arey, L.B. (1942). The number of myelinated and unmyelinated fibers in the optic nerve of vertebrates. Journal of Comparative Neurology 77, 631665.CrossRefGoogle Scholar
Cei, G. (1946). Ortogenesi parallela e degenerazione degli organi dello visto negli Spalacidi. Monitore Zoologico Italiano 55, 6988.Google Scholar
Cooper, H.M., Herbin, M. & Nevo, E. (1993 a). Ocular regression conceals adaptive progression of the visual system in a blind subterranean mammal. Nature 361, 156159.Google Scholar
Cooper, H.M., Herbin, M. & Nevo, E. (1993 b). The visual system of a naturally microphthalmic mammal: The blind mole rat, Spalax ehrenberghi. Journal of Comparative Neurology 328, 313350.CrossRefGoogle Scholar
De Grip, W.J., Jannsen, J.J.M., Foster, R.G., Korf, H.-W., Rothschild, K.J., Nevo, E. & De Caluwe, G.L.J. (1992). Molecular analysis of photoreceptor protein function. In Signal Transduction in Photoreceptors, ed. Hargrave, P.A., Hofmann, K.P. & Kauf, U.B., pp. 4359. Berlin: Springer-Verlag.Google Scholar
De Jong, W.W., Hendriks, W., Sanyal, S. & Nevo, E. (1990). The eye of the blind mole rat (Spalax ehrenbergi): Regressive evolution at the molecular level. In Evolution of Subterranean Mammals at the Organismal and Molecular Levels, ed. Nevo, E. & Reig, O.A., pp. 383395. New York: Alan R. Liss.Google Scholar
De Juan, J., Iniguez, C. & carreres, J. (1978). Number diameter and distribution of the rat optic nerve fibers. Acta Anatomica 102, 294299.CrossRefGoogle ScholarPubMed
De Juan, J., Cuenca, N., Iniguez, C. & Fernandez, E. (1992). Axon types classified by morphometric and multi variate analysis in the rat optic nerve. Brain Research, 585, 431434.CrossRefGoogle Scholar
Dubost, G. (1968). Les mammifères souterrains. Revue d'Ecologie et de Biologie du Sol 5, 99197.Google Scholar
Fuentes, C., Roch, G. & Marty, R. (1979). Le nerf optique du chat. II Aspects qualitatifs de la maturation à l'âge adulte. Acta Anatomica 105, 326337.CrossRefGoogle Scholar
Fukuda, Y. (1977). A three-group classification of rat retinal ganglion cells: Histological and physiological studies. Brain Research 119, 327344.CrossRefGoogle ScholarPubMed
Geoffroy Saint Hilaire, E. (1829). Leçon XVI: “Si la taupe voit, et comment elle voit”. In Cours de l'Histoire Naturelle des Mammifères, ed. Baillère, J.-B., pp. 1349. Paris: Baillère, J.-B.Google Scholar
Griffin, R., Illis, L.S. & Mitchell, J. (1972). Identification of neuroglia by light and electron microscopy. Acta Neuropathologica (Berlin) 22, 712.CrossRefGoogle Scholar
Guy, J., Ellis, E.A., Kelley, K. & Hope, G.M. (1989). Spectra of G ratio, myelin sheath thickness, and axon and fiber diameter in the guinea pig optic nerve. Journal of Comparative Neurology 287, 446454.Google Scholar
Haim, A., Heth, G., Pratt, H. & Nevo, E. (1983). Photoperiodic effects on thermorégulation in a "blind" subterranean mammal. Journal of Experimental Biology 107, 5964.Google Scholar
Heil, P., Bronchti, G., Wollberg, Z. & Scheich, H. (1991). Invasion of visual cortex by the auditory system in the naturally blind mole rat. Neuro Report 2, 735738.Google Scholar
Herbin, M., Repérant, J. & Cooper, H.M. (1994). The visual system of the fossorial mole-lemming, Ellobius talpinus and Ellobius lutescens. Journal of Comparative Neurology 340, 253275.CrossRefGoogle Scholar
Hokoç, J.N. & Oswaldo-Cruz, E. (1978). Quantitative analysis of the opossum's optic nerve: An electron microscopic study. Journal of Comparative Neurology 178, 773782.CrossRefGoogle Scholar
Johnson, A.B. & Bettica, A. (1989). On-grid immunogold labeling of glial intermediate filaments in epoxy-embedded tissue. American Journal of Anatomy 185, 335.CrossRefGoogle ScholarPubMed
Johnson, T.N. (1954). The superior and inferior colliculi of the mole (Scalopus aquaticus machrinus). Journal of Comparative Neurology 101, 765800.CrossRefGoogle ScholarPubMed
Jones, R. & Culver, D.C. (1989). Evidence for selection on sensory structures in a cave population of Cammarus minus (Amphipoda). Evolution 43, 688693.Google Scholar
Kirby, M.A., 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 microscopic study. Journal of Comparative Neurology 211, 318327.Google Scholar
Kirby, M.A., Wilson, P.D. & Fischer, T.M. (1988). Development of the optic nerve of the opossum (Didelphis virginiana). Developmental Brain Research 44, 3748.CrossRefGoogle ScholarPubMed
Kreigler, S. & Chiu, S. Y. (1993). Calcium signaling of glial along mammalian axons. Journal of Neuroscience 13(10), 42294245.CrossRefGoogle Scholar
Kudo, M., Nakamura, Y., Morizumi, T., Tokuno, H. & Kitao, Y. (1988). Direct retinal projections to the lateroposterior thalamic nucleus (LP) in the mole. Neuroscience Letters 93, 176180.Google Scholar
Kudo, M., Yamamoto, M. & Nakamura, Y. (1991). Suprachiasmatic nucleus and retinohypothalamic projections in moles. Brain, Behavior, and Evolution 38, 332338.Google ScholarPubMed
Ling, E.A., Paterson, J.A., Privat, A., Mori, S. & Leblond, C.P. (1973). Identification of glial cells in semithin sections. I. Identification of glial cells in the brain of young rats. Journal of Comparative Neurology 149, 4372.Google Scholar
Lund, R.D. & Lund, J.S. (1965). The visual system of the mole, Talpa europaea. Experimental Neurology 13, 302316.Google Scholar
Lund, R.D. & Lund, J.S. (1966). The central visual pathways and their functional significance in the mole (Talpa europaea). Journal of Zoology 149, 95101.CrossRefGoogle Scholar
Meijer, J.H. & Rietveld, W.J. (1989). Neurophysiology of the supra-chiasmatic circadian pacemaker in rodents. Physiological Reviews 69, 671707.CrossRefGoogle Scholar
Moore, R.Y. (1973). Retinohypothalamic projections in mammals. A comparative study. Brain Research 49, 403409.Google Scholar
Moore, R.Y. & Lenn, N.J. (1972). A retinohypothalamic projection in the rat. Journal of Comparative Neurology 146, 114.Google Scholar
Mori, S. & Leblond, C.P. (1969). Identification of microglia in light and electron microscopy. Journal of Comparative Neurology 135, 5780.Google Scholar
Necker, R., Rehkämper, G. & Nevo, E. (1992). Electrophysiological mapping of body representation in the cortex of the blind mole rat. NeuroReport 3, 505508.CrossRefGoogle ScholarPubMed
Nevo, E., Guttman, R., Haber, M. & Erez, E. (1982). Activity patterns of evolving mole rats. Journal of Mammalogy 63, 453463.CrossRefGoogle Scholar
Nevo, E. (1991). Evolutionary theory and processes of active specia-tion in subterranean mole rats, Spalax ehrenbergi superspecies in Israel. In Evolutionary Biology, Vol. 25, ed. Hecht, M.K., Wallace, B. & Mac Intyre, R.J., pp. 1125. New York: Plenum.Google Scholar
Pévet, P., Heth, G., Haim, A. & Nevo, E. (1984). Photoperiod perception in the blind mole rat (Spalax ehrenbergi, Nehring): Involvement of the harderian gland, atrophied eyes, and melatonin. Journal of Experimental Zoology 232, 4150.Google Scholar
Poulson, T.L. & White, W.B. (1969). The cave environment. Science 165, 971980.CrossRefGoogle ScholarPubMed
Quilliam, T.A. (1964). Special features of the eye of the mole (Talpa europaea). Anatomical Record 148, 396.Google Scholar
Quilliam, T.A. (1966 a). The mole's sensory apparatus. Journal of Zoology 146, 7688.CrossRefGoogle Scholar
Quilliam, T.A. (1966 b). The problem of vision in the ecology of Talpa europaea. Experimental Eye Research 5, 6378.Google Scholar
Rado, R., Gev, H. & Terkel, J. (1988). The role of light in entraining mole rats' circadian rhythms. Israeli Journal of Zoology 35, 105106.Google Scholar
Rado, R., Bronchti, G., Wollberg, Z. & Terkel, J. (1992). Sensitivity to light of the blind mole rat — behavioral and neuroanatomical study. Israeli Journal of Zoology 38, 323331.Google Scholar
Rado, R. & Terkel, J. (1989). Circadian activity of the blind mole rats, Spalax ehrenbergi monitored by radio-telemetry in seminatural and natural conditions. In Environmental Quality and Ecosystem Stability, vol. B, ed. Spanier, E., Steinberger, Y. & Luria, M., pp. 391400. Jerusalem: ISEEQS.Google Scholar
Reese, B.E. & Ho, K.Y. (1988). Axon diameter distributions across the monkey's optic nerve. Neuroscience 27, 205214.CrossRefGoogle ScholarPubMed
Rhoades, R.W., Hsu, L. & Parfett, G. (1979). An electron microscopic analysis of the optic nerve in the golden hamster. Journal of Comparative Neurology 186, 491504.CrossRefGoogle Scholar
Rochon-Duvigneaud, A. (1943). Les yeux et la vision des vertébrés. Paris: Masson.Google Scholar
Sanyal, S., Jansen, H.G., De Grip, W.J., Nevo, E. & De Jong, W.W. (1990). The eye of the blind mole rat, Spalax ehrenberghi. Rudiment with hidden function? Investigative Ophthalmology and Visual Science 31, 13981404.Google Scholar
Savic, I.R. & Nevo, E. (1990). The Spalacidae: Evolutionary history, speciation and population biology. In Evolution of Subterranean Mammals at the Organismal and Molecular Levels, ed. Nevo, E. & Reig, A.O., pp. 129153. New York: Alan R. Liss.Google Scholar
Somogyi, P. & Hodgson, A.J. (1985). Antisera to gamma-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. Journal of Histochemistry and Cytochemistry 33, 249257.CrossRefGoogle ScholarPubMed
Stone, J. (1983). The classification of retinal ganglion cells and its impact on the neurobiology of vision. In Parallel Processing in the Visual System, pp. 1438. New York: Plenum Press.Google Scholar
Sturrock, R.R. (1987). Changes in the number of axons in the human embryonic optic nerve from 8 to 18 weeks gestation. Journal für Hirnforschung 6, 649652.Google Scholar
Tay, D., So, K.-F., Jen, L.S. & Lau, K.C. (1986). The postnatal development of the optic nerve in hamsters: An electron microscopic study. Developmental Brain Research 30, 268273.CrossRefGoogle Scholar
Trimmer, P.A. & Wunderlich, R.E. (1990). Changes in astroglial scar formation in rat optic nerve as a function of development. Journal of Comparative Neurology 296, 359378.CrossRefGoogle ScholarPubMed
Vaughn, J.E. & Peters, A. (1968). A third neuroglial cell type: An electron microscopic study. Journal of Comparative Neurology 133, 269288.Google Scholar
Vuillez, P., Herbin, M., Cooper, H.M., Nevo, E. & Pévet, P. (1994). Photic induction of Fos-immunoreactivity in the suprachiasmatic nuclei of the blind mole rat (Spalax ehrenbergi). Brain Research 654, 8184.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
Wilkens, H. (1971). Genetic interpretation of regressive evolutionary processes: Studies on hybrid eyes of two Astyanax cave populations (Characidae, Pisces). Evolution 25, 530544.CrossRefGoogle Scholar
Wilkens, H. (1988). Evolution and genetics of epigean and cave Astyanax fasciatus (Characidae, Pisces). Evolutionary Biology 23, 271367.CrossRefGoogle Scholar
Williams, R.W. & Chalupa, L.M. (1983). An analysis of the axon caliber within the optic nerve of the cat: Evidence of size groupings and regional organization. Journal of Neuroscience 3, 15541564.Google Scholar
Wright, S. (1964). Pleiotropy in the evolution of structural reduction and of dominance. American Naturalist 98, 6569.Google Scholar