Changes of immunocytochemical localization of vesicular glutamate transporters in the rat visual system after the retinofugal denervation

Journal of Comparative Neurology

Volumn 465, Issue 2, 2003, Pages 234-249

  Fujiyama, Fumino ^a   Hioki, Hiroyuki ^a   Tomioka, Ryohei ^a   Taki, Kousuke ^a   Tamamaki, Nobuaki ^a   Nomura, Sakashi ^a   Okamoto, Keiko ^a   Kaneko, Takeshi ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Enucleation; Glutamatergic neurons; Retinal ganglion cell; Retinofugal neuron; VGluT1; VGluT2

Indexed keywords

GLUTAMATE TRANSPORTER; GLUTAMIC ACID; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; WHEAT GERM AGGLUTININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENERVATION; ENUCLEATION; IMMUNOCYTOCHEMISTRY; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; LATERAL GENICULATE BODY; NERVE ENDING; NERVE FIBER TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIVARY NUCLEUS; PERIKARYON; PRETECTUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RETINA; RETINOFUGAL DENERVATION; SUPERIOR COLLICULUS; SUPRACHIASMATIC NUCLEUS; SYNAPSE VESICLE; VISUAL SYSTEM;

ANIMALS; CARRIER PROTEINS; DENERVATION; EYE ENUCLEATION; FUNCTIONAL LATERALITY; GENICULATE BODIES; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, IMMUNOELECTRON; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RETINA; RETINAL GANGLION CELLS; RNA, MESSENGER; SUPERIOR COLLICULUS; SYNAPSES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VESICULAR TRANSPORT PROTEINS; VISUAL PATHWAYS;

EID: 0042915938     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10848     Document Type: Article

References (84)

1. Ashwell K. 1986. An abnormal retinal projection to the lateral posterior nucleus in microencephalic rats. Neurosci Lett 72:7-13.
2. Bai L, Xu H, Collins J, Ghishan FK. 2001. Molecular and functional analysis of a novel neuronal vesicular glutamic transporter. J Biol Chem 276:36764-36769.
3. Bellocchio EE, Hu H, Pohorille A, Chan J, Pickel VM, Edwards R. 1988. The localization of the brain-specific inorganic phosphate transporter suggests a specific presynaptic role in glutamatergic transmission. J Neurosci 18:8648-8659.
4. Bellocchio EE, Reimer RJ, Fremeau RT, Edwards RH. 2000. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289:957-960.
5. Blanks, RH, Giolli RA, Pham SV. 1982. Projections of the medial terminal nucleus of the accessory optic system upon pretectal nuclei in the pigmented rat. Exp Brain Res 48:228-237.
6. Bolz J, Hubener M, Keher I, Novak N. 1991. Structural organization and development of identified projection neurons in primary visual cortex. In: Bagnoli P, Hodos and W, editors. The changing visual system. New York: Plenum Press. p 233-246.
7. Crooks J, Kolb H. 1992. Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. J Comp Neurol 315:287-302.
8. Davanger S, Otterson OP, Storm-Mathisen J. 1991. Glutamate, GABA, and glycine in the human retina: an immunocytochemical investigation. J Comp Neurol 311:483-494.
9. Dreher B, Sefton A, Ni SYK. 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.
10. Ehinger B, Otterson OP, Storm-Mathisen L, Dowling JE. 1988. Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proc Natl Acad Sci U S A 85:8321-8325.
11. Fosse VM, Opstad PK. 1986. Biochemical plasticity in the superior colliculus of adult rats after chronic visual cortex ablation. Brain Res 372:189-192.
12. Fremeau RT, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ. 2001. The expression of vesicular glutamate transporters defines two classes of excitatory synapses. Neuron 31:247-260.
13. Fujiyama F, Furuta T, Kaneko T. 2001. Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex. J Comp Neurol 435:379-387.
14. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy S. 2002. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22:5442-5451.
15. Graybiel AM. 1974. Visuo-cerebellar and cerebello-visual connections involving the ventral lateral geniculate nucleus. Exp Brain Res 20:303-306.
16. Hallman LC, Schofield BR, Lin C-S. 1988. Dendritic morphology and axon collaterals of corticotectal, corticopontine and callosal neurons in layer V of primary visual cortex of the hooded rat. J Comp Neurol 272:149-160.
17. Harting JK, Van Lieshout DP, Hashikawa T, Weber JT. 1991. The parabigeminogeniculate projection: connectional studies in eight mammals. J Comp Neurol 305:559-581.
18. Hashimoto K, Kano M. 1998. Presynaptic origin of paired pulse depression at climbing fiber-Purkinje cell synapses in the rat cerebellum. J Physiol 506:391-405.
19. Hayhow WR, Sefton A, Webb C. 1962. Primary optic centers in the rat relation to the terminal distribution of the crossed and uncrossed optic nerve fibers. J Comp Neurol 115:187-216.
20. Herzog E, Bellenchi GC, Gras C, Bernard V, Ravassard P, Bedet C, Gasnier B, Giros B, Mestikawy SE. 2001. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21:RC181.
21. Hickey TL, Spear PD. 1976. Retinogeniculate projections in hooded and albino rats: an autoradiographic study. Exp Brain Res 24:523-529.
22. Hioki H, Fujiyama F, Taki K, Tomioka R, Furuta T, Tamamaki N, Kaneko T. 2003. Differential distribution of vesicular glutamate transporters in the rat cerebellar cortex. Neuroscience 117:1-6.
23. +-dependent inorganic phosphate cotransporter (VGluT2) in the rat forebrain. Mol Brain Res 83:34-43.
24. Hollander H, Schonitzer K. 1983. Corticotectal terminals in the superior colliculus of the rabbit: a light and electron microscopic analysis using horseradish peroxidase (HRP)-tetra-methyl benzidine (TMB). J Comp Neurol 219:81-87.
25. Huberner M, Bolz J. 1988. Morphology of identified projection neurons in layer V of rat visual cortex. Neurosci Lett 94:76-81.
26. Jeffery G. 1984. Transneuronal effects of early eye removal on geniculocortical projection cells. Dev Brain Res 13:257-263.
27. Kageyama GH, Meyer RL. 1989. Glutamate-immunoreactivity in the retina and optic tectum of goldfish. Brain Res 503:118-127.
28. Kaneko T, Fujiyama F. 2002. Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci Res 42:243-250.
29. Kaneko T, Itoh K, Shigemoto R, Mizuno N. 1989. Glutaminase-like immunoreactivity in the lower brainstem and cerebellum of the adult rat. Neuroscience 32:79-98.
30. Kaneko T, Fujiyama F, Hioki H. 2002. Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J Comp Neurol 444:39-62.
31. Karlsen RL, Fonnum F. 1978. Evidence for glutamate as a neurotransmitter in the corticofugal fibers to the dorsal lateral geniculate body and the superior colliculus in rats. Brain Res 151:457-467.
32. Kemp JA, Sillito AM. 1982. The nature of the excitatory transmitter mediating X and Y cell inputs to the cat dorsal lateral geniculate nucleus. J Physiol (Lond) 323:377-391.
33. Konnerth A, Llano I, Armstrong CM. 1990. Synaptic currents in cerebellar Purkinje cells. Proc Natl Acad Sci U S A 87:2662-2665.
34. Kwon YH, Esguerra M, Sur M. 1991. NMDA and non-NMDA receptors mediate visual responses of neurons in the cat's lateral geniculate nucleus. J Neurophysiol 66:414-428.
35. Legg CR. 1979. An autoradiographic study of the efferent projections of the ventral lateral geniculate nucleus of the hooded rat. Brain Res 170:349-352.
36. Leong SK. 1980. Plasticity and interaction after ablations of visual or somatosensory motor cortex or retina in neonatal rats. J Neurol Sci 45:87-102.
37. Lieberman AR, Webster KE. 1974. Aspects of the synaptic organization of intrinsic neurons on the dorsal lateral geniculate nucleus: an ultrastructural study of the normal and of the experimentally deafferented nucleus in the rat. J Neurocytol 3:677-710.
38. Lindstrom S, Wrobel A. 1990. Frequency dependent corticofugal excitation of principal cells in the cat's dorsal lateral geniculate nucleus. Exp Brain Res 79:313-318.
39. Lund RD, Cunningham TJ. 1972. Aspects of synaptic and laminar organization of the mammalian lateral geniculate body. Invest Ophthalmol 11:291-302.
40. Mackay-Sim A, Sefton AJ, Martin PR. 1983. Subcortical projections to lateral geniculate and thalamic reticular nuclei in the hooded rat. J Comp Neurol 213:24-35.
41. Marc RE, Massey SC, Kalloniatis M, Basinger SF. 1989. Immunochemical evidence that the fast neurotransmitter of rods, cones, bipolar and ganglion cells is glutamic acid. Invest Opthalmol 30(Suppl):320.
42. Marc RE, Liu WS, Kalloniatis M, Raiguel SF, Van Hasendonck E. 1990. Patterns of glutamate immunoreactivity in the goldfish retina. J Neurosci 10:4006-4034.
43. Margolis RK, Heller A, Moore RY. 1968. Effects of changes in cellular composition following neuronal degeneration on amino acid in brain. Brain Res 11:19-31.
44. Massey SC. 1990. Cell types using glutamate as a neurotransmitter in the vertebrate retina. In: Osborne NN, Chader GJ, editors. Progress in retinal research. Oxford, UK: Pergamon. p 399-425.
45. Moga MM, Moore RY. 1997. Organization of neural inputs to the suprachiasmatic nucleus in the rat. J Comp Neurol 389:508-534.
46. Moody CI, Sillito AM. 1988. The role of the N-methyl-D-asparate (NMDA) receptor in the transmission of visual information in the feline dorsal lateral geniculate nucleus (dLGN). J Physiol (Lond) 396:62P.
47. Moore RY, Weis R, Moga MM. 2000. Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J Comp Neurol 420:398-418.
48. Ni B, Rosteck PR Jr, Nadi NS, Paul SM. 1994. Cloning and expression of a cDNA encoding a brain-specific Na +-dependent inorganic phosphate cotransporter. Proc Natl Acad Sci U S A 91:5607-5611.
49. Ni B, Wu X, Yan G-M, Wang J, Paul SM. 1995. Regional expression and cellular localization of the Na+-dependent inorganic phosphate cotransporter of rat brain. J Neurosci 15:5789-5799.
50. Ogawa-Meguro R, Itoh K, Mizuno N. 1992. Substance P-, vasoactive intestinal polypeptide-, and cholecystokinin-like immunoreactive fiber projections from the superior colliculus to the dorsal lateral geniculate nucleus in the rat. Exp Brain Res 89:59-66.
51. Ohara PT, Lieberman AR, Hunt SP, Wu U-C. 1983. Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat: immunohistochemical studies by light microscopy. Neuroscience 8:189-211.
52. Ohtsuki H, Tokunaga A, Ono K, Hasebe S, Tadokoro Y. 1992. Distribution of efferent neurons projecting to the tectum and cerebellum in the rat prepositus hypoglossi nucleus. Invest Ophthalmol Vis Sci 33:2567-2574.
53. Olavaria J, Van Sluyters R. 1982. The projection from striate and extrastriate cortical area to the superior colliculus in the rat. Brain Res 242:332-336.
54. Ortega F, Donate-Oliver F, Grandes P. 1993. Retinal afferents on Golgi-identified vertical neurons in the superior colliculus of the rabbit. A Golgi-EM, degenerative and autoradiographic study. Histol Histopathol 8:105-111.
55. Perkel DJ, Hestrin S, Sah P, Nicoll RA. 1990. Excitatory synaptic currents in Purkinje cells. Proc R Soc Lond B 241:116-121.
56. Perry VH, Cowey A. 1979a. The effects of unilateral cortical and tectal lesions on retinal ganglion cells in rats. Exp Brain Res 35:85-95.
57. Perry VH, Cowey A. 1979b. Changes in the retino-fugal pathways following cortical and tectal lesions in neonatal and adult rats. Exp Brain Res 35:97-108.
58. Polyak S. 1957. The vertebrate visual system. Chicago: University of Chicago Press.
59. Ribak CE, Peters A. 1975. An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Res 92:341-368.
60. Rodiek RW, Watabe M. 1993. Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus. J Comp Neurol 338:289-303.
61. Sakurai T, Okada Y. 1992. Selective reduction of glutamate in the rat superior colliculus and dorsal lateral geniculate nucleus after contralateral enucleation. Brain Res 573:197-203.
62. Sakurai T, Miyamoto T, Okada Y. 1990. Reduction of glutamate content in rat superior colliculus after retino-tectal denervation. Neurosci Lett 109:299-303.
63. Salt TE. 1988. Electrophysiological studies of excitatory amino acid neurotransmitters in the ventrobasal thalamus. In: Macchi G, Bentivoglio M, Spreafico R, editors. Cellular thalamic mechanisms. Amsterdam: Elsevier. p 297-310.
64. Salt TE, Eaton SA. 1996. Functions of ionotropic and metabotropic glutamic receptors in sensory transmission in the mammalian thalamus. Prog Neurobiol 48:55-72.
65. Scalia F. 1972. The termination of retinal axons in the pretectal region of mammals. J Comp Neurol 145:223-258.
66. Scharfman HE, Lu S-M, Guido W, Adams PR, Sherman SM. 1990. N-methyl-D-aspartate (NMDA) receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. Proc Natl Acad Sci U S A 87:4548-4552.
67. Schofield BR, Hallman LE, Lin C-S. 1987. Morphology of corticotectal cells in the primary visual cortex of hooded rats. J Comp Neurol 261:85-97.
68. Sefton AJ. 1969. The electrical activity of the anterior colliculus in the rat. Vision Res 9:207-222.
69. Sefton AJ, Mackay-Sim A, Baur LA, Cottee LJ. 1981. Cortical projections to visual centers in the rat: an HRP study. Brain Res 215:1-13.
70. Stornetta RL, Sevigny CP, Guyenet PG. 2002. Vesicular glutamate transporter DNPI/VGluT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. J Comp Neurol 444:191-206.
71. Swanson LW, Hartman BK. 1975. The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J Comp Neurol 163:467-505.
72. Takamori S, Rhee JS, Rosenmund C, Jahn R. 2000. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-194.
73. Takamori S, Rhee JS, Rosenmund C, Jahn R. 2001. Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGluT2). J Neurosci 21:U7-U12.
74. Takatsuna Y, Chiba T, Adachi-Usami E, Kaneko T. 1994. Distribution of phosphate-activated glutaminase-like immunoreactivity in the retina of rodents. Curr Eye Res 13:629-637.
75. Taylor AM, Jeffery G, Lieberman AR. 1986. Subcortical afferent and efferent connections of the superior colliculus in the rat and comparisons between albino and pigmented strains. Exp Brain Res 62:131-142.
76. Thong IG, Dreher B. 1986. The development of the corticotectal pathway in the albino rat. Dev Brain Res 25:227-238.
77. Thong IG, Dreher B. 1987. The development of the corticotectal pathway in the albino rat: transient projections from the visual and motor cortices. Neurosci Lett 80:275-282.
78. Turner JP, Salt TE. 1998. Characterization of sensory and corticothalamic excitatory inputs to rat thalamocortical neurones in vitro. J Physiol (Lond) 510:829-843.
79. Van Haesendonck E, Missotten L. 1990. Glutamate-like immunoreactivity in the retina of a marine telolist, the dragonet. Neurosci Lett 111:281-286.
80. Varoqui H, Schafer MK-H, Zhu H, Weihe E, Erickson D. 2002. Identification of the differentiation-associated Na/Pi transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22:142-155.
81. Villar MJ, Vitale ML, Hokfelt T, Verhofstad AA. 1988. Dorsal raphe serotoninergic branching neurons projecting both to the lateral geniculate body and superior colliculus: a combined retrograde tracing-immunohistochemical study in the rat. J Comp Neurol 277:126-140.
82. Von Krosigk M, Monckton IE, Reiner PB, McCormick DA. 1999. Dynamic properties of corticothalamic excitatory postsynaptic potentials and thalamic reticular inhibitory postsynaptic potentials in thalamocortical neurons of the guinea-pig dorsal lateral geniculate nucleus. Neuroscience 91:7-20.
83. Waterhouse BD, Border B, Wahl L, Mihailoff GA. 1993. Topographic organization of rat locus coeruleus and dorsal raphe nuclei: distribution of cells projecting to visual system structures. J Comp Neurol 336:345-361.
84. Wree A, Zilles K. 1983. Ipsilateral projections to the terminal nuclei of the accessory optic system in the albino rat. Neurosci Lett 43:19-24.