The eye of the African mole-rat Cryptomys anselli: To see or not to see?

European Journal of Neuroscience

Volumn 17, Issue 4, 2003, Pages 709-720

  Cernuda Cernuda, Rafael ^a   García Fernández, José M ^a   Gordijn, Marijke C M ^b   Bovee Geurts, Petra H M ^c   DeGrip, Willem J ^c  

^a UNIVERSITY OF OVIEDO   (Spain)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c NONE

Author keywords

Cones; Mole rat; Photoreceptor morphology; Retina; Rhodopsin; Rods

Indexed keywords

CELL MARKER; LECTIN;

ANTERIOR EYE CHAMBER; ANTIBODY LABELING; APOPTOSIS; ARTICLE; CELL ASSAY; CELL LOSS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EYE; FEMALE; LENS; MALE; MOLE RAT; NERVE CELL; NONHUMAN; PEANUT; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA CONE; RETINA ROD; STAINING; STRUCTURE ANALYSIS; SYNAPSE; THICKNESS; VISION; VISUAL CORTEX; VITREOUS BODY;

ACUTE-PHASE PROTEINS; ANIMALS; CHICKENS; EYE; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, IMMUNOELECTRON; MOLE RATS; OCULAR PHYSIOLOGY; OPSIN; PHOTORECEPTORS; RATS; RETINA; RHODOPSIN; TRANSDUCIN;

EID: 0037295372     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02485.x     Document Type: Article

References (71)

1. Avivi, A., Oster, H., Joel, A., Beiles, A., Albrecht, U. & Nevo, E. (2002) Circadian genes in a blind subterranean mammal II: Conservation and uniqueness of the three Period homologs in the blind subterranean mole rat, Spalax ehrenbergi superspecies. Proc. Natl Acad. Sci. USA, 99, 11718-11723.
2. Bazylinski, D.A. (1999) Synthesis of the bacterial magnetosome: the making of a magnetic personality. Int. Microbiol., 2, 71-80.
3. Beard, M.E., Davies, T., Holloway, M. & Holtzman, E. (1988) Peroxisomes in pigment epithelium and Müller cells of amphibian retina possess D-amino acid oxidase as well as catalase. Exp. Eye Res., 47, 795-806.
4. Bennett, N.C. (1992) The locomotory activity patterns of a functionally complete colony of Cyptomys hottentotus hottentotus (Rodentia: Bathyergidae). J. Zool. Lond., 228, 435-443.
5. Berson, D.M., Dunn, E.A. & Takao, M. (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science, 295, 1070-1013.
6. Blanks, J.C. & Johnson, L.V. (1983) Selective lectin binding of the developing mouse retina. J. Comp. Neurol., 221, 31-41.
7. 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. Brain Res. Dev. Brain Res., 58, 159-170.
8. Burda, H., Bruns, V. & Muller, M. (1990a) Sensory adaptations in subterranean mammals. Prog. Clin. Biol. Res., 335, 269-293.
9. Burda, H., Marhold, S., Westenberger, T., Wiltschko, R. & Wiltschko, W. (1990b) Magnetic compass orientation in the subterranean rodent Cryptomys hottentotus (Bathyergidae). Experientia, 46, 528-530.
10. Burda, H., Zima, J., Scharff, A., Macholán, M. & Kawalika, M. (1999) The karyotypes of Cryptomys anselli sp. nova and Cryptomys kafuensis sp. nova: new species of the common mole-rat from Zambia (Rodentia, Bathyergidae). Z. Säugetierk., 64, 36-50.
11. Cano, J., Machado, A. & Reinoso-Suárez, F. (1986) Morphological changes in the retina of ageing rats. Arch. Gerontol. Geriatr., 5, 41-50.
12. Carter-Dawson, L.D. & LaVail, M.M. (1979) Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J. Comp. Neurol., 188, 245-262.
13. Cei, G. (1946) L'occhio di Heterocephalus glaber Rüppell. Note anatomo-descriptive istologiche. Monit. Zool. Ital., 55, 89-96.
14. Cernuda-Cernuda, R., DeGrip, W.J., Cooper, H.M., Nevo, E. & García-Fernández, J.M. (2002) The retina of Spalax ehrenbergi: novel histologic features supportive of a modified photosensory role. Invest. Ophthalmol. Vis. Sci., 43, 2374-2383.
15. Chun, M.H., Grünert, U., Martin, P.R. & Wässle, H. (1996) The synaptic complex of cones in the fovea and the periphery of the macaque monkey retina. Vission Res., 36, 3383-3395.
16. Cooper, H.M., Herbin, M. & Nevo, E. (1993a) Ocular regression conceals adaptive progression of the visual system in a blind subterranean mammal. Nature, 361, 156-159.
17. Cooper, H.M., Herbin, M. & Nevo, E. (1993b) Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi. J. Comp. Neurol., 328, 313-350.
18. David-Gray, Z.K., Bellingham, J., Munoz, M., Avivi, A., Nevo, E. & Foster, R.G. (2002) Adaptive loss of ultraviolet/violet-sensitive (UVS/VS) cone opsin in the blind mole rat (Spalax ehrenbergi). Eur. J. Neurosci., 16, 1186-1194.
19. David-Gray, Z.K., Cooper, H.M., Jahssen, J.W.H., Nevo, E. & Foster, R.G. (1999) Spectral tuning of a circadian photopigment in a subterranean 'blind' mammal (Spalax ehrenbergi). FEBS Lett., 461, 343-347.
20. David-Gray, Z.K., Janssen, J.W., De Grip, W.J., Nevo, E. & Foster, R.G. (1998) Light detection in a 'blind mammal'. Nature Neurosci., 1, 655-656.
21. Deguchi, J., Yamamoto, A., Fujiki, Y., Uyama, M., Tsukahara, I. & Tashiro, Y. (1992) Localization of nonspecific lipid transfer protein (nsLTP = sterol carrier protein 2) and acyl-CoA oxidase in peroxisomes of pigment epithelial cells of rat retina. J. Histochem. Cytochem., 40, 403-410.
22. Diebel, C.E., Proksch, R., Green, C.R., Neilson, P. & Walker, M.M. (2000) Magnetite defines a vertebrate magnetoreceptor. Nature, 406, 299-302.
23. Eloff, G. (1958) The functional and structural degeneration of the eye of the South African rodent moles, Cryptomys bigalkei and Bathyergus maritimus. S. Afr. J. Sci., 54, 293-302.
24. Foster, R.G., Provencio, I., Hudson, D., Fiske, S., De Grip, W.J. & Menaker, M. (1991) Circadian photoreception in the retinally degenerate mouse (rd/rd). J. Comp. Physiol. A., 169, 39-50.
25. Gooley, J.J., Lu, J., Chou, T.C., Scammell, T.E. & Saper, C.B. (2001) Melanopsin in cells of origin of the retinohypothalamic tract. Nature Neurosci., 4, 1165.
26. Hacker, G. (2000) The morphology of apoptosis. Cell Tissue Res., 301, 5-17.
27. Hannibal, J., Hindersson, P., Knudsen, S.M., Georg, B. & Fahrenkrug, J. (2002a) The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. J. Neurosci., 22-RC191, 1-7.
28. Hannibal, J., Hindersson, P., Nevo, E. & Fahrenkrug, J. (2002b) The circadian photopigment melanopsin is expressed in the blind subterranean mole rat Spalax. Neuroreport, 23, 1411-1414.
29. Harman, A., Abrahams, B., Moore, S. & Hoskins, R. (2000) Neuronal density in the human retinal ganglion cell layer from 16 to 77 years. Anat. Rec., 260, 124-131.
30. Hattar, S., Liao, H.W., Takao, M., Berson, D.M. & Yau, K.W. (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science, 295, 1065-1070.
31. Haverkamp, S., Grunert, U. & Wässle, H. (2000) The cone pedicle, a complex synapse in the retina. Neuron, 27, 85-95.
32. Herbin, M., Rio, J.P., Reperant, J., Cooper, H.M., Nevo, E. & Lemire, M. (1995) Ultrastructural study of the optic nerve in blind mole-rats (Spalacidae, Spalax). Visual Neurosci., 12, 253-261.
33. Hickman, G.C. (1980) Locomotory activity of captive Cryptomys hottentotus (Mammalia: Bathyergidae), a fossorial rodent. J. Zool. Lond., 192, 225-235.
34. Hicks, D. & Molday, R.S. (1986) Differential immunogold-dextran labelling of bovine and frog rod and cone cells using monoclonal antibodies again bovine rhodopsine. Exp. Eye Res., 42, 55-71.
35. Hughes, A. (1977) The topography of vision in mammals of contrasting lifestyle. In Cresitelli, F. (ed.), The Visual System of Vertebrates, Handbook of Sensory Physiology, Vol. VII/5. Springer-Verlag, Berlin, pp. 614-756.
36. Janssen, J.J.M. (1991) The Rod Visual Pigment Rhodopsin: In Vitro Expression and Site Specific Mutagenesis. PhD Thesis. University of Nijmegen, The Netherlands.
37. Janssen, J.W.H., Bovee-Geurts, P.H.M., Peeters, Z.P.A., Bowmaker, J.K., Cooper, H.M., David-Gray, Z.K., Nevo, E. & De Grip, W.J. (2000) A fully functional rod visual pigment in a blind mammal. A case for adaptative functional reorganization? J. Biol. Chem., 275, 38674-38679.
38. Jeon, C.-J., Strettoi, E. & Masland, R.H. (1998) The major cell populations of the mouse retina. J. Neurosci., 18, 8936-8946.
39. Jiménez, A.J., García-Fernández, J.M., González, B. & Foster, R.G. (1996) The spatio-temporal pattern of photoreceptor degeneration in the aged rd/rd mouse retina. Cell Tissue Res., 284, 193-202.
40. Kimchi, T. & Terkel, J. (2001) Magnetic compass orientation in the blind mole rat Spalax ehrenbergi. J. Exp. Biol., 204, 751-758.
41. Kornhauser, J.M., Nelson, D.E., Mayo, K.E. & Takahashi, J.S. (1990) Photic and circadian regulation of c-fos gene expression in the hamster suprachiasmatic nucleus. Neuron, 5, 127-134.
42. Kössl, M., Frank, G., Burda, H. & Burns, V. (1996) Acoustic distortion products from the cochlea of the blind African mole rat, Cryptomys spec. J. Comp. Physiol. A, 178, 427-434.
43. Lovegrove, B.G., Heldmaier, G. & Ruf, T. (1993) Circadian activity rhythms in colonies of 'blind' molerats Cryptomys damarensis (Bathyergidae). S. Afr. J. Zool., 28, 46-55.
44. Lovegrove, B.G. & Papenfus, M.E. (1993) Circadian activity rhythms in the solitary Cape mole-rat (Georychus capensis: Bathyergidae) with some evidence of splitting. Physiol. Behav., 58, 679-685.
45. Lukáts, A., Dkhissi-Benyahya, O., Szepessy, Z., Rohlich, P., Vigh, B., Bennett, N.C., Cooper, H.M. & Szél, A. (2002) Visual pigment coexpression in all cones of two rodents, the Siberian hamster, and the pouched mouse. Invest. Ophthalmol. Vis. Sci., 43, 2468-2473.
46. Mann, S., Sparks, N.H., Walker, M.M. & Kirschvink, J.L. (1988) Ultrastructure, morphology and organization of biogenic magnetite from sockeye salmon, Oncorhynchus nerka: implications for magnetoreception. J. Exp. Biol., 140, 35-49.
47. Marhold, S., Beiles, A., Burda, H. & Nevo, E. (2000) Spontaneous directional preference in a subterranean rodent, the blind mole-rat, Spalax ehrenbergi. Folia Zool., 49, 7-18.
48. Marhold, S., Wiltschko, W. & Burda, H. (1997) A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften, 84, 421-423.
49. Müller, M. & Burda, H. (1989) Restricted hearing range in a subterranean rodent, Cryptomys hottentotus. Naturwissenschaften, 76, 134-135.
50. Müller, M., Laube, B., Burda, H. & Bruns, V. (1992) Structure and function of the cochlea in the African mole rat (Cryptomys hottentotus): evidence for a low frequency acoustic fovea. J. Comp. Physiol. A, 171, 469-476.
51. Nemec, P., Altmann, J., Marhold, S., Burda, H. & Oelschläger, H.H. (2001) Neuroanatomy of magnetoreception: the superior collicullus involved in magnetic orientation in a mammal. Science, 294, 366-368.
52. Nevo, E. (1999) Mosaic Evolution of Subterranean Mammals: Regression, Progression, and Global Convergence. Oxford University Press, Oxford.
53. Oelschläger, H.H.A., Nakamura, M., Herzog, M. & Burda, H. (2000) Visual system labeled by c-Fos immunohistochemistry after light exposure in the 'blind' subterranean zambian mole-rat (Cryptomys anselli). Brain Behav. Evol., 55, 209-220.
54. Pickard, G.E. (1982) The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection. J. Comp. Neurol., 211, 65-83.
55. Provencio, I., Rodríguez, I.R., Jiang, G., Hayes, W.P., Moreira, E.F. & Rollag, M.D. (2000) A novel human opsin in the inner retina. J. Neurosci., 20, 600-605.
56. Provencio, I., Rollag, M.D. & Castrucci, A.M. (2002) Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature, 415, 493.
57. Rao-Mirotznik, R., Harkins, A.B., Buchsbaum, G. & Sterling, P. (1995) Mammalian rod terminal: architecture of a binary synapse. Neuron, 14, 561-569.
58. Rea, M.A. (1992) Different populations of cells in the suprachiasmatic nuclei express c-fos in association with light-induced phase delays and advances of the free-running activity rhythm in hamsters. Brain Res., 579, 107-112.
59. Reppert, S.M. & Weaver, D.R. (2002) Coordination of circadian timing in mammals. Nature, 418, 935-941.
60. Riccio, A.P. & Goldman, B.D. (2000) Circadian rhythms of locomotor activity in naked mole-rats (Heterocephalus glaber). Physiol. Behav., 71, 1-13.
61. Ritz, T., Dommer, D.H. & Phillips, J.B. (2002) Shedding light on vertebrate magnetoreception. Neuron, 34, 503-506.
62. Röhlich, P., Szél, A., Johnson, L.V. & Hageman, G.S. (1989) Carbohydrate components recognized by the cone-specific monoclonal antibody CSA-1 and by peanut agglutinin are associated with red- and green-sensitive cone photoreceptors. J. Comp. Neurol., 289, 395-400.
63. Sanyal, S., Jansen, H.G., De Grip, W.J., Nevo, E. & De Jong, W.W. (1990) The eye of the blind mole rat, Spalax ehrenbergi. Rudiment with hidden function? Invest. Ophthalmol. Vis. Sci., 31, 1398-1404.
64. Schalken, J.J. & De Grip, W.J. (1986) Enzyme-linked immunosorbent assay for the quantitative determination of the visual pigment rhodopsin in total eye extracts. Exp. Eye Res., 43, 431-439.
65. Scharff, A. & Grütjen, O. (1997) Evidence for aboveground activity of Zambian mole-rats (Cryptomys, Bathyergidae, Rodentia). Z. Säugetierk., 62, 253-254.
66. Sefton, A.J. & Dreher, B. (1995) Visual system. In Paxinus, G. (ed.), The Rat Nervous System. Academic Press, San Diego, pp. 883-880.
67. Söderström, K.-O. (1988) Lectin binding to the human retina. Anat. Rec., 220, 219-223.
68. St Jules, R., Kennard, J., Setlik, W. & Holtzman, E. (1992) Frog cones as well as Müller cells have peroxisomes. Exp. Eye Res., 54, 1-8.
69. Sternberger, L.A. (1986) Immunocytochemistry, 3rd edn. John Wiley & Sons, New York.
70. 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 Res., 654, 81-84.
71. Weisse, I. (1995) Changes in the aging rat retina. Ophthal. Res., 27, 154-163.