Development of visual projections follows an avian/mammalian-like sequence in the lizard Ctenophorus ornatus

Journal of Comparative Neurology

Volumn 453, Issue 1, 2002, Pages 71-84

  Dunlop, Sarah A ^a,b   Tee, Lisa B G ^b   Rodger, Jenny ^b   Harvey, Alan R ^a,b   Roberts, J Dale ^b   Beazley, Lynda D ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Optic pathways; Reptiles; Retinal ganglion cell

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; IMMUNOHISTOCHEMISTRY; LIZARD; NONHUMAN; OPTIC CHIASM; OPTIC NERVE; OPTIC TECTUM; PRIORITY JOURNAL; RETINA FOVEA; RETINA GANGLION CELL; VISUAL SYSTEM;

ANIMALS; EMBRYO, NONMAMMALIAN; GAP-43 PROTEIN; IMMUNOHISTOCHEMISTRY; LIZARDS; NEURONS; VISUAL PATHWAYS;

EID: 0037020706     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10394     Document Type: Article

References (118)

1. Barton RA. 1998. Visual specialisation and brain evolution in primates. Proc R Soc London [Biol] 265:1933-1937.
2. Beaver RS, Dunlop SA, Harman AM, Stirling RV, Easter SS, Roberts JD, Beazley LD. 2001. Continued neurogenesis is not a pre-requisite for regeneration of a topographic retino-tectal projection. Vis Res 41:1765-1770.
3. Beazley LD, Dunlop SA. 1983. The evolution of an area centralis and visual streak in the marsupial Setonix brachyurus. J Comp Neurol 216:211-231.
4. Beazley LD, Dunlop SA. 1999. Evolutionary hierarchy of optic nerve regeneration: implications for cell survival, axon outgrowth and map formation. In: Saunders NR, Dziegielwska KM, editors. Degeneration and regeneration in the nervous system. Singapore: Harwood Academic Publishers. p 119-152.
5. Beazley LD, Sheard PW, Tennant M, Starac D, Dunlop SA. 1997. Optic nerve regenerates but does not restore topographic projections in the lizard Ctenophorus ornatus. J Comp Neurol. 377:105-120.
6. Beazley LD, Tennant M, Stewart TM, Anstee SD. 1998. The primary visual system of adult lizards demonstrates that neurogenesis is not obligatorily linked to central nerve regeneration but may be a prerequisite for the restoration of maps in the brain. Vis Res 38:789-793.
7. Benowitz LI, Routtenberg A. 1987. A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism, and synaptic palsticity. TINS 10:527-532.
8. Bhide PG, Frost DO. 1992. Axon substitution in the reorganisation of developing connections. Proc Natl Acad Sci USA 89:11847-11851.
9. Bhide PG, Frost DO. 1999. Intrinsic determinants of retinal axon collateralization and arborization patterns. J Comp Neurol 411:119-129.
10. Blasco B, Avendano C, Cowada C. 1999. A stereological analysis of the lateral geniculate nucleus in adult Macaca nermstrina monkeys. Vis Neurosci 16:933-941.
11. Bunt SM, Lund RD. 1981. Development of a transient retino-retinal pathway in hooded and albino rats. Brain Res 211:399-404.
12. Bunt SM, Lund RD, Land P. 1983. Postnatal development of the optic projection in albino and hooded rats. Exp Brain Res 6:149-168.
13. Campbell G, So KF, Lieberman AR. 1984. Normal postnatal development of retinogeniculate axons and terminals and identification of inappropriately-located transient synapses. Neuroscience 13:743-759.
14. Chen P, Stirling RV, Rodger J, Beazley LD, Dunlop SA. 2002. Visual stimulation improves the outcome of optic nerve regeneration in the lizard, Ctenophorus ornatus. Proc Aust Neurosci Soc 13:60.
15. Coleman L-A, Dunlop SA, Beazley LD. 1984. Patterns of cell division during visual streak formation in the frog Limnodynastes dorsalis. J Embyol Exp Morphol 83:119-135.
16. Collin SP, Shand J, Tee LBG, Beazley LD. 2001. Transient ipsilateral projections in a developing teleost is related to the relocation of the area centralis. Proc Aust Neurosci Soc 12:179.
17. Cooper ML, Rakic P. 1983. Gradients of cellular maturation and synaptogenesis in the superior colliculus of the fetal rhesus monkey. J Comp Neurol 215:165-186.
18. Currie J, Cowan WM. 1974. Evidence for the late development of the uncrossed retinothalamic projections in the frog Rana pipiens. Brain Res 71:133-139.
19. Cusick CG, Kaas JH. 1982. Retinal projections in adult and newborn grey squirrels. Brain Res Dev Brain Res 4:275-284.
20. Drager U. 1985. Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse. Proc R Soc London [Biol] 224:57-77.
21. Dreher B, Sefton AJ, Ni SKY, Nisbett G. 1985. The morphology, number, distribution and central projections of class I retinal ganglion cells in albino and hooded rats. Brain Behav Evol 26:10-48.
22. Dunlop SA. 1990. Early development of retinal ganglion cell dendrites in the marsupial Setonix brachyurus. J Comp Neurol 29:425-447.
23. Dunlop SA, Beazley LD. 1981. Changing retinal ganglion cell distribution in the frog Heleioporus eyrei. J Comp Neurol 202:221-236.
24. Dunlop SA, Beazley LD. 1984. A morphometric study of the retinal ganglion cell layer and optic nerve from metamorphosis in Xenopus laevis. Vis Res 24:417-427.
25. Dunlop SA, Longley WA, Beazley LD. 1987. The development of the area centralis and visual streak in the grey kangaroo Macropus fuliginosus. Vis Res 27:151-164.
26. Dunlop SA, Tee LBG, Beazley LD. 2000a. Topographic order of retinofugal axons in a marsupial: implications for map formation in visual nuclei. J Comp Neurol 428:33-44.
27. Dunlop SA, Tran N, Papadimitriou J, Beazley LD. 2000b. Retinal projections throughout optic nerve regeneration in the lizard Ctenophorus ornatus. J Comp Neurol 416:188-200.
28. Ebbesson SOE. 1970. On the organisation of central visual pathways in vertebrates. Brain Behav Evol 3:178-194.
29. Finlay BL, Pallas SL. 1989. Control of cell number in the developing mammalian visual system. Progr Neurobiol 32:207-234.
30. Fraser SE. 1986. A physiological measure of shifting connections in the Rana pipiens retinotectal system. J Embryol Exp Morphol 94:149-161.
31. Fritzsch B, Wilm C. 1992. The development of ipsilateral retinal projections into the tectum in the cichlid fish Haplochromis bortoni: a DiI study in fixed tissue. J Neurobiol 23:708-719.
32. Frost DO. 1984. Axonal growth and target selection during development: retinal projections to the ventrobasal complex and other "nonvisual" structures in neonatal Syrian hamsters. J Comp Neurol 230:576-592.
33. Frost DO. 1986. Development of anomalous retinal projections to nonvisual thalamic nuclei in Syrian hamsters: a quantitative study. J Comp Neurol 252:95-105.
34. Frost DO, So K-F, Schneider GE. 1979. Postnatal development of retinal projections in Syrian hamsters: a study using autoradiographic and anterograde degeneration techniques. Neuroscience 4:1649-1677.
35. Gaze RM, Keating MJ, Ostberg A, Chung SH. 1979. The relationship between retinal and tectal growth in larval Xenopus: implications for the development of the retino-tectal projection. J Embryol Exp Morphol 53:103-143.
36. Giolli RA, Towns LC. 1980. A review of axon collateralization in the mammalian visual system. Brain Behav Evol 17:364-390.
37. Godemont P, Salaun J, Imbert M. 1984. Prenatal and postnatal devlopment of retinogeniculate and retinocollicular projections in the mouse. J Comp Neurol 230:552-573.
38. Godemont P, Salûn J, Mason CA. 1990. Retinal axon pathfinding in the optic chiasm: divergence of crossed nd uncrossed fibres. Neurona 5:173-186.
39. Goldberg JL, Barres BA. 2000. Nogo in nerve regeneration. Nature 403: 369-370.
40. Halfter W. 1987. Anterograde tracing of retinal axons in the avian embryo with low molecular weight derivatives of biotin. Dev Biol 119:322-335.
41. Harman AM, Beazley LD. 1986. Development of visual projections in the marsupial, Setonix brachyurus. Anat Embryol 175:181-188.
42. Harman AM, Beazley LD. 1989. Generation of retinal cells in the wallaby, Setonix brachyurus (quokka). Neuroscience 28:219-232.
43. Hedges SB, Mober KD, Maxson LR. 1990. Tetrapod phylogeny inferred from 18S and 28S ribosomal RNA sequences ansd a review of the evidence for Amniote relationships. Mol Biol Evol 7:607-633.
44. Hitchcock PF, Easter SS Jr. 1987 Evidence for centripetally shifting terminals on the tectum of postmetamorphic Rana pipiens. J Comp Neurol 266:556-564.
45. Holder N, Clarke JDW. 1988. Is there a correlation between continuous neurogenesis and directed axon regeneration in the vertebrate nervous system? TINS 11:94-99.
46. Holt CE. 1984. Does timing of axon ingrowth influence retinotectal topography in Xenopus? J Neurosci 4:1130-1152.
47. Holt CE. 1989. A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip. J Neurosci 9:3123-3145.
48. Hoskins S. 1986. Control of the development of the ipsilateral retinothalamic projection in Xenopus laevis by thyroxine: results and speculation. J Neurobiol 17:203-229.
49. Hoskins SG, Grobstein P. 1985a. Development of the ipsilateral retinothalamic projection in the frog Xenopus laevis. I. Retinal distribution of ipsilaterally projecting cells in normal and experimentally manipulated frogs. J Neurosci 5:911-919.
50. Hoskins SG, Grobstein P. 1985b. Development of the ipsilateral retinothalamic projection in the frog Xenopus laevis. II. Ingrowth of optic fibres and production of ipsilaterally projecting retinal ganglion cells. J Neurosci 5:920-929.
51. Hsiao K, Sachs GM, Schneider GE. 1984. A minute fraction of Syrian golden hamster retinal ganglion cells project bilaterally. J Neurosci 4:359-367.
52. Hutchinson MN, Donnellan SC. 1993. Biogeography and phylogeny of the Squamata. In: Glasby CJ, Ross GJB, Beesley P, editors. Fauna of Australia, vol 2A. Amphibia and Reptilia. Canberra: Australian Government Publishing Service. p 210-220.
53. Illing RB. 1980. Axonal bifurcation of cat retinal ganglion cells as demonstrated by retrograde double labelling with fluorescent dyes. Neurosci Lett 19:125-130.
54. Jacobson M. 1976. Histogenesis of the retina in the clawed frog with implications for the pattern of development of retinotectal connections. Brain Res 103:541-545.
55. Jacobson M. 1991. Developmental neurobiology. New York: Plenum Press.
56. Jeffrey G, Perry VH. 1982. Evidence for ganglion cell death during development of the ipsilateral retinal projection in the rat. Brain Res Dev Brain Res 2:176-180.
57. Jeffrey G, Cowey A, Kuypers HGJM. 1981. Bifurcating retinal ganglion cell axons in the rat, demonstrated by retrograde double labelling. Exp Brain Res 44:34-40.
58. Jen LS, Cheung YM, Chow KL. 1989. The origin and terminal arbors of individual uncrossed retinogeniculate fibers in rabbits. Neuroscience 29:479-493.
59. Jhaveri S, Edwards MA, Schneider GE. 1991. Initial stages of retinofugal axon development in the hamster: evidence for two distinct modes of growth. Exp Brain Res 87:371-382.
60. Johns PR. 1977. Growth of the adult goldfish eye. III. Source of new retinal cells. J Comp Neurol 176:343-358.
61. Johns PR, Easter SS. 1977. Growth of the adult goldfish eye. II. Increase in retinal cell number. J Comp Neurol 176:331-342.
62. Kaas JH, Huerta MF, Weber JT, Harting JK. 1978. Petterns of retinal terminations and laminar organisation of the lateral geniculate nucleus of primates. J Comp Neurol 182:517-554.
63. Kahn AJ. 1973. Ganglion cell formation in the chick neural retina. Brain Res 63:285-290.
64. Khalil SH, Szekely G. 1976. The development of the ipsilateral retinothalamic projections in the Xenopus toad. Acat Biol Acad Sci Hung 27: 253-260.
65. Kennard C. 1981. Factors involved in the development of ipsilateral retinothalamic projections in Xenopus laevis. J Embryol Exp Morphol 65:199-217.
66. Kennedy MC, Rubinson K. 1977. Retinal projections in larval, transforming and adult sea lamprey, Petromyzon marinus. J Comp Neurol 171: 456-480.
67. Knapp HF, Scalia F, Riss W. 1965. The optic tracts of Rana pipiens. Acta Neurol Scand 41:325-355.
68. Langdon RB, Frost DO. 1991. Transient retinal axon collaterals to visual and somatosensory thalamus in neonatal hamsters. J Comp Neurol 310:200-214.
69. Lia BL, Williams RW, Chalupa LM. 1987. Formation of retinal ganglion cell topography during prenatal development. Science 236:848-851.
70. Linden DC, Guillery RW, Cucchiaro J. 1981. The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. J Comp Neurol 203:189-211.
71. Linden R, Perry VH. 1983. Massive retinotectal projection in rats. Brain Res 272:145-149.
72. Lund RD, Bunt AH. 1976. Prenatal development of central optic pathways in albino rats. J Comp Neurol 165:247-264.
73. Marcus RC, Mason CA. 1995. The first retinal axon growth in the mouse optic chiasm: axon patterning and the cellular environment. J Neurosci 15:6389-6402.
74. McLoon SC, Lund RD. 1982. Transient retinofugal pathways in the developing chick. Exp Brain Res 45:277-284.
75. Meissirel C, Wikler KC, Chalupa LM, Rakic P. 1997. Early divergence of magnocellular and parvaocellular functional subsystems in the embryonic primate visual system. Proc Natl Acad Sci USA 94:5900-5905.
76. Mendez-Otero R, Cavalcante LA, Rocha-Miranda AE, Bernardes RF, Barradas PCR. 1985. Growth and restriction of the ipsilateral retinocollicular projection in the opossum. Brain Res Dev Brain Res 18:199-210.
77. Mey J, Thanos S. 2000. Development of the visual system of the chick. I. Cell differentiation and histogenesis. Brain Res Rev 32:343-379.
78. Meyer RL. 1978. Evidence from thymidine labelling for continuing growth of retina and tectum in juvenile goldfish. Exp Neurol 59:99-111.
79. Nyugen VS, Straznicky C. 1989. The development and the topographic organisation of the retinal ganglion cell layer in Bufo marinus. Exp Brain Res 75:345-353.
80. O'Leary DMM, Gerfen CR, Cowan WM. 1983. The development and restriction of the ipsilateral retinofugal projection in the chick. Brain Res Dev Brain Res 10:93-109.
81. O'Leary DMM, Fawcett JW, Cowan WM. 1986. Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. J Neurosci 6:3692-3705.
82. Provis JM, Billson FA, Russell P. 1983. Ganglion cell topography in human fetal retinae. Invest Ophthalmol Vis Sci 24:1316-1320.
83. Rakic P. 1977. Prenatal development of the visual system in rhesus monkey. Phil Trans R Soc London 276:245-269.
84. Rakic P. 1986. Mechanisms of ocular dominance segregation in the lateral geniculate nucleus: competitive elimination hypothesis. TINS 9:11-15.
85. Rapaport DH, Rakic P, LaVail MM. 1996. Spatio-temporal gradients of cell genesis in the primate retina. Perspect Dev Neurobiol 3:147-159.
86. Reh TA, Constantine-Paton M. 1983. Qualitative and quantitative measures of plasticity during the normal development of the Rana pipiens retinotectal projection. Exp Brain Res 30:187-200.
87. Rettig G. 1988. Development ofretinofugal neurpil areas in the brain of the alpine newt, Triturus alpestris. II. Topographic organization and formation of projections. Anat Embryol 177:257-265.
88. Rettig G, Fritzsch B, Himstedt W. 1981. Development of retinofugal neuropil areas in the brain of the alpine newt, Triturus alpestris. Anat Embryol 162:163-171.
89. Rodger J, Bartelett, CA, Beazley LD, Dunlop SA. 2000. Transient up-regulation of the rostrocaudal gradeint of ephrin-A2 in the tectum coincides with re-establishment of orderly projections during optic nerve regeneration in goldfish. Exp Neurol 166:196-200.
90. Rodger J, Bartlett CA, Harman AM, Thomas C, Beazley LD, Dunlop SA. 2001. Evidence that regenerating optic axons maintain long-term growth in the lizard Ctenophorus ornatus: growth associated protein-43 and gefiltin expression. Neuroscience 102:647-654.
91. Rodieck RW. 1979. Visual pathways. Annu Rev Neurosci 2:193-225.
92. Rubinson K. 1990. The developing visual system and metamorphosis in the lamprey. J Neurobiol 21:1123-1135.
93. Scalia F. 1970. The optic pathway of the frog: nuclear organisation and connections. In: Linas R, Aecht W, editors. Frog neurobiology. Berlin: Springer. p 386-406.
94. Sefton AJ. 1968. The innervation of the lateral geniculate nucleus and anterior colliculus in the rat. Vis Res 8:867-881
95. Sefton AJ, Dreher B. 1995. Visual system. In: Paxinos G, editor. The rat nervous system, 2nd ed. Sydney: Academic Press. p 833-897.
96. Sharma SC, Ungar F. 1980. Histogenesis of the goldfish retina. J Comp Neurol 191:373-382.
97. Shatz CJ. 1990. Competitive interactions between retinal ganglion cells during prenatal development. J Neurobiol 21:197-211.
98. Shatz CJ. 1983. The prenatal development of the cat's retinogeniculate pathway. J Neurosci 3:482-499.
99. Sherman SM. 1985. Development of retinal projections to the cat's lateral geniculate nucleus. TINS 8:350-355.
100. Snider CJ, Dehay C, Berland M, Kennedy H, Chalupa LM. 1999. Prenatal development of retinogeniculate axons in the macaque monkey during segregation of binocular inputs. J Neurosci 19:220-228.
101. Sretavan DW, Shatz CJ. 1986. Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat's lateral geniculate nucleus. J Neurosci 6:226-251.
102. Sretavan DW, Shatz CJ, Stryker MP. 1988. Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336:468-471.
103. Stirling RV, Merrill G. 1987. Functional morphology of frog retinal ganglion cells and their central projections: the dimming detectors. J Comp Neurol 258:477-495.
104. Stirling RV, Harman AM, Dunlop SA, Beazley LD. 1998. Optic nerve regeneration in a turtle. Proc Aust Neurosci Soc 9:38.
105. Stirling RV, Dunlop SA, Beazley LD. 1999. Electrophysiological evidence for transient topographic organization of retinotectal projections during optic nerve regeneration in the lizard, Ctenophorus ornatus. Vis Neurosci 16:681-693.
106. Straznicky C, Chehade M. 1987. The formation of the area centralis of the retinal ganglion cell layer in the chick. Development 100:411-420.
107. Straznicky K, Gaze RM. 1971. The growth of the retina in Xenopus laevis: an autoradiographic study. J Embryol Exp Morphol 26:67-79.
108. Symonds ACE, Rodger J, Tan MML, Dunlop SA, Beazley LD, Harvey AR. 2001. Reinnervation of the superior colliculus delays down-regulation of ephrin-A2 in neonatal rat. Exp Neurol 170:364-370.
109. Tennant M, Moore SR, Beazley LD. 1993. Survival of retinal ganglion cells that give rise to a retino-retinal projection during optic nerve regeneration in the frog. Vis Neurosci 10:684-612.
110. Thanos S. 1999. Genesis, neurotrophin responsiveness, and apoptosis of a pronounced direct connection between the two eyes of the chick embryo: a natural error or a meaningful developmental event? J Neurosci 19:3900-3917.
111. Thanos SS, Bonhoeffer F. 1984. Development of the transient ipsilateral retinotectal projection in the chick embryo: a numerical fluorescence-microscope analysis. J Comp Neurol 224:407-414.
112. Toth P, Straznicky C. 1989. Retino-retinal projections in three anuran species. Neurosci Lett 104:43-47.
113. Walsh C, Polley EH. 1985. The topography of ganglion cell production in the cat's retina. J Neurosci 5:741-750.
114. Warton SS, McCart R. 1989. Synaptogenesis in the stratum griseum superficiale of the rat superior colliculus. Synapse 3:136-148.
115. Williams RW, Chalupa LM. 1982. Prenatal development of retinocollicular projections in the cat: an anterograde tracer transport study. J Neruosci 2:604-622.
116. Williams RW, McLoon SC. 1991. Elimination of the transient ipsilateral retinotectal projection is not solely achieved by cell death in the developing chick. J Neurosci 11:446-453.
117. Wye-Dvorak J. 1984. Postnatal development of primary visual projections in the tammar wallaby (Macropus eugenii). J Comp Neurol 28:491-508.
118. Young RW. 1985. Cell proliferation during postnatal development of the retina in the mouse. Exp Brain Res 21:229-239.