The Photoreceptor Populations in the Retina of the Greater Horseshoe Bat Rhinolophus ferrumequinum

  • Kim, Tae-Jin (Department of Biology, College of Natural Sciences, Kyungpook National University) ;
  • Jeon, Young-Ki (Department of Biology, College of Natural Sciences, Kyungpook National University) ;
  • Lee, Jea-Young (Department of Biology, College of Natural Sciences, Kyungpook National University) ;
  • Lee, Eun-Shil (Department of Biology, College of Natural Sciences, Kyungpook National University) ;
  • Jeon, Chang-Jin (Department of Biology, College of Natural Sciences, Kyungpook National University)
  • Received : 2008.04.16
  • Accepted : 2008.06.27
  • Published : 2008.10.31

Abstract

Recently, we reported the existence of AII "rod" amacrine cells in the retina of the greater horseshoe bat Rhinolophus ferrumequinum (Jeon et al., 2007). In order to enhance our understanding of bat vision, in the present study, we report on a quantitative analysis of cone and rod photoreceptors. The average cone density was $9,535cells/mm^2$, giving a total number of cones of 33,538 cells/retina. The average rod density was $368,891cells/mm^2$, giving a total number of rods of 1,303,517 cells. On average, the total populations of rods were 97.49%, and cones were 2.51% of all the photoreceptors. Rod: cone ratios ranged from 33.85:1 centrally to 42.26:1 peripherally, with a mean ratio of 38.96:1. The average regularity index of the cone mosaic in bat retina was 3.04. The present results confirm the greater horseshoe bat retina to be strongly rod-dominated. The rod-dominated retina, with the existence of AII cells discovered in our previous study, strongly suggests that the greater horseshoe bat retina has a functional scotopic property of vision. However, the existence of cone cells also suggests that the bat retina has a functional photopic property of vision.

Keywords

Acknowledgement

Supported by : Korea Science and Engineering Foundation

References

  1. Altringham, J. (1996). Bats: Biology and Behaviour. (New York, USA: OUP)
  2. Andrade da Costa, B L., and Hokoç, J. (2000). Photoreceptor topography of the retina in the new world monkey Cebus apella. Vision Res. 40, 2395-2409 https://doi.org/10.1016/S0042-6989(00)00104-8
  3. Beaudet, L., Novales Flamarique, I., and Hawryshyn, C.W. (1997). Cone photoreceptor topography in the retina of sexually mature Pacific salmonid fishes. J. Comp. Neurol. 383, 49-59 https://doi.org/10.1002/(SICI)1096-9861(19970623)383:1<49::AID-CNE4>3.0.CO;2-L
  4. Blanks, J.C., and Johnson, L.V. (1984). Specific binding of peanut lectin to a class of retinal photoreceptor cells. A species comparison. Invest. Ophthalmol. Vis. Sci. 25, 546-557
  5. Bridges, C.D. (1981). Lectin receptors of rods and cones. Visualization by fluorescent label. Invest. Ophthalmol. Vis. Sci. 20, 8-16
  6. Brudenall, D.K., Schwab, I.R., Lloyd III, W., Giorgi, P.P., and Graydon, M.L. (2007). Optimized architecture for nutrition in the avascular retina of megachiroptera. Anat. Histol. Embryol. 36, 382-388 https://doi.org/10.1111/j.1439-0264.2007.00779.x
  7. Chandler, M.J., Smith, P.J., Samuelson, D.A., and Mackay, E.O. (1999). Photoreceptor density of the domestic pig retina. Vet. Ophthalmol. 2, 179-184 https://doi.org/10.1046/j.1463-5224.1999.00077.x
  8. Chase, J. (1982). The evolution of retinal vascularization in mammals. A comparison of vascular and avascular retinae. Ophthalmology 89, 1518-1525 https://doi.org/10.1016/S0161-6420(82)34608-4
  9. Curcio, C.A., Sloan, J.K.R., Packer, O., Hendrickson, A.E., and Kalina, R.E. (1987). Distribution of cones in human and monkey retina: Individual variability and radial asymmetry. Science 236, 579-582 https://doi.org/10.1126/science.3576186
  10. Curcio, C.A., Sloan, K.R., Kalina, R.E., and Hendrickson, A.E. (1990). Human photoreceptor topography. J. Comp. Neurol. 292, 497-523 https://doi.org/10.1002/cne.902920402
  11. Dartnall, H.J., Bowmaker, J.K., and Mollon, J.D. (1983). Human visual pigments: Microspectrophotometric results from the eyes of seven persons. Proc. R. Soc. Lond. B. Biol. Sci. 220, 115-130
  12. Fei, Y. (2003). Development of the cone photoreceptor mosaic in the mouse retina revealed by fluorescent cones in transgenic mice. Mol. Vis. 9, 31-42
  13. Fure, A. (2006). Bats and lighting. The London Naturalist. 85, 1-20
  14. Glosmann, M., Steiner, M., Peichl, L., and Ahnelt, P.K. (2008). Cone photoreceptors and potential UV vision in a subterranean insectivore, the European mole. J. Vis. 8, 23.1-12
  15. Govardovskii, V.I., Rohlich, P., Szel, A., and Khoklova, T.V. (1992). Cones in the retina of the Mongolian gerbil, Meriones unguiculatus; an immunocytochemical and electrophysiological study. Vision Res. 32, 19-27 https://doi.org/10.1016/0042-6989(92)90108-U
  16. Graydon, M.L., Giorgi, P.P., and Pettigrew, J.D. (1987). Vision in flying foxes (Chiroptera: Pteropodidae). Aust. Mammal. 10, 102-106
  17. Hallett, P.E. (1987). The scale of the visual pathways of mouse and rat. Biol. Cybern. 57, 275-286 https://doi.org/10.1007/BF00338820
  18. Hirsch, J., and Miller, W.H. (1987). Does cone positional disorder limit resolution? J. Opt. Soc. Am. 4, 1481-1492 https://doi.org/10.1364/JOSAA.4.001481
  19. Hubel, D.H. (1988). Eye, Brain, and Vision. (New York: Scientific American Library)
  20. Hughes, A. (1971). Topographical relationships between the anatomy and physiology of the rabbit visual system. Doc. Ophthalmol. 30, 33-159 https://doi.org/10.1007/BF00142518
  21. Hughes, A. (1975). A quantitative analysis of the cat retinal ganglion cell topography. J. Comp. Neurol. 163, 107-128 https://doi.org/10.1002/cne.901630107
  22. Jacobs, G.H. (1981). Comparative Color Vision. (New York: Academic)
  23. Jacobs, G.H., Fenwick, J.A., and Williams, G.A. (2001). Cone-based vision of rats for ultraviolet and visible lights. J. Exp. Biol. 204, 2439-2446
  24. Jeon, C.J., Strettoi, E., and Masland, R.H. (1998). The major cell populations of the mouse retina. J. Neurosci. 18, 8936-8946 https://doi.org/10.1523/JNEUROSCI.18-21-08936.1998
  25. Jeon, Y.K., Kim, T.J., Lee, J.Y., Choi, J.S., and Jeon, C.J. (2007). All amacrine cells in the inner nuclear layer of bat retina: identification by parvalbumin immunoreactivity. Neuroreport 18, 1095-1099 https://doi.org/10.1097/WNR.0b013e3281e72afe
  26. Jones, G., and Rayner, J.M.V. (1989). Foraging behavior and echolocation of wild horseshoe bats Rhinolophus ferrumequinum and R. hipposideros (Chiroptera, Rhinolophidae). Behav. Ecol. Sociobiol. 25, 183-191 https://doi.org/10.1007/BF00302917
  27. Kawamura, S., and Tachibanaki, S. (2008). Rod and cone photoreceptors: Molecular basis of the difference in their physiology. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 150, 369-377 https://doi.org/10.1016/j.cbpa.2008.04.600
  28. Kolb, H., and Wang, H.H. (1985). The distribution of photoreceptor, dopaminergic amacrine cells and ganglion cells in the retina of the North American opossum (Didelphis virginiana). Vis. Res. 25, 1207-1221 https://doi.org/10.1016/0042-6989(85)90035-5
  29. Kryger, Z., Galli-Resta, L., Jacobs, G.H., and Reese, B.E. (1998). The topography of rod and cone photoreceptors in the retina of the ground squirrel. Vis. Neurosci. 15, 685-691
  30. Lopez-Lopez, R., Lopez-Gallardo, M., Perez-Alvarez, M.J., and Prada, C. (2008). Isolation of chick retina cones and study of their diversity based on oil droplet colour and nucleus position. Cell Tissue Res. 332, 13-24 https://doi.org/10.1007/s00441-007-0572-6
  31. Matthew, J.C., Patricia, J.S., Don, A.S., and Edward, O.M. (1999). Photoreceptor density of the domestic pig retina. Vet. Ophthalmol. 2, 179-184 https://doi.org/10.1046/j.1463-5224.1999.00077.x
  32. Müller, B., Goodman, S.M., and Peichl, L. (2007). Cone photoreceptor diversity in the retinas of fruit bats (megachiroptera). Brain Behav. Evol. 70, 90-104 https://doi.org/10.1159/000102971
  33. Nemec, P., Cvekova, P., Benada, O., Wielkopolska, E., Olkowicz, S., Turlejski, K., Burda, H., Bennett, N.C., and Peichl, L. (2008). The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): Retina, subcortical visual nuclei and primary visual cortex. Brain Res. Bull. 75, 356-364 https://doi.org/10.1016/j.brainresbull.2007.10.055
  34. Nowak, R. (1994). Walker's Bats of the World (Baltimore: The John Hopkins University Press)
  35. Packer, O., Hendrickson, A.E., and Curcio, C.A. (1989). Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina). J. Comp. Neurol. 288, 165-183 https://doi.org/10.1002/cne.902880113
  36. Peichl, L. (2005). Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat. Rec. A 287, 1001-1012
  37. Petry, H.M., Erichsen, J.T., and Szel, A. (1993). Immunocytochemical identification of photoreceptor populations in the tree shrew retina. Brain Res. 616, 344-350 https://doi.org/10.1016/0006-8993(93)90230-K
  38. Pugh, E.N. Jr., Lyubarsky, A.L., Faisini, B., Valentini, P., and Pennisi, M. (1998). UV- and M-cone pathways in the mouse retina are linked. Invest. Ophthalmol. Vis. Sci. 39, S974
  39. Radhakrishna, S. (2005). Midnight's children?: solitary primates and gregarious chiropterans. Curr. Sci. 89, 7-10
  40. Ransome, R.D. (1968). The distribution of the greater horseshoe bat, Rhinolophus ferrumequinum, during hibernation, in relation to environmental factors. J. Zool. Lond. 154, 77-112 https://doi.org/10.1111/j.1469-7998.1968.tb05040.x
  41. Ransome, R.D., and Hutson, A.M. (2000). Action plan for the conservation of the greater horseshoe bat in Europe (Rhinolopus ferrumequinum). Nature Environment 109, Council & Europe Publishing
  42. Rodieck, R.W. (1998). The first steps in seeing. (Sunderland: Sinauer Associates)
  43. Steinberg, R.H., Reid, M., and Lacy, P.L. (1973). The distribution of rods and cones in the retina of the cat (Felis domesticus). J. Comp. Neurol. 148, 229-248 https://doi.org/10.1002/cne.901480209
  44. Szel, A., and Rohlich, P. (1988). Four photoreceptor types in the ground squirrel retina as evidenced by immunocytochemistry. Vision Res. 28, 1297-1302 https://doi.org/10.1016/0042-6989(88)90060-0
  45. Szel, A., and Rohlich, P. (1992). Two cone types of rat retina detected by antivisual pigment antibody. Exp. Eye Res. 55, 47-52 https://doi.org/10.1016/0014-4835(92)90090-F
  46. Szel, A., Rohlich, P., Caffe, A.R., and van, Veen, T. (1996). Distribution of cone photoreceptors in the mammalian retina. Microsc. Res. Tech. 35, 445-462 https://doi.org/10.1002/(SICI)1097-0029(19961215)35:6<445::AID-JEMT4>3.0.CO;2-H
  47. Tachibanaki, S., Shimauchi-Matsukawa, Y., Arinobu, D., and Kawamura, S. (2007). Molecular mechanisms characterizing cone photoresponses. Photochem. Photobiol. 83, 19-26
  48. Thibos, L.N., Walsh, D.J., and Cheney, F.E. (1987). Vision beyond the resolution limit: aliasing in the periphery. Vision Res. 27, 2193-2197 https://doi.org/10.1016/0042-6989(87)90134-9
  49. Umino, Y., Solessio, E., and Barlow, R.B. (2008). Speed, spatial, and temporal tuning of rod and cone vision in mouse. J. Neurosci. 28, 189-198 https://doi.org/10.1523/JNEUROSCI.3551-07.2008
  50. Wang, D., Oakley, T., Mower, J., Shimmin, L.C., Yim, S., Honeycutt, R.L., Tsao, H., and Li, W.H. (2004). Molecular evolution of bat color vision genes. Mol. Biol. Evol. 21, 295-302 https://doi.org/10.1093/molbev/msh015
  51. Wassle, H., and Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proc. R. Soc. Lond. B. Biol. Sci. 200, 441-461
  52. Wikler, K.C., and Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diuranal and nocturnal primates. J. Neurosci. 10, 3390-3401 https://doi.org/10.1523/JNEUROSCI.10-10-03390.1990
  53. Wilker, K.C., Williams, R.W., and Pakic, P. (1990). Photoreceptor mosaic: number and distribution of rods and cones in the rhesus monkey retina. J. Comp. Neurol. 297, 499-508 https://doi.org/10.1002/cne.902970404
  54. Williams, D.R., and Colletta, N.J. (1987). Cone spacing and the visual resolution limit. J. Opt. Soc. Am. 4, 1514-1523 https://doi.org/10.1364/JOSAA.4.001514
  55. Winter, Y., Lopez, J., and Von, Helversen, O. (2003). Ultraviolet vision in a bat. Nature 425, 612-614 https://doi.org/10.1038/nature01971