Retinal neurogenesis and ontogenetic changes in the visual system of the brown banded bamboo shark, Chiloscyllium punctatum (hemiscyllidae, elasmobranchii)

Journal of Comparative Neurology

Volumn 513, Issue 1, 2009, Pages 83-97

  Harahush, Blake K ^a   Hart, Nathan S ^a   Green, Kathryn ^a   Collin, Shaun P ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Cell differentiation; Development; Elasmobranch; Eye growth; Eye ontogenesis; Retina

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EGG LAYING; ELASMOBRANCHII; EYE DEVELOPMENT; GESTATION PERIOD; HATCHING; MICROSCOPY; MUELLER CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; ONTOGENY; OVIPARITY; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA CELL; RETINA CONE; RETINA DEVELOPMENT; RETINA GANGLION CELL; RETINA HORIZONTAL NERVE CELL; RETINA ROD; SYNAPSE; TRANSMISSION ELECTRON MICROSCOPY; VERTEBRATE; ANIMAL; EYE; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LENS; MORPHOGENESIS; PHYSIOLOGY; PRENATAL DEVELOPMENT; RETINA; SHARK; ULTRASTRUCTURE; VISUAL SYSTEM;

ANIMALS; CELL DIFFERENTIATION; EYE; LENS, CRYSTALLINE; MORPHOGENESIS; NEUROGENESIS; RETINA; SHARKS; VISUAL PATHWAYS;

EID: 59649099844     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21953     Document Type: Article

References (97)

1. Ahlbert I. 1973. Ontogeny of double cones in the retina of perch fry ( P. fluviatilis, Teleostei). Acta Zool 54:241-254.
2. Ali MA, Anctil M. 1974. Retinas of the electric ray (Narcine brasiliensis) and the freshwater stingray (Paratrygon motoro). Vis Res 14:587-588.
3. Ali MA, Klyne MA. 1985. Vision in vertebrates. New York: Plenum Press. 272 p.
4. Altman J. 1970. Postnatal neurogenesis and the problem of neural plasticity. In: Himwich WA, editor. Developmental neurobiology. Springfield, IL: Thomas. p 197-237.
5. Altshuler DM, Turner DL, Cepko CL. 1991. Specification of cell type in the vertebrate retina. In: Lam DMK, Shatz CJ, editors. Development of the visual system: Cambridge, MA: MIT Press. p 37-78.
6. Anderson DH, Neitz J, Saari JC, Kaska DD, Fenwick J, Jacobs GH, Fisher SK. 1986. Retinoid-binding proteins in the cone-dominant retinas. Invest Ophthalmol Vis Sci 27:1015-1026.
7. Bailes HJ, Trezise AEO, Collin SP. 2007. The optics of the growing lungfish eye: lens shape, focal ratio and pupillary movements in Neoceratodus forsteri (Krefft, 1870). Vis Neurosci 24:377-387.
8. Bantseev KL, Moran KL, Dixon DG, Sivak JG. 2004. Optical properties, mitochondria, and sutures of lenses of fishes: a comparative study of nine species. Can J Zool 82:86-93.
9. Bhattacharjee J, Sanyal S. 1975. Developmental origin and early differentiation of retinal Müller cells in mice. J Anat 120:367-372.
10. Blanks JC, Bok D. 1977. An autoradiographic analysis of postnatal cell proliferation in the normal and degenerative mouse retina. J Comp Neurol 174:317-328.
11. Blaxter JHS, Pattie Jones M. 1967. The development of the retina and retinomotor responses in the herring. J Mar Biol Assoc U K 47:677-697.
12. Branchek T, Bremiller R. 1984. The development of photoreceptors in the zebrafish, Brachydanio rerio. I. Structure. J Comp Neurol 224:107-115.
13. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A. 2006. Müller cells in the healthy and diseased retina. Prog Ret Eye Res 25:397-424.
14. Chang WS, Harris WA. 1998. Sequential genesis and determination of cones and rod photoreceptors in Xenopus. J Neurobiol 35:227-244.
15. Cheon EW, Kaneko Y, Saito T. 1998. Regeneration of the newt retina: order of appearance of photoreceptors and ganglion cells. J Comp Neurol 396:267-274.
16. Collin SP, Fritzsch B. 1993. Observations on the shape of the lens in the eye of the silver lamprey, Ichthyomyzon unicuspis. Can J Zool 71:34-41.
17. Collin SP, Pettigrew JD. 1988. Retinal topography in reef teleosts. I. Some species with well developed areae but poorly developed streaks. Brain Behav Evol 31:269-282.
18. Collin SP, Potter IC, Braekevelt CR. 1999. The ocular morphology of the southern hemisphere lamprey Geotria australis Gray, with special reference to optical specialisations and the characterisation and phylogeny of photoreceptor types. Brain Behav Evol 54:96-118.
19. Dahm R, Schonthaler HB, Soehn AS, van Marle J, Vrensen GFJM. 2007. Developmental and adult morphology of the eye lens in the zebrafish. Exp Eye Res 85:74-89.
20. De Miguel E, Anadón R. 1987. The development of retina and the optic tectum of Petromyzon marinus L. A light microscopic study. J Hirnforschung 28:445-456.
21. Distler C, Dreher Z. 1996. Glia cells of the monkey retina-II. Müller cells. Vision Res 36(16):2381-2394.
22. Douglas RH, Collin SP, Corrigan J. 2002. The eyes of suckermouth armoured catfish (Loricariidae, subfamily Hypostpmus): pupil response, lenticular longitudinal spherical aberration and retinal topography. J Exp Biol 205:3424-3433.
23. Duke-Elder S. 1958. The eye in evolution. In: Duke-Elder S, editor. System of ophthalmology. London: Henry Kimpton. p 1-843.
24. Easter SS Jr, Nicola GN. 1996. The development of vision in the zebrafish (Danio rerio). Dev Biol 180:646-663.
25. Fernald RD. 1989. Fish vision. In: Finlay BL, Sengelaub DR, editors. Development of the vertebrate retina. New York: Plenum Press. p 247-265.
26. Fernald RD, Wright SE. 1985. Growth of the visual system in the African cichlid fish, Haplochromis burtoni. Vis Res 25:163-170.
27. Fischer AJ, Reh TA. 2001. Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci 4:247-252.
28. Fishelson L, Baranes A. 1999. Ocular development in the oman shark, Iago omanensis (Triakidae), Gulf of Aqaba, Red Sea. Anat Rec 256:389-402.
29. Francke M, Makarov F, Kacza J, Wendt S, Gärtner U, Faude F, Wiedemann P, Reichenbach A. 2001. Retinal pigment epithelium melanin granules are phagocytozed by Müller glial cells in experimental retinal detachment. J Neurocytol 30:131-136.
30. Garamszegi LZ, Moller AP, Erritzoe J. 2002. Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proc R Soc Lond B Biol Sci 269:961-967.
31. Gilbert PW. 1963. The visual apparatus in sharks. In: Gilbert PW, editor. Sharks and survival. Boston: Health. p 283-326.
32. Gruber SH, Hamasaki DH, Bridges CDB. 1963. Cones in the retina of the lemon shark (Negaprion brevirostris). Vis Res 3:397-399.
33. Hagedorn M, Fernald RD. 1992. Retinal growth and cell addition during embryogenesis in the teleost Haplochromis burtoni. J Comp Neurol 321:193-208.
34. Harahush BH, Fischer AB, Collin SP. 2007. Captive breeding and embryonic development of Chiloscyllium punctatum Muller & Henle, 1838 (Elasmobranchii: Hemiscyllidae). J Fish Biol 71:1007-1022.
35. Harman AM, Beazley LD. 1989. Generation of retinal cells in the wallaby, Setonix brachyurus (Quokka). Neuroscience 28:219-232.
36. Hart NS, Lisney TJ, Collin SP. 2006. Visual communication in elasmobranchs. In: Ladich F, Collin SP, Moller P, Kapoor BG, editors. Communication in fishes. Enfield: Science Publishers Inc. p 337-392.
37. Hollyfield JG. 1972. Histogenesis of the retina in the killifish, Fundulus heteroclitus. J Comp Neurol 144:373-380.
38. Holt CE, Bertsch TW, Ellis HM, Harris WA. 1988. Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1:15-26.
39. Howland HC, Merola S, Basarab JR. 2004. The allometry and scaling of the size of the vertebrate eyes. Vis Res 44:2043-2065.
40. Huber R, van Staaden MJ, Kaufman LS, Liem KF. 1997. Microhabitat use, trophic patterns, and the evolution of brain structure in African cichlids. Brain Behav Evol 50:167-182.
41. Hueter RE. 1980. Physiological optics of the eye of the juvenile lemon shark (Negaprion brevirostris). MS dissertation. Miami: University of Miami. 145 p.
42. Jacobson M. 1970. Developmental neurobiology. New York: Holt, Rinehart and Winston. 465 p.
43. Kahn AJ. 1974. An autoradiographic analysis of the time of appearance of neurons in the developing chick neural retina. Dev Biol 18:163-179.
44. Kobayashi S, Morgans CW, Casey JR, Kopito RR. 1994. AE3 anion exchanger isoforms in the vertebrate retina: developmental regulation and differential expression in neurons and glia. J Neurosci 14:6266-6279.
45. Kuwabara T, Weidman TA. 1974. Development of the prenatal rat retina. Invest Ophthalmol 13:725-739.
46. Lamb TD, Collin SP, Pugh EN. 2007. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev 8:960-975.
47. Last PR, Stevens JD. 1994. Longtail carpet sharks. In: Veroni M, editor. Sharks and rays of Australia. Australia: CSIRO. p 135.
48. LaVail MM, Rapaport DH, Rakic P. 1991. Cytogenesis in the monkey retina. J Comp Neurol 309:86-114.
49. Leuckart RKGF. 1876. Organologie des Auges. Vergleichende Anatomie. In: Graefe-Saemisch, editor. I Handbuch der Gesamten Augenheilkunde. Leipzig: Engelmann. p 145-301.
50. Linser P, Moscona AA. 1979. Induction of glutamine synthetase in embryonic neural retina: localization in Müller fibers and dependence on cell interactions. Proc Natl Acad Sci U S A 76:6476-6480.
51. Linser PJ, Moscona AA. 1982. Carbonic anhydrase-C in neural retina of the chick embryo: developmental changes in cellular localization. Prog Clin Biol Res 85:459-471.
52. Lisney T. 2004. Neuroethology and vision in elasmobranchs. PhD Thesis, St. Lucia: University of Queensland.
53. Lisney TJ, Collin SP. 2007. Relative eye size in elasmobranchs. Brain Behav Evol 69:266-279.
54. Malicki J. 2004. Cell fate decisions and patterning in the vertebrate retina: the importance of timing, asymmetry, polarity and waves. Curr Opin Neurobiol 14:15-21.
55. Mann I. 1969. The development of the human eye. New York: Grune and Stratton. 1-316 p.
56. Mano T, Puro DG. 1990. Phagocytosis by human retinal glial cells in culture. Invest Ophthalmol Vis Sci 31:1047-1055.
57. Marquardt T, Gruss P. 2002. Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci 25:32-38.
58. Mathis U, Schaeffel F, Howland HC. 1988. Visual optics in toads (Bufo americanus). J Comp Physiol 163:201-213.
59. Miller TJ, Crowder LB, Rice JA. 1993. Ontogenetic changes in behavioural and histological measures of visual acuity in three species of fish. Environ Biol Fishes 37:1-8.
60. Molnar ML, Stefansson K, Molnar GK, Tripathi RC, Marton LS. 1985. Species variations in distribution of S100 in retina: demonstration with a monoclonal antibody and a polyclonal antiserum. Invest Ophthalmol Vis Sci 26:283-288.
61. Munk O. 1984. Non-spherical lenses in the eyes of some deep sea teleosts. Arch Fischereiwissenschaft 34:145-153.
62. Munk O. 1986. A multifocal lens in the eyes of mesopelagic teleosts Traipterus tracypterus (Gmelin, 1789) and T. arcticus (Brunich, 1771). Arch Fischereiwissenschaft 37:43-57.
63. Newman EA, Reichenbach A. 1996. The Müller cell: a functional element of the retina. Trends Neurosci 19:307-317.
64. Novales Flamarique I, Hawryshyn CW. 1996. Retinal development and visual sensitivity of young Pacific sockeye salmon (Oncorhynchus nerka). J Exp Biol 199:869-882.
65. Olson AJ, Picones A, Julian D, Korenbrot JI. 1999. A developmental time line in a retinal slice from rainbow trout. J Neurosci Methods 93:91-100.
66. Peterson RE, Fadool JM, McClintock J, Linser PJ. 2001. Müller cell differentiation in the zebrafish neural retina: evidence of distinct early and late stages in cell maturation. J Comp Neurol 429:530-540.
67. Pettigrew JD, Collin SP. 1995. Terrestrial optics in an aquatic eye: the sandlance Limnichthyes fasciatus (Creeidae, Teleostei). J Comp Physiol A177:397-408.
68. Prada FA, Magalhaés MM, Coimbra A, Genis-Galvez JM. 1989. Morphological differentiation of the Müller cell: Golgi and electron microscopy study in the chick retina. J Morphol 201:11-22.
69. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61-84.
70. Ramon y Cajal S. 1892. La retina de los teleosteos y algunas observaciones sobre la de los vertebrados superiores. An Soc Hist Nat 21:281-305.
71. Rapaport DH. 2006. Retinal neurogenesis. In: Sernagor E, Eglen S, Harris B, Wong R, editors. Retinal development. Cambridge: Cambridge University Press. p 30-58.
72. Rapaport DH, Wong LL, Wood ED, Yasumura D, LaVail MM. 2004. Timing and topography of cell genesis in the rat retina. J Comp Neurol 474:304-324.
73. Raymond PA. 1985. Cytodifferentiation of photoreceptors in larval goldfish: delayed maturation of rods. J Comp Neurol 236:90-105.
74. Reichenbach A, Reichelt W. 1986. Postnatal development of radial glial (Müller) cells of the rabbit retinal. Neurosci Lett 71:125-130.
75. Reichenbach A, Stolzenburg JU, Eberhardt W, Chao TI, Dettmer D, Hertz L. 1993. What do retinal Müller (glial) cells do for their neuronal "small siblings"? J Chem Neuroanat 6:201-213.
76. Reichenbach A, Frömter C, Engelmann R, Wolburg H, Kasper M, Schnitzer J. 1995. Müller glial cells of the tree shrew retina. J Comp Neurol 360:257-270.
77. Robinson SR, Dreher Z. 1990. Müller cells in adult rabbit retinae: Morphology, distribution and implications for function and development. J Comp Neurol 292:178-192.
78. Rochon-Duvigneaud A. 1943. Les yeux des reptiles - les sauriens. In: Les yeux et la vision des vertébré's. Paris: Masson et Cie. p 391-418.
79. Rodicio MC, Pombal MA, Anadón R. 1995. Early development and organization of the retinopetal system in the larval sea lamprey, Petromyzon marinus L. Anat Embryol 192:517-526.
80. Rubinson K. 1990. The developing visual system and metamorphosis in the lamprey. J Neurobiol 21:1123-1135.
81. Schmechel DE, Rakic P. 1979. A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol 156:115-152.
82. Schmitt EA, Dowling JE. 1999. Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J Comp Neurol 404:515-536.
83. Schmitt E, Kunz YW. 1989. Retinal morphogenesis in the rainbow trout, Salmo gairdneri. Brain Behav Evol 34:48-64.
84. Sharma SC, Ungar F. 1980. Histogenesis of the goldfish retina. J Comp Neurol 191:373-382.
85. Sivak JG. 1988. Optics of amphibious eyes in vertebrates. In: Atema J, Fay RR, Popper AN, Tavolga WN, editors. Sensory biology of aquatic animals. New York: Springer-Verlag. p 467-486.
86. Sivak JG. 1991. Elasmobranch visual optics. J Exp Zool Suppl 5:13-21.
87. Sivak JG, Luer CA. 1991. Optical development of the ocular lens of an elasmobranch, Raja eglanteria. Vis Res 31:373-382.
88. Sivak JG, Levy B, Weber AP, Glover RF. 1985. Environmental influence on shape of the crystalline lens: the amphibian example. Exp Biol 44:29-40.
89. Stolzenburg JU, Haas J, Härtig W, Paulke BR, Wolburg H, Reichelt W, Chao TI, Wolff JR, Reichenbach A. 1992. Phagocytosis of latex beads by rabbit retinal Müller (glial) cells in vitro. J Hirnforschung 33:557-564.
90. Tripathi RC, Tripathi BJ. 1983. Lens morphology, aging and cataract. Gerontology 38:258-270.
91. Uga S, Smelser GK. 1973. Electron microscope study of the development of retinal Müller cells. Invest Ophthalmol Vis Sci 12:295-307.
92. Villegas EDM, Dans MJD, Castillo CP-A, Alvarez RA. 1997. Development of the eye in the turbot Psetta maxima (Teleosti) from hatching through metamorphosis. J Morphol 233:31-42.
93. Wahl CM. 1994. Periodic cone cell twists in the walleye, Stizosteidon vitreum; a new type of retinomotor activity. Vis Res 34:11-18.
94. Walls GL. 1942. The vertebrate eye and its adaptive radiation. New York: Hafner.
95. White WT, Potter IC. 2004. Habitat partitioning among four elasmobranch species in nearshore, shallow waters of a subtropical embayment in Western Australia. Mar Biol 145:1023-1032.
96. Willbold E, Berger J, Reinicke M, Wolburg H. 1997. On the role of Müller glia cells in histogenesis: only retinal spheroids, but not tectal, telencephalic and cerebellar spheroids develop histotypical patterns. J Hirnforsch 38:383-396.
97. Young RW. 1985. Cell differentiation in the retina of the mouse. Anat Rec 212:199-205.