The retina of Spalax ehrenbergi: novel histologic features supportive of a modified photosensory role.

PURPOSE The retina of the blind mole rat Spalax ehrenbergi was compared with other vertebrate photosensitive organs in an attempt to correlate its histologic organization with a presumptive nonvisual photoreceptor role. METHODS The eyes of eight adult animals were analyzed by light and electron microscopy, using conventional staining and immunolabeling with antibodies against phototransduction proteins and calretinin. RESULTS Rods accounted for most of the photoreceptor cells in the Spalax retina, although their morphology is dissimilar to that of sighted mammals, in that they contained only rudimentary outer segments. The latter showed strong rod-opsin and transducin immunoreactions. The phagosomes in the retinal pigmentary epithelium were also rod-opsin positive. Synapses were evident at the photoreceptor cells pedicles. Occasionally, several synaptic active sites were present, suggesting cone cell origin; however, cone-opsin was not immunodetected in the study samples. Synaptic ribbon fields, sometimes distant to the active sites, resembled those found in the vertebrate pineal. The other retinal layers were somewhat less organized than in sighted mammals. Some cells were displaced and the calretinin-positive inner plexiform layer had no sublayers. Calretinin immunolabeling was found in horizontal, amacrine, and ganglion cells. Folding of the retina produced rosette-like images similar to those reported before in the retina of nocturnal mammals and in the avian pineal gland. CONCLUSIONS These data suggest that the retina of the mole rat has undergone evolutionary restructuring to a photoreceptive pineal-like organization. This supports the thesis that the photoreceptor cells of this unique organ have been reprogrammed during the subterranean adaptation of Spalax, from their original visual function to mediating photoperiodic regulation.

[1]  R. Foster,et al.  Opsin localization and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis , 1993, Journal of Comparative Physiology A.

[2]  M. Menaker,et al.  Circadian photoreception in the retinally degenerate mouse (rd/rd) , 1991, Journal of Comparative Physiology A.

[3]  D. Farner,et al.  Electron microscopic and experimental studies of the pineal organ in the white-crowned sparrow, Zonotrichia leucophrys gambelii , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[4]  A. Oksche,et al.  Elektronenmikroskopische Untersuchungen am Pinealorgan von Passer domesticus , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[5]  H. Burda Adaptive Radiation of Blind Subterranean Mole Rats , 2002, Heredity.

[6]  E. Nevo,et al.  Biological clock in total darkness: The Clock/MOP3 circadian system of the blind subterranean mole rat , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Á. Szél,et al.  Comparative ultrastructure and cytochemistry of the avian pineal organ , 2001, Microscopy research and technique.

[8]  E. Nevo,et al.  The lens protein alpha-B-crystallin of the blind subterranean mole-rat: high homology with sighted mammals. , 2001, Gene.

[9]  E. Nevo,et al.  Adaptive radiation of blind subterranean mole rats : naming and revisiting the four sibling species of the Spalax ehrenbergi superspecies in Israel: Spalax galili ( 2n=52), S. golani (2n=54), S. carmeli (2n=58), and S. judaei (2n=60) , 2001 .

[10]  Á. Szél,et al.  Pineal organ-like organization of the retina in megachiroptean bats. , 2001, Acta biologica Hungarica.

[11]  Izzo,et al.  SUPPRESSION OF MELATONIN SECRETION IN SOME BLIND PATIENTS BY EXPOSURE TO BRIGHT LIGHT , 2001 .

[12]  J. Bowmaker,et al.  A Fully Functional Rod Visual Pigment in a Blind Mammal , 2000, The Journal of Biological Chemistry.

[13]  H. Wässle,et al.  Immunocytochemical analysis of the mouse retina , 2000, The Journal of comparative neurology.

[14]  Heinz Wässle,et al.  The Cone Pedicle, a Complex Synapse in the Retina , 2000, Neuron.

[15]  G. Häcker The morphology of apoptosis , 2000, Cell and Tissue Research.

[16]  E. Nevo,et al.  Spectral tuning of a circadian photopigment in a subterranean ‘blind’ mammal (Spalax ehrenbergi) , 1999, FEBS Letters.

[17]  S. Massey,et al.  Antibody to calretinin stains AII amacrine cells in the rabbit retina: Double‐label and confocal analyses , 1999, The Journal of comparative neurology.

[18]  M. Barinaga,et al.  The Clock Plot Thickens , 1999, Science.

[19]  R. Foster,et al.  Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. , 1999, Science.

[20]  R. Foster,et al.  Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. , 1999, Science.

[21]  E. Nevo Mosaic Evolution of Subterranean Mammals: Regression, Progression, and Global Convergence , 1999 .

[22]  Á. Szél,et al.  The pineal organ as a folded retina: immunocytochemical localization of opsins. , 1998, Biology of the cell.

[23]  R. Foster,et al.  Light detection in a 'blind' mammal , 1998, Nature Neuroscience.

[24]  H. Kolb,et al.  Uniqueness of the S‐cone pedicle in the human retina and consequences for color processing , 1997, The Journal of comparative neurology.

[25]  L. Vollrath,et al.  Plasticity of retinal ribbon synapses , 1996, Microscopy research and technique.

[26]  E. Brambilla,et al.  In situ apoptotic cell labeling by the TUNEL method: improvement and evaluation on cell preparations. , 1996, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[27]  R. Foster,et al.  The spatio-temporal pattern of photoreceptor degeneration in the aged rd/rd mouse retina , 1996, Cell and Tissue Research.

[28]  Heinz Wässle,et al.  The rod pathway of the macaque monkey retina: Identification of AII‐amacrine cells with antibodies against calretinin , 1995, The Journal of comparative neurology.

[29]  M. Herbin,et al.  Photic induction of Fos immunoreactivity in the suprachiasmatic nuclei of the blind mole rat (Spalax ehrenbergi) , 1994, Brain Research.

[30]  R. Foster,et al.  Visual and circadian responses to light in aged retinally degenerate mice , 1994, Vision Research.

[31]  H. Kolb,et al.  Horizontal cells and cone photoreceptors in primate retina: A Golgi‐light microscopic study of spectral connectivity , 1994, The Journal of comparative neurology.

[32]  E. Nevo,et al.  Visual system of a naturally microphthalmic mammal: The blind mole rat, Spalax ehrenbergi , 1993, The Journal of comparative neurology.

[33]  Eviatar Nevo,et al.  Ocular regression conceals adaptive progression of the visual system in a blind subterranean mammal , 1993, Nature.

[34]  G. Bronchti,et al.  Retinal projections in the blind mole rat: a WGA-HRP tracing study of a natural degeneration. , 1991, Brain research. Developmental brain research.

[35]  J. Grim Whorl-like outer segments in the retina of the mole (Scalopus aquaticus). , 1990, Acta anatomica.

[36]  F. Blachier,et al.  Calbindin and calretinin localization in retina from different species , 1990, Visual Neuroscience.

[37]  E. Nevo,et al.  The eye of the blind mole rat, Spalax ehrenbergi. Rudiment with hidden function? , 1990, Investigative ophthalmology & visual science.

[38]  H. Kolb,et al.  Identification of pedicles of putative blue‐sensitive cones in the human retina , 1990, The Journal of comparative neurology.

[39]  H. Jansen,et al.  Development and degeneration of retina in rds mutant mice: ultraimmunohistochemical localization of opsin. , 1987, Experimental eye research.

[40]  W. D. de Grip,et al.  Enzyme-linked immunosorbent assay for quantitative determination of the visual pigment rhodopsin in total-eye extracts. , 1986, Experimental eye research.

[41]  R. Molday,et al.  Differential immunogold-dextran labeling of bovine and frog rod and cone cells using monoclonal antibodies against bovine rhodopsin. , 1986, Experimental eye research.

[42]  E. Nevo,et al.  Photoperiod perception in the blind mole rat (Spalax ehrenbergi, Nehring): involvement of the Harderian gland, atrophied eyes, and melatonin. , 1984, The Journal of experimental zoology.

[43]  L. Vollrath The Pineal Organ , 1981 .

[44]  M. Lavail,et al.  Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy , 1979, The Journal of comparative neurology.

[45]  Helga Kolb,et al.  The connections between horizontal cells and photoreceptors in the retina of the cat: Electron microscopy of Golgi preparations , 1974, The Journal of comparative neurology.

[46]  H. Pease,et al.  On understanding the organisation of the retinal receptor synapses. , 1971, Brain research.

[47]  A. Oksche,et al.  [Electron microscopic studies of the pineal organ in Passer domesticus]. , 1969, Zeitschrift fur Zellforschung und mikroskopische Anatomie.