Subcortical visual system of the African mole-rat Cryptomys anselli: To see or not to see?

European Journal of Neuroscience

Volumn 20, Issue 3, 2004, Pages 757-768

  Němec, Pavel ^a,b   Burda, Hynek ^c   Peichl, Leo ^d  

^a CHARLES UNIVERSITY   (Czech Republic)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

Bathyergidae; Dark reared; Microphthalmia; Ocular regression; Rodent; Subterranean mammals

Indexed keywords

CYTOCHROME C OXIDASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ENZYME ACTIVITY; EYE MOVEMENT; FEMALE; GENICULATE NUCLEUS; INNERVATION; LATERAL GENICULATE NUCLEUS; MALE; MOLE RAT; MYELINATED NERVE; NONHUMAN; NONMYELINATED NERVE; OLIVARY NUCLEUS; OPTIC NERVE; OPTIC TRACT; PHOTOPERIODICITY; PRETECTUM; PRIORITY JOURNAL; RETINA; RETINA DEVELOPMENT; SUPERIOR COLLICULUS; SUPRACHIASMATIC NUCLEUS; VISION; VISUAL CORTEX; VISUAL DISCRIMINATION; VISUAL SYSTEM; VISUOMOTOR COORDINATION;

ANIMALS; BRAIN MAPPING; CHOLERA TOXIN; ELECTRON TRANSPORT COMPLEX IV; FEMALE; FUNCTIONAL LATERALITY; GENICULATE BODIES; HORSERADISH PEROXIDASE; MALE; MOLE RATS; OPTIC NERVE; RATS; RETINA; SUPERIOR COLLICULUS; SUPRACHIASMATIC NUCLEUS; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 3843103843     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03510.x     Document Type: Article

References (85)

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. Bennett, N.C. (1992) The locomotory activity patterns of a functionally complete colony of Cryptomys hottentotus hottentotus (Rodentia: Bathyergidae). J. Zool. Lond., 228, 435-443.
3. Bennett, N.C. & Faulkes, C.G. (2000) African Mole-Rats, Ecology and Eusociality. Cambridge University Press, Cambridge.
4. Bronchti, G., Rado, R., Terkel, J. & Wollberg, Z. (1991) Retinal projections in the blind mole rat: a WGA-HPR tracing study of a natural degeneration. Dev. Brain Res., 58, 159-170.
5. Brückmann, G. & Burda, H. (1997) Hearing in blind subterranean Zambian common mole-rats (Cryptomys sp., Bathyergidae, Rodentia). J. Comp. Physiol. A, 181, 83-88.
6. Burda, H., Bruns, V. & Müller, M. (1990a) Sensory adaptations in subterranen mammals. In Nevo, E. & Reig, O.A. (eds), Evolution of Subterranean Mammals at the Organismal and Moleculars Levels. Alan R. Liss, Inc., New York, pp. 269-294.
7. 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.
8. Card, J.P. & Moore, R.Y. (1991) The organization of visual circuits influencing the circadian activity of the suprachiasmatic nucleus. In Klein, D.C., Moore, R.Y. & Reppert, S.M. (eds), Suprachiasmatic Nucleus: the Mind's Clock. Oxford University Press, New York, pp. 51-76.
9. Cei, G. (1943) L'occhio di 'Heterocephalus glaber' Rupp. Organo Ufficiale Della Societa Italiana Di Anatomia, 54, 89-96.
10. 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.
11. Cernuda-Cernuda, R., García-Fernández, J.M., Gordijn, M.C.M., Bovee-Geurts, P.H.M. & DeGrip, W.J. (2003) The eye of the african mole-rat Cryptomys anselli: to see or not to see? Eur. J. Neurosci., 17, 709-720.
12. Clarke, R.J. & Ikeda, H. (1985) Luminance and darkness detectors in the olivary and posterior pretectal nuclei and their relationship to the pupillary light reflex in the rat. Exp. Brain Res., 57, 224-232.
13. 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.
14. 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.
15. Cotter, J.R. (1985) Retinofugal projections of the big brown bat, Eptesicus fuscus and the neotropical fruit bat, Artibeus jamaicensis. Am. J. Anat., 172, 105-124.
16. Cotter, J.R. & Pentney, R.J.P. (1979) Retinofugal projections of none-cholocating (Pteropus giganteus) and echolocating (Myotis lucifugus) bats. J. Comp. Neurol., 184, 381-400.
17. De Olmos, J., Hardy, H. & Heimer, L. (1978) The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J. Comp. Neurol., 181, 213-244.
18. Dean, P., Redgrave, P. & Westby, G.W.M. (1989) Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci., 12, 137-147.
19. Deutschlander, M.E., Phillips, J.B. & Borland, S.C. (1999) The case for light-dependant magnetic orientation in animals. J. Exp. Biol., 202, 891-908.
20. Eloff, G. (1958) Functional and structural degeneration of the eye of the south African rodent mole, Cryptomys bigalkei and Bathyergus maritimus. S. Afr. J. Sci., 54, 292-302.
21. Frost, D.O., So, K.-F. & Schneider, G.E. (1979) Postnatal development of retinal projections in syrian hamsters: a study using autoradiographic and anterograde degeneration techniques. Neuroscience, 4, 1649-1677.
22. Gattermann, R. & Burda, H. (1994) Soziale Isolation und Circadianrhythmik beim eusozialen Graumull. Verh. Dtsch. Zool. Ges., 87, 39.
23. Godement, P., Salaün, J. & Imbert, M. (1984) Prenatal and postnatal development of retinogeniculate and retinocullicular projections in the mouse. J. Comp. Neurol., 230, 552-575.
24. Haim, A., Heth, G., Pratt, H. & Nevo, E. (1983) Photoperiodic effects on thermoregulation in a 'blind' subterranean mammal. J. Exp. Biol., 107, 59-64.
25. Hall, W.C. & Moschovakis, A. (2004) The Superior Colliculus. New Approaches for Studying Sensorimotor Integration. CRC Press, Boca Raton.
26. Hannibal, J., Hindersson, P., Nevo, E. & Fahrenkrug, J. (2002) The circadian photopigment melanopsin is expressed in the blind subterranean mole rat Spalax. Neuroreport, 13, 1411-1414.
27. Harrington, M.E. (1997) The ventral lateral geniculate nucleus and the intergeniculate leaflet: interrelated structures in the visual and circadian systems. Neurosci. Biobehav. Rev., 21, 705-727.
28. Herbin, M., Repérant, J. & Cooper, H.M. (1994) Visual system of the fossorial mole-lemmings, Ellobius talpinus and Ellobius lutescens. J. Comp. Neurol., 346, 253-275.
29. Herbin, M., Rio, J.-P., Repérant, J., Cooper, H.M., Nevo, E. & Lemire, M. (1995) Ultrastructural study of the optic nerve in blind mole-rats (Spalacidae, Spalax). Vis. Neurosci., 12, 253-261.
30. Hickey, T.L. & Spear, R.P.D. (1976) Retinogeniculate projections in hooded and albino rats: an autoradiographic study. Exp. Brain Res., 24, 523-529.
31. Hickman, G.C. (1980) Locomotory activity of captive Cryptomys hottentotus (Mammalia: Bathyergidae), a fossorial rodent. J. Zool. Lond., 192, 225-235.
32. Huerta, M.F. & Harting, J.K. (1984) The mammalian superior colliculus: studies of its morphology and connections. In Vanegas, H. (ed.), Comparative Neurology of the Optic Tectum. Plenum Press, New York, pp. 687-773.
33. Hutchins, B. & Weber, J.T. (1983) A rapid myelin stain for frozen sections: modification of the Heidenhain procedure. J. Neurosci. Meth., 7, 289-294.
34. Johannesson-Gross, K. (1988) Brightness discrimination of the mole (Talpa europaea L) in learning experiments applying a modified tube-maze method. Z. Säugetierkunde, 53, 193-201.
35. Kaczmarek, L. & Caudhuri, A. (1997) Sensory regulation of immediate-early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity. Brain Res. Rev., 23, 237-256.
36. Kimchi, T., Etienne, A.S. & Terkel, J. (2004) A subterranean mammals uses the magnetic compass for path integration. Proc. Natl Acad. Sci. USA, 101, 1105-1109.
37. Kimchi, T. & Terkel, J. (2001) Magnetic compass orientation in the blind mole rat Spalax ehrenbergi. J. Exp. Biol., 204, 751-758.
38. Kimchi, T. & Terkel, J. (2002) Seeing or not seeing. Curr. Opin. Neurobiol., 12, 728-734.
39. Kudo, M., Nakamura, Y., Moriizumi, T., Tokuno, H. & Kitao, Y. (1988) Direct retinal projections to the lateroposterior thalamic nucleus (LP) in the mole. Neurosc. Lett., 93, 176-180.
40. Kudo, M., Yamamoto, M. & Nakamura, Y. (1991) Suprachiasmatic nucleus and retinohypothalamic projections in moles. Brain Behav. Evol., 38, 332-338.
41. Lacey, E.A., Patton, J.L. & Cameron, G.N. (2000) Life Underground, the Biology of Subterranean Rodents. University of Chicago Press, Chicago.
42. Linden, R. & Perry, V.H. (1983) Massive retinotectal projection in rats. Brain Res., 272, 145-149.
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. Lund, R.D. & Lund, J.S. (1965) The visual system of the mole, Talpa europaea. Exp. Neurol., 13, 302-316.
45. Magnin, M., Cooper, H.M. & Mick, G. (1989) Retinohypothalamic pathway: a break in the law of Newton-Müller-Gudden? Brain Res., 488, 390-397.
46. 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.
47. Marhold, S., Wiltschko, W. & Burda, H. (1997) A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften, 84, 421-423.
48. Miller, A.M., Miller, R.B., Obermayer, W.H., Behan, M. & Benca, R.M. (1999) The pretectum mediates rapid eye movement sleep regulation by light. Behav. Neurosci., 113, 755-765.
49. Mills, S.L. & Catania, K.C. (2004) Identification of retinal neurons in a regressive rodent eye (the naked mole-rat). Vis. Neurosci., 21, 107-117.
50. Mizuno, N., Sumi, M.-U., Tashiro, T., Takahashi, O. & Satoda, T. (1991) Retinofugal projections in the house musk shrew, Suncus murinus. Neurosci. Lett., 125, 133-135.
51. Montero, V.M. (1997) c-Fos induction in sensory pathways of rats exploring a novel complex environment: shifts of active thalamic reticular sectors by predominant sensory cues. Neuroscience, 76, 1069-1081.
52. Montero, V.M. & Jian, S. (1995) Induction of c-Fos protein by patterned visual stimulation in central visual pathways of the rat. Brain Res., 690, 189-199.
53. Moore, R.Y. & Card, J.P. (1994) Intergeniculate leaflet: an anatomically and functionally distinct subdivision of the lateral geniculate complex. J. Comp. Neurol., 344, 403-430.
54. Moore, R.Y., Speh, J.C. & Leak, R.K. (2002) Suprachiasmatic nucleus organization. Cell Tissue Res., 309, 89-98.
55. Movshon, J.A. & Kiorpes, L. (1990) The role of experience in visual development. In Coleman, J.R. (ed.), Development of Sensory Systems in Mammals. John Wiley & Sons, New York, pp. 155-202.
56. Negroni, J., Bennett, N.C. & Cooper, H.M. (2003) Organization of the circadian system in the subterranean mole rat, Cryptomys hottentotus (Bathyergidae). Brain Res., 967, 48-62.
57. Negroni, J., Nevo, E. & Cooper, H.M. (1997) Neuropeptidergic organization of the suprachiasmatic nucleus in the blind mole rat (Spalax ehrenbergi). Brain Res. Bull., 44, 633-639.
58. Nevo, E. (1999) Mosaic Evolution of Subterranean Mammals: Regression, Progression and Global Convergence. Oxford University Press, Oxford.
59. Němec, P., Altmann, J., Marhold, S., Burda, H. & Oelschläger, H.H.A. (2001) Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal. Science, 294, 366-368.
60. 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.
61. Olucha, F., Martinez-Garcia, F. & Lopéz-Garcia, C. (1985) A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP). J. Neurosci. Meth., 13, 131-138.
62. Omlin, F.X. (1997) Optic disc and optic nerve of the blind Cape mole-rat (Georychus capensis): a proposed model for naturally occurring reactive gliosis. Brain Res. Bull., 44, 627-632.
63. Oosthuizen, M.K., Cooper, H.M. & Bennet, N.C. (2003) Circadian rhythms of locomotor activity in solitary and social species of African mole-rats (Family: Bathyerdidae). J. Biol. Rhythm., 18, 481-490.
64. Paxinos, G. & Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, San Diego.
65. Peichl, L., Němec, P. & Burda, H. (2004) Unusual cone and rod properties in subterranean African mole-rats (Rodentia, Bathyergidae). Eur. J. Neurosci., 19, 1545-1558.
66. van den Pol, A.N. (1980) The hypothalamic suprachiasmatic nucleus of rat: intrinsic anatomy. J. Comp. Neurol., 191, 661-702.
67. Prichard, J.R., Stoffel, R.T., Quimby, D.L., Obermeyer, W.H., Benca, R.M. & Behan, M. (2002) Fos immunoreactivity in rat subcortical visual shell in response to illuminance changes. Neuroscience, 114, 781-793.
68. Quilliam, T.A. (1966) The problem of vision in the ecology of Talpa europaea. Exp. Eye Res., 5, 63-78.
69. 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.
70. Reimer, K. (1989) Retinofugal projections in the rufous horseshoe bat, Rhinolophus rouxi. Anat. Embryol., 180, 89-98.
71. Rhoades, R.W., Hsu, L. & Parrfett, G. (1979) An electron microscopic analysis of the optic nerve in the golden hamster. J. Comp. Neurol., 186, 491-504.
72. Ritz, T., Dommer, D.H. & Phillips, J.B. (2002) Shedding light on vertebrate magnetoreception. Neuron, 34, 503-506.
73. 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. Invest. Ophthalmol. Vis. Sci., 31, 1398-1404.
74. Scalia, F. (1972) The termination of retinal axons in the pretectal region of mammals. J. Comp. Neurol., 145, 223-258.
75. Scherbakov, V.P. & Winklhofer, M. (1999) The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals. Eur. Biophys. J., 28, 380-392.
76. Sefton, A.J. & Dreher, B. (1995) Visual system. In Paxinos, G. (ed.), The Rat Nervous System. Academic Press, San Diego, pp. 833-880.
77. Simpson, J.I. (1984) The accessory optic system. Annu. Rev. Neurosci., 7, 13-41.
78. Stein, B.E. & Meredith, M.A. (1993) The Merging of the Senses. MIT Press, Cambridge, MA.
79. 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. Dev. Brain Res., 30, 268-273.
80. Tobler, I., Herrmann, M., Cooper, H.M., Negroni, J., Nevo, E. & Achermann, P. (1998) Rest-activity rhythm of the blind mole rat Spalax ehrenbergi under different lighting conditions. Behav. Brain Res., 96, 173-183.
81. Trejo, L.J. & Cicerone, C.M. (1984) Cells in the pretectal olivary nucleus are in the pathway for the direct light reflex of the pupil in the rat. Brain Res., 300, 49-62.
82. Vaney, D.I., Peichl, L., Wässle, H. & Illing, R.-B. (1981) Almost all ganglion cells in the rabbit retina project to the superior colliculus. Brain Res., 212, 447-453.
83. Vuillez, P., Herbin, M., Cooper, H.M., Nevo, E. & Pevet, P. (1994) Photic induction of Fos immunoreactivity in the suprachiasmatic nuclei of the blind mole rat (Spalax ehrenbergi). Brain Res., 654, 81-84.
84. Walls, G.L. (1942) The Vertebrate Eye and its Adaptive Radiation. Cranbrook Press, Michigan.
85. Wong-Riley, M. (1979) Changes in visual system of monocularly sutured or enucleated cats demonstratable with cytochrome oxidase histochemistry. Brain Res., 171, 11-28.