Differential distribution of AMPA receptors and glutamate during pre- and postnatal development in the visual cortex of ferrets

Journal of Comparative Neurology

Volumn 375, Issue 1, 1996, Pages 1-17

  Herrmann, Kathrin ^a  

^a NIH Animal Center   (United States)

Author keywords

cortical development; excitatory amino acid; GluR1; GluR2 3; immunohistochemistry

Indexed keywords

AMPA RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRAIN BIOPSY; BRAIN DEVELOPMENT; FERRET; GROWTH REGULATION; IMMUNOHISTOCHEMISTRY; NERVE CELL DIFFERENTIATION; NEUROTRANSMISSION; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; RECEPTOR DENSITY; TISSUE DISTRIBUTION; VISUAL CORTEX;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL MOVEMENT; EMBRYONIC AND FETAL DEVELOPMENT; FERRETS; GESTATIONAL AGE; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; RECEPTORS, AMPA; VISUAL CORTEX;

EID: 0029960501     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19961104)375:1<1::AID-CNE1>3.0.CO;2-7     Document Type: Article

References (97)

1. Allendoerfer, K.L., and C.J. Shatz (1994) The subplate, a transient neocortical structure - its role in the development of connections between thalamus and cortex. Annu. Rev. Neurosci. 17:185-218.
2. Allendoerfer, K.L., R.J. Cabelli, E. Escandon, D.R. Kaplan, K. Nicoliks, and C.J. Shatz (1994) Regulation of neurotrophin receptors during the maturation of the mammalian visual system. J. Neurosci. 14:1795-1811.
3. Aoki, C., C. Venkatesan, C.G. Go, J.A. Mong, and T.M. Dawson (1994) Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats. J. Neurosci. 14:5202-5222.
4. Bahn, S., B. Volk, and W. Widen (1994) Kainate receptor gene expression in the developing rat brain. J. Neurosci. 14:5525-5547.
5. Bettler, B., J. Boulter, I. Hermans-Borgemeyer, A. O'Shea-Greenfield, E.S. Deneris, C. Moll, U. Borgemeyer, U. Hollmann, and S. Heinemann (1990) Cloning of a novel glutamate receptor subunit, GluR5: Expression in the nervous system during development. Neuron 5:583-595.
6. Bode-Greuel, K.M., and W. Singer (1989) The development of N-methyl-D-aspartate receptors in cat visual cortex. Dev. Brain Res. 46:197-204.
7. Boulter, J., M. Hollmann, A. O'Shea-Greenfield, M. Hartley, E.S. Deneris, C. Maron, and S. Heinemann (1990) Molecular cloning and functional expression of glutamate receptor subunit genes. Science 249:1033-1037.
8. Brewer, G.L., and C.W. Cotman (1989) NMDA receptor regulation of neuronal morphology in cultured hippocampal neurons. Neurosci. Lett. 99:268-273.
9. Carder, R.K., and S.H.C. Hendry (1994) Neuronal characterization, compartmental distribution, and activity-dependent regulation of glutamate immunoreactivity in adult monkey striate cortex. J. Neurosci. 14:242-262.
10. Carmignoto, G., and S. Vicini (1992) Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258:1007-1011.
11. Catania, M.V., G.B. Landwehrmeyer, C.M. Testa, D.G. Standaert, J.B. Penney, and A.B. Young (1994) Metabotropic glutamate receptors are differentially regulated during development. Neuroscience 61:481-495.
12. Cavanagh, M.E., and J.G. Parnavelas (1988) Development of somatostatin immunoreactive neurons in the rat occipital cortex: A combined immunocytochemical-autordiographic study. J. Comp. Neurol. 268:1-12.
13. Chapman, B., and M.P. Stryker (1993) Development of orientation selectivity in ferret visual cortex and effects of deprivation. J. Neurosci. 13:5251-5262.
14. Choi, D. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634.
15. Chun, J.J.M., and C.J. Shatz (1988) Redistribution of synaptic vesicle antigens is correlated with the disappearance of a transient synaptic zone in the developing cerebral cortex. Neuron 1:297-310.
16. A receptor. Neuroscience 40:375-397.
17. Collingridge, G.L., and W. Singer (1990) Excitatory amino acid receptors and synaptic plasticity. TIPS 11:290-296.
18. Conti, F., A. Rustioni, P. Petrusz, and A.C. Towle (1987) Glutamate-positive neurons in the somatic sensory cortex of rats and monkeys. J. Neurosci. 7:1887-1901.
19. Conti, F., M. Fabri, and T. Manzoni (1988) Glutamate-positive corticocortical neurons in the somatic sensory areas I and II of cats. J. Neurosci. 8:2948-2960.
20. Dalva, M.B., and L.C. Katz (1994) Rearrangements of synaptic connections in visual cortex revealed by laser photostimulation. Science 265:255-258.
21. D'Amato, R.J., M.E. Blue, B.L. Largent, D.R. Lynch, D.J. Ledbetter, M.E. Molliver, and S.H. Snyder (1987) Ontogeny of the serotonergic projection to rat neocortex: Transient expression of a dense innervation to primary sensory areas. Proc. Natl. Acad. Sci. USA 84:4322-4326.
22. DeFelipe, J., F. Conti, S.L. Van Eyck, and T. Manzoni (1988) Demonstration of glutamate-positive axon terminals forming asymmetric synapses in cat neocortex. Brain Res. 455:162-165.
23. Del Rio, J.A., E. Soriano, and I. Ferrer (1992) Development of GABA-immunoreactivity in the neocortex of the mouse. J. Comp. Neurol. 326:501-526.
24. Dori, I., M. Petrou, and J.G. Parnavelas (1989) Excitatory transmitter amino acid-containing neurons in the rat visual cortex: A light and electron microscopic immunocytochemical study. J. Comp. Neurol. 290:169-184.
25. Dori, I., A. Dinopoulos, M.E. Cavanah, and J.G. Parnavelas (1992) Proportion of glutamate- and aspartate-immunoreactive neurons in the efferent pathways of the rat visual cortex varies according to the target. J. Comp. Neurol. 319:191-204.
26. Fox, K., H. Sato, and N. Daw (1989) The location and function of NMDA receptors in cat and kitten visual cortex. J. Neurosci. 9:2443-2454.
27. Fox, K., N. Daw, H. Sato, and D. Czepita (1992) The effect of visual experience on development of NMDA receptor synaptic transmission in kitten visual cortex. J. Neurosci. 12:2672-2684.
28. Friauf, E., and C.J. Shatz (1991) Changing patterns of synaptic input to subplate and cortical plate during development of visual cortex. J. Neurophysiol. 66:2059-2071.
29. Gilbert, C. (1983) Microcircuitry of the visual cortex. Annu. Rev. Neurosci. 6:217-247.
30. Giuffrida, R., and A. Rustioni (1989) Glutamate and aspartate immunoreactivity in cortico-cortical neurons of the sensorimotor cortex of rats. Exp. Brain Res. 74:41-46.
31. Gonzalez, B.J., P. Leroux, P.C. Bodenant, and H. Vaudry (1991) Ontogeny of somatostatin receptors in the rat somatosensory cortex. J. Comp. Neurol. 305:177-188.
32. Götz, M., and J. Bolz (1994) Differentiation of transmitter phenotypes in rat cerebral cortex. Eur. J. Neurosci. 6:18-32.
33. Hepler, J.R., C.S. Toomim, K.D. McCarthy, F. Conti, G. Battaglia, A. Rustioni, and P. Petrusz (1988) Characterization of antisera to glutamate and aspartate. J. Histochem. Cytochem. 36:13-22.
34. Herrmann, K., and R.O.L. Wong (1995) Optical recording of calcium responses to ATP in the ferret cortical ventricular zone. Soc. Neurosci. Abstr. 21(2):1285.
35. Herrmann, K., A. Antonini, and C.J. Shatz (1994) Ultrastructural evidence for synaptic interactions between thalamocortical axons and subplate neurons. Eur. J. Neurosci. 6:1729-1742.
36. Hollmann, M., and S. Heinemann (1994) Cloned glutamate receptors. Annu. Rev. Neurosci. 17:31-108.
37. Hollmann, M., A. O'Shea-Greenfield, S.W. Rogers, and S. Heinemann (1989) Cloning by functional expression of a member of the glutamate receptor family. Nature 342:643-648.
38. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252:851-853.
39. Iino, M., S. Ozawa, and K. Tsuzuki (1990) Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones. J. Physiol. 424:151-165.
40. Insel, T., L.P. Miller, and R.E. Gelhard (1990) The ontogeny of excitatory amino acid receptors in rat forebrain-I. N-methyl-D-aspartate and quisqualate receptors. Neuroscience 35:31-43.
41. Jackson, C.A., J.D. Peduzzi, and T.L. Hickey (1989) Visual cortex development in the ferret. I. Genesis and migration of visual cortical neurons. J. Neurosci. 9:1242-1253.
42. Jahr, C.E., and C.F. Stevens (1993) Calcium permeability of the N-methyl-D-aspartate receptor channel in hippocampal neurons in culture. Proc. Natl. Acad. Sci. USA 90:11573-11577.
43. Johnson, R.R., and A. Burkhalter (1992) Evidence for excitatory amino acid neurotransmitters in the geniculocortical pathway and local projections within rat primary visual cortex. Exp. Brain Res. 89:20-30.
44. Jones, K.A., and R.W. Baughman (1991) Both NMDA and non-NMDA subtypes of glutamate receptors are concentrated at synapses on cerebral cortical neurons in culture. Neuron 7:593-603.
45. Keinänen, K., W. Wisden, B. Sommer, P. Werner, A. Herb, T.A. Verdoorn, B. Sakmann, and P.H. Seeburg (1990) A family of AMPA-selective glutamate receptors. Science 249:556-560.
46. Kharazia, V.N., and R.J. Weinberg (1993) Glutamate in terminals of thalamocortical fibers in rat somatic sensory cortex. Neurosci. Lett. 157:162-166.
47. Komuro, H., and P. Rakic (1993) Modulation of neuronal migration by NMDA receptors. Science 260:95-97.
48. König, N., G. Roch, and R. Marty (1975) The onset of synaptogenesis in rat temporal cortex. Anat. Embryol. 148:73-87.
49. Lauder, J.M. (1993) Neurotransmitters as growth regulatory signals - role of receptors and 2nd messengers. Trends Neurosci. 16:233-240.
50. Liu, Y., W. Jia, Q. Gu, and M. Cynader (1994) Involvement of muscarinic acetylcholine receptors in regulation of kitten visual cortical plasticity. Dev. Brain Res. 70:63-70.
51. López, T., A.M. López-Colomé, and A. Ortega (1994) AMPA/KA receptor expression in radial glia. Neuroreport 5:504-506.
52. LoTurco, J.J., M.G. Blanton, and A.R. Kriegstein (1991) Initial expression and endogenous activation of NMDA channels in early neocortical development. J. Neurosci. 11:792-799.
53. LoTurco, J.J., D.F. Owens, M.J.S. Heath, M.B.E. Davis, and A.R. Kriegstein (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1286-1298.
54. Malenka, R.C., and R.A. Nicoll (1993) NMDA-receptor-dependent synaptic plasticity - multiple forms and mechanisms. Trends Neurosci. 16:521-527.
55. Martin, L.J., C.D. Blackstone, A.I. Levey, R.L. Huganir, and D.L. Price (1993) AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53:327-358.
56. Masu, M., Y. Tanabe, K. Tsuchida, R. Shigemoto, and S. Nakanishi (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349:760-765.
57. Mattson, M.P., P. Dou, and S.B. Kater (1988a) Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. J. Neurosci. 8:2087-2100.
58. Mattson, M.P., R.E. Lee, M.E. Adams, P.B. Guthrie, and S.B. Kater (1988b) Interactions between entorhinal axons and target hippocampal neurons: a role for glutamate in the development of hippocampal circuitry. Neuron 1:865-876.
59. McAllister, A.K., D.C. Lo, and L.C. Katz (1995) Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15:791-803.
60. McConnell, S.K. (1988) Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation. J. Neurosci. 8:945-974.
61. McConnell, S.K., and C.E. Kaznowski (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254:282-285.
62. McCormick, D. (1992) Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog. Neurobiol. 39:337-388.
63. Molliver, M.E., I. Kostovic, and H. Van der Loos (1973) The development of synapses in the cerebral cortex of the human fetus. Brain Res. 50:403-407.
64. Monaghan, D.T., R.J. Bridges, and C.W. Cotman (1989) The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 29:365-402.
65. Montero, V.M. (1990) Quantitative immunogold analysis reveals high glutamate levels in synaptic terminals of retino-geniculate, cortico-geniculate, and geniculocortical axons in the cat. Vis. Neurosci. 4:437-443.
66. Monyer, H., R. Sprengel, F. Schoepfer, A. Herb, M. Higuchi, H. Lomeli, N. Burnashev, B. Sakmann, and P.H. Seeburg (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221.
67. Moriyoshi, K., M. Masu, T. Ishii, R. Shigemoto, N. Mizuno, and S. Nakanishi (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37.
68. Nakanishi, N., N.A. Shneider, and R. Axel (1990) A family of glutamate receptor genes: Evidence for the formation of heteromultimeric receptors with distinct channel properties. Neuron 5:569-581.
69. Nakanishi, S. (1992) Molecular diversity of glutamate receptors and implications for brain function. Science 258:597-603.
70. Naus, C.C.G., F.D. Miller, J.H. Morrison, and F.E. Bloom (1988) Immunohistochemical and in situ hybridization analysis of the development of the rat somatostatin-containing neocortical system. J. Comp. Neurol. 269: 448-463.
71. Nelson, D.A., and L.C. Katz (1995) Emergence of functional circuits in ferret visual cortex visualized by optical imaging. Neuron 15:23-34.
72. Nicoll, R.A., R.C. Malenka, and J.A. Kauer (1990) Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol. Rev. 70:513-565.
73. O'Rourke, N.A., M.E. Daily, S.J. Smith, and S.K. McConnell (1992) Diverse migratory pathways in the developing cerebral cortex. Science 258:299-302.
74. Ottersen, O.P., and J. Storm-Mathisen (1984) Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J. Comp. Neurol. 229:374-392.
75. Papadopoulos, G.C., M.E. Cavanagh, J. Antonopoulos, H. Michaloudi, and J.G. Parnavelas (1993) Postnatal development of somatostatin-containing neurons in the visual cortex of normal and dark-reared rats. Exp. Brain Res. 92:473-478.
76. Parnavelas, J.G., and M.E. Cavanagh (1988) Transient expression of neurotransmitters in the developing neocortex. TINS 11:92-93.
77. Pearce, I.A., M.A. Cambray-Deakin, and R.D. Burgoyne (1987) Glutamate acting on NMDA receptors stimulates neuron outgrowth from cerebellar granule cells. FEBS Lett. 223:143-147.
78. Pellegrini-Giampietro, D.E., M.V. Bennett, and R.S. Zukin (1991) Differential expression of three glutamate receptor genes in developing rat brain: An in situ hybridization study. Proc. Natl. Acad. Sci. USA 88:4157-4161.
79. Perkel, D.J., J.J. Petrozzino, R.A. Nicoll, and J.A. Connor (1993) The role of Ca2+ entry via synaptically activated NMDA receptors in the induction of long-term potentiation. Neuron 11:817-823.
80. Petralia, R.S., and R.J. Wenthold (1992) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318:329-354.
81. Pow, D.V., D.K. Crook, and R.O.L. Wong (1994) Early appearance and expression of putative amino acid neurotransmitters and related molecules in the developing rabbit retina: An immunohistochemical study. Vis. Neurosci. 11:1115-1134.
82. Roßner, S., A. Kumar, W. Hues, V. Witzemann, and R. Schliebs (1993) Differential laminar expression of AMPA receptor genes in the developing rat visual cortex using insitu hybridization histochemistry - effect of visual deprivation. Int. J. Dev. Neurosci. 11:411-424.
83. Rogers, S.W., T.E. Hughes, M. Hollmann, G.P. Gasic, E.S. Deneris, and S. Heinemann (1991) The characterization and localization of the glutamate receptor subunit GluR1 in the rat brain. J. Neurosci. 11:2713-2724.
84. Ruthazer, E.S., G.E. Baker, and M.P. Stryker (1995) Development and pattern of ocular dominance columns in ferret visual cortex. Soc. Neurosci. Abstr. 21(3):1795.
85. Sato, K., H. Kiyama, and M. Tohyama (1993) The differential expression patterns of messenger RNAs encoding non-N-methyl-D-aspartate glutamate receptor subunits (GluR1-4) in the rat brain. Neuroscience 52:515-539.
86. Schwartz, J.P. (1991) Neurotransmitters as neurotrophic factors: A new set of functions. Int. Rev. Neurobiol. 34:1-23.
87. Smith, A.L., and I.D. Thompson (1994) Distinct laminar differences in the distribution of excitatory amino acid receptors in adult ferret primary visual cortex. Neuroscience 61:467-479.
88. Sommer, B., K. Keinänen, T.A. Verdoorn, W. Wisden, N. Burnashev, A. Herb, M. Kohler, T. Takagi, B. Sakmann, and P.H. Seeburg (1990) Flip and flop: A cell-specific functional switch in glutamate-operated channels of the CNS. Science 249:1580-1585.
89. Sucher, N.J., N. Brose, D.L. Deitcher, M. Awobuuyi, G.P. Gasic, H. Bading, C.L. Cepko, M.E. Greenberg, R. Jahn, and S.F. Heinemann (1993) Expression of endogenous NMDAR1 transcripts without receptor protein suggests post-transcriptional control in PC12 cells. J. Biol. Chem. 268:22299-22304.
90. Tanabe, Y., M. Masu, T. Ishii, R. Shigemoto, and N. Nakanishi (1992) A family of metabotropic glutamate receptors. Neuron 8:169-179.
91. Tsumoto, T., K. Hagihara, H. Sato, and Y. Hata (1987) NMDA receptors in the visual cortex of young kittens are more effective than those of the adult. Nature 327:513-514.
92. Van Eden, C., L. Mrjljak, P. Voorn, and H. Uylings (1989) Prenatal development of GABAergic neurons in the neocortex of the rat. J. Comp. Neurol. 289:213-227.
93. Vickers, J.C., G.W. Huntley, A.M. Edwards, T. Moran, S.W. Rogers, S.F. Heinemann, and J.H. Morrison (1993) Quantitative localization of AMPA/kainate and kainate glutamate receptor subunit immunoreactivity in neurochemically identified subpopulations of neurons in the prefrontal cortex of the macaque monkey. J. Neurosci. 13:2982-2992.
94. Voigt, T., and A.D. DeLima (1991) Serotoninergic innervation of the ferret cerebral cortex. II. Postnatal development. J. Comp. Neurol. 314:415-428.
95. Voigt, T., A.D. DeLima, and M. Beckmann (1993) Synaptophysin immunohistochemistry reveals inside-out pattern of early synaptogenesis in ferret cerebral cortex. J. Comp. Neurol. 330:48-64.
96. Werner, P., M. Voigt, W. Keinänen, and P. Seeburg (1991) Cloning of a putative high affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature 351:742-744.
97. 2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6:333-344.