Laminar and cellular distribution of AMPA, kainate, and NMDA receptor subunits in monkey sensory-motor cortex

Journal of Comparative Neurology

Volumn 407, Issue 4, 1999, Pages 472-490

  Munoz A ^a,b   Woods, T M ^a,c   Jones, E G ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSIDAD EUROPEA DE MADRID   (Spain)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell specific expression; GABA cells; Glutamate receptors; Immunocytochemistry; In situ hybridization; Pyramidal cells

Indexed keywords

4 AMINOBUTYRIC ACID; AMPA RECEPTOR; GLUTAMATE RECEPTOR; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; CELLULAR DISTRIBUTION; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MONKEY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; SENSORIMOTOR CORTEX; SENSORIMOTOR FUNCTION;

ANIMALS; HISTOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACACA; MACACA MULATTA; MOTOR CORTEX; NEURONS; RECEPTORS, AMPA; RECEPTORS, KAINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; SOMATOSENSORY CORTEX; TISSUE DISTRIBUTION;

EID: 0344849456     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990517)407:4<472::AID-CNE2>3.0.CO;2-2     Document Type: Article

References (130)

1. Akbarian S, Sucher NJ, Bradley D, Tafazzoli A, Trinh D, Hetrick P, Potkin SG, Sandman CA, Bunney WE, Jones EG. 1996. Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics. J Neurosci 16:19-30.
2. Armstrong-James M, Welker E, Callahan CA. 1993. The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat SI barrel cortex. J Neurosci 13:2149-2160.
3. Bear MF, Coleman H. 1990. Binocular competition in the control of geniculate cell size depends upon visual cortical N-methyl-D-aspartate receptor activation. Proc Natl Acad Sci USA 87:9246-9249.
4. Bettler B, Mulle C. 1995. AMPA and kainate receptors. Neuropharmacology 34:123-139.
5. Bettler B, Boulter J, Hermans-Borgmeyer I, O'Shea-Greenfield A, Deneris ES, Moll C, Borgmeyer U, Hollmann M, Heinemann S. 1990. Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5:583-595.
6. Bettler B, Egebjerg J, Sharma G, Pecht G, Hermans-Borgmeyer I, Moll C, Stevens CF, Heinemann S. 1992. Cloning of a putative glutamate receptor: a low affinity kainate-binding subunit. Neuron 8:257-265.
7. Bochet P, Audinat E, Lambolez B, Crepel F, Rossier J, lino M, Tsuzuki K, Ozawa S. 1994. Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel. Neuron 12:383-388.
8. Boulter J, Hollmann M, O'Shea-Greenfield A, Hartmey M, Deneris E, Maron C, Heinemann S. 1990. Molecular cloning and functional expression of glutamate receptor subunit gene. Science 249:1033-1036.
9. Bredt DS, Hwang PM, Glatt CE, Lowenstein C, Reed RR, Snyder SH. 1991. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351:714-718.
10. Buller AL, Larson HC, Schneider BE, Beaton JA, Morrisett RA, Monaghan DT. 1994. The molecular basis of NMDA receptor subtypes: native receptor diversity is predicted by subunit composition. J Neurosci 14:5471-5484.
11. Calford MB, Tweedale R. 1988. Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after induced sensory deficits. Nature 322:446-448.
12. Calford MB, Tweedale R. 1991a. Acute changes in cutaneous receptive fields in primary somatosensory cortex after digit denervation in adult flying fox. J Neurophysiol 65:178-187.
13. Calford MB, Tweedale R. 1991b. Immediate expansion of receptive fields of neurons in area 3b of macaque monkeys after digit denervation. Somatosens Motor Res 8:249-260.
14. Carder RK. 1997. Immunocytochemical characterization of AMPA-selective glutamate receptor subunits: laminar and compartmental distribution in macaque striate cortex. J Neurosci 17:3352-3363.
15. Carder R, SHC Hendry. 1994. Neuronal characterization, compartmental distribution, and activity-dependent regulation of glutamate immunore-activity in adult monkey striate cortex. J Neurosci 14:242-262.
16. Catania MV, Tölle TR, Monyer H. 1995. Differential expression of AMPA receptor subunits in NOS-positive neurons of cortex, striatum and hippocampus. J Neurosci 15:7046-7061.
17. Cik M, Chazot PL, Stephenson FA. 1993. Optimal expression of cloned NMDAR1/NMDAR2A heteromeric glutamate receptors: a biochemical characterization. Biochem J 296:877-883.
18. Clark SA, Allard T, Jenkins W, Merzenich MM. 1988. Receptive fields in the body-surface map in adult cortex defined by temporally correlated inputs. Nature 332:444-445.
19. Collingridge GL, Lester RAJ. 1989. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol Rev 40:143-210.
20. Conti F, Hicks TF. 1996. Excitatory amino acids and the cerebral cortex. Cambridge (MA): MIT Press.
21. Conti F, Minelli A. 1996. The anatomy of glutamatergic-transmission in the cerebral cortex. In: Conti F, Hicks TF, editors. Excitatory amino acids and the cerebral cortex. Cambridge (MA): MIT Press. p 77-93.
22. Conti F, Minelli A, Brecha NC. 1994. Cellular localization and laminar distribution of AMPA glutamate receptor subunits mRNAs and proteins in the rat cerebral cortex. J Comp Neurol 350:241-259.
23. Conti F, Minelli A, Pons TP. 1996. Changes in glutamate immunoreactivity in the somatic sensory cortex of adult monkeys induced by nerve cuts. J Comp Neurol 368:503-515.
24. Daw NW, Stein PSG, Fox K. 1993. The role of NMDA receptors in information processing. Annu Rev Neurosci 16:207-222.
25. Durand GM, Bennett MV, Zukin RS. 1993. Splice variants of the N-methyl-D-aspartate receptor NR1 identify domains involved in regulation by polyamines and protein kinase C. Proc Natl Acad Sci USA 90:6731-6735.
26. 2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci USA 90:755-759.
27. Egebjerg B, Bettler B, Hermans-Borgmeyer K, Heinemann S. 1991. Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 351:745-748.
28. Farrant M, Feldmeyer D, Takahashi T, Cull-Candy SG. 1994. NMDA-receptor channel diversity in the developing cerebellum. Nature 368: 335-339.
29. Fitzgerald LW, Deutch AY, Gasic G, Heinemann SF, Nestler EJ. 1995. Regulation of cortical and subcortical glutamate receptor subunit expression by antipsychotic drugs. J Neurosci 15:2453-2461.
30. Fleidervisch IA, Binshtok A, Gutnick MJ. 1998. Functionally distinct NMDA receptors mediate horizontal connectivity within layer 4 of mouse barrel cortex. Neuron in press.
31. Forrest D, Yuzaki M, Soares HD, Ng L, Luk DC, Sheng M, Stewart CL, Morgan JI, Connor JA, Curran T. 1994. Targeted disruption of NMDA receptor 1 gene abolishes NMDA response and results in neonatal death. Neuron 13:325-338.
32. Fox K, Armstrong-James M. 1986. The role of the anterior intralaminar nuclei and N-methyl D-aspartate receptors in the generation of spontaneous bursts in rat neocortical neurones. Exp Brain Res 63:505-518.
33. Fox K, Sato H, Daw NW. 1989. The location and function of NMDA receptors in cat and kitten visual cortex. J Neurosci 9:2445-2453.
34. Fox K, Sato H, Daw NW. 1990. The effect of varying stimulus intensity on NMDA receptor activity in cat visual cortex. J Neurophysiol 64:1414-1428.
35. Gall C, Sumikawa K, Lynch G. 1990. Levels of mRNA for a putative kainate receptor are affected by seizures. Proc Natl Acad Sci USA 87:7643-7647.
36. Garraghty PE, Kaas JH. 1991. Large-scale functional reorganization in adult monkey cortex after peripheral nerve injury. Proc Natl Acad Sci USA 88:6976-6980.
37. Garraghty PE, Muja N. 1996. NMDA receptors and plasticity in adult primate somatosensory cortex. J Comp Neurol 367:319-326.
38. Greenamyre JT, Olson JM, Penney JB Jr, Young AB. 1985. Autoradiographic characterization of N-methyl-D-aspartate-, quisqualate-and kainate-sensitive glutamate binding sites. J Pharmacol Exp Ther 233:254-263.
39. Hebb DO. 1949. The organization of behavior. New York: Wiley.
40. Herb A, Burnashev N, Werner P, Sakmann B, Wisden W, Seeburg PH. 1992. The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and form ion channels with distantly related subunits. Neuron 8:775-785.
41. Hollmann M, Heinemann S. 1994. Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
42. 2+ permeability of KA-AMPA-gated receptor channels depends on subunits composition. Science 252:851-853.
43. Hollmann M, Boulter J, Maron C, Beasley L, Sullivan J, Pecht G, Heinemann S. 1993. Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 10:943-954.
44. Hume RI, Dingledine R, Heinemann S. 1991. Identification of a site in glutamate receptor subunits that controls calcium permeability. Science 253:1028-1031.
45. Huntley GW, Rogers SW, Moran T, Janssen W, Archin N, Vickers JC, Cauley K, Heinemann SF, Morrison JH. 1993. Selective distribution of kainate receptor subunit immunoreactivity in monkey neocortex revealed by a monoclonal antibody that recognizes glutamate receptor subunits GluR5/6/7. J Neurosci 13:2965-2981.
46. Huntley GW, Vickers JC, Janssen W, Brose N, Heinemann SF, Morrison JH. 1994a. Distribution and synaptic localization of immunocytochemically identified NMDA receptor subunit proteins in the sensory-motor and visual cortices of the monkey and human. J Neurosci 14:3603-3619.
47. Huntley GW, Vickers JC, Morrison JH. 1994b. Cellular and synaptic localization of NMDA and non-NMDA receptor subunits in neocortex: organizational features related to cortical circuitry, function and disease. Trends Neurosci 17:536-543.
48. Huntley GW, Liang F, Woods TM, Tullai JW, Jones EG. 1995. NMDA receptor antagonist reversibly blocks plasticity of adult motor cortex representations. Soc Neurosci Abstr 21:1902P.
49. Ikeda K, Nagasawa M, Mori H, Araki K, Sakimura K, Watanabe M, Inoue K, Mishina M. 1992. Cloning and expression of the e4 subunit of the NMDA receptor channel. FEBS Lett 313:34-38.
50. Insel TR, Miller LP, Gelhard RE. 1990. The ontogeny of excitatory amino acids receptors in rat forebrain. I. N-methyl-D-aspartate and quisqualate receptors. Neuroscience 35:31-43.
51. Ishii T, Moriyoshi K, Sugihara H, Sakurada K, Kadotani H, Yokoi M, Akawaza C, Shigemoto R, Mizuno N, Masu M, Nakanishi S. 1993. Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J Biol Chem 268:2836-2843.
52. Jonas P, Racca C, Sakmann B, Seeburg PH, Monyer H. 1994. Functional and molecular diversity of AMPA-type glutamate receptor channels in neocortical neurons. Neuron 12:1281-1289.
53. Jones EG, Coulter JD, Hendry SHC. 1978. Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol 181:291-348.
54. Jones EG, Tighilet B, Tran BV, Huntsman MM. 1998. Nucleus-and cell-specific NMDA and non-NMDA receptor subunits in monkey thalamus. J Comp Neurol 397:371-393.
55. Jones KA, Baughman RW. 1988. NMDA-and non-NMDA-receptor components of excitatory synaptic potentials recorded from cells in layer V of rat visual cortex. J Neurosci 8:3522-3524.
56. Kaas JH, 1991. Plasticity of sensory and motor maps in adult mammals. Annu Rev Neurosci 14:137-167.
57. Kaas JH, Merzenich MM, Killackey HP. 1983. The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. Annu Rev Neurosci 6:325-356.
58. Kano M, Lino K, Kano M. 1991, Functional reorganization of adult cat somatosensory cortex is dependent on NMDA receptors. NeuroReport 2:77-80.
59. Kawaguchi Y. 1992. Receptor subtypes involved in callosally-induced postsynaptic potentials in rat frontal agranular cortex in vitro. Exp Brain Res 88:33-40.
60. Keinänen K, Wisden W, Sommer B, Werner P, Herb H, Verdoon TA, Sakmann B, Seeburg PH. 1990. A family of AMPA-selective glutamate receptors. Science 249:556-560.
61. Kelehand A, Doetsch GS. 1984. Time-dependent changes in the functional organization of somatosensory cerebral cortex following digit amputation in adult raccoons. Somatosens Res 2:49-81.
62. Kharazia VN, Wenthold RJ, Weinberg RJ. 1996. GluR1-immunopositive interneurons in rat neocortex. J Comp Neurol 368:399-412.
63. Kondo M, Sumino R, Okado H. 1997. Combinations of AMPA receptor subunit expression in individual cortical neurons correlate with expression of specific calcium binding proteins. J Neurosci 17:1570-1581.
64. Kutsuwada T, Kashiwabuchi N, Mori M, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, Mishina M. 1992. Molecular diversity of the NMDA receptor channel. Nature 358:36-41.
65. Larson-Prior LJ, Ulinski PS, Slater NT. 1991. Excitatory amino acid receptor-mediated transmission in geniculocortical and intracortical pathways within visual cortex. J Neurophysiol 66:293-306.
66. Laurie DJ, Seeburg PH. 1994. Regional and developmental heterogeneity in splicing of the rat brain NMDAR1 mRNA. J Neurosci 14:3180-3194.
67. Lomeli H, Mosbacher J, Melcher T, Höger T, Geiger JRP, Kuner T, Monyer H, Higuchi M, Bach A, Seeburg P. 1994. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266:1709-1713.
68. Manger PR, Woods TM, Jones EG. 1996. Plasticity of the somatosensory cortical map in macaque monkeys after chronic partial amputation of a digit. Proc R Soc Lond B 263:933-939.
69. Martin LJ, Blackstone CD, Levey AI, Huganir RL, Price DL. 1994. AMPA glutamate receptor subunits are differentially distributed in the rat brain. Neuroscience 53:327-358.
70. McKinley PA, Kruger L. 1988. Nonoverlapping thalamocortical connections to normal and deprived primary somatosensory cortex for similar forelimb receptive fields in chronic spinal cats. Somatosens Res 5:311-323.
71. Meguro H, Mori H, Araki K, Kushiya E, Kutsuwada T, Yamazaki M, Kumanishi T, Arakawa M, Sakimuram K, Mishina M. 1992. Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357:70-74.
72. Merzenich MM, Kaas JH, Wall J, Nelson RJ, Sur M, Felleman D. 1983a. Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8:33-55.
73. Merzenich MM, Kaas JH, Wall JT, Sur M, Nelson RJ, Felleman DJ. 1983b. Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10:639-665.
74. Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM. 1984. Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol 224:591-605.
75. Miller KD, Keller JB, Stryker MP. 1989. Ocular dominance column development: analysis and simulation. Science 245:605-615.
76. 2+ permeability of AMPA-selective glutamate receptor channels. Biochem Biophys Res Commun 180:813-821.
77. 3H]kainic acid binding sites in rat CNS as determined by autoradiography. Brain Res 252:91-100.
78. 3H-L-glutamate binding sites. Nature 306:176-179.
79. Monyer H, Seeburg PH, Wisden W. 1991. Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron 5:1-20.
80. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, Seeburg PH. 1992. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221.
81. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. 1994. Developmental and regional expression in the rat brain and functional properties of four NMDA receptor subtypes. Neuron 12:529-540.
82. Mon H, Yamakura T, Masaki H, Mishina M. 1993. Involvement of the carboxyl-terminal region in modulation by TPA of the NMDA receptor channel. NeuroReport 4:519-522.
83. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuni N, Nakanishi S. 1991. Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37.
84. Nakanishi S. 1992. Molecular diversity of glutamate receptors and implications for brain function. Science 258:597-603.
85. Nicoll A, Larkman A, Blakemore C. 1992. EPSPs in rat neocortical pyramidal neurones in vitro are prolonged by NMDA receptor-mediated currents. Neurosci Lett 143:5-9.
86. Nishigori A, Tsumoto T, Kimura F. 1990. Contribution of quisqualate/ kainate and NMDA receptors to excitatory synaptic transmission in the rat's visual cortex. Vis Neurosci 5:591-604.
87. 3]AMPA binding to glutamate receptor subpopulations in rat brain. Brain Res 402:243-254.
88. Pellegrini-Giampetro DE, Bennett MVL, Zukin RS. 1991. Differential expression of three glutamate receptor genes in the developing rat brain: an in situ hybridization study. Proc Natl Acad Sci USA 88:4157-4161.
89. Petralia RS, Wenthold RJ. 1992. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neural 318:329-354.
90. Petralia RS, Wang YX, Wenthold RJ. 1994a. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14:6102-6120.
91. Petralia RS, Yokotani N, Wenthold RJ. 1994b. Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective antipeptide antibody. J Neurosci 14:667-696.
92. Pin JP, Duvoisin R. 1995. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1-26.
93. Pons TP, Garraghty PE, Ommaya AK, Kaas JH, Taub E, Mishkin M. 1991. Massive cortical reorganization after sensory deafferentation in adult macaques. Science 252:1857-1860.
94. Powell TPS, Mountcastle VB. 1959. The cytoarchitecture of the postcentral gyrus of the monkey Macaco mulatta. Bull Johns Hopkins Hosp 105:108-131.
95. Qiu XO, O'Donogue DL, Humphrey DR. 1990. NMDA antagonist (MK-801) blocks plasticity of motor cortex maps induced by passive limb movement. Soc Neurosci Abstr 16:422.
96. Raditsch M, Ruppersberg JP, Kuner T, Gunther W, Schoepfer R, Seeburg PH, Jahn W, Witzemann V. 1993. Subunit-specific block of cloned NMDA receptors by argiotoxin 636. FEBS Lett 324:63-66.
97. 3]AMPA, a structural analogue of glutamic acid. Brain Res 309:173-177.
98. Rasmusson DD. 1982. Reorganization of raccoon somatosensory cortex following removal of the fifth digit. J Comp Neurol 205:313-326.
99. Roberts TS, Akert K. 1963. Insular and opercular cortex and its thalamic projection in Macaca mulatta. Schweiz Arch Neurol Neurochir Psychiatr 92:1-43.
100. Robner S, Kumar A, Kues W, Witzemann V, Schliebs R. 1993. Differential laminar expression of AMPA receptor genes in the developing rat visual cortex using in situ hybridization histochemistry. Effect of visual deprivation. Int J Dev Neurosci 11:411-424.
101. Sakimura K, Monta T, Kushiya E, Mishina M. 1992. Primary structure and expression of the gamma-2 subunit of the glutamate receptor channel selective for kainate. Neuron 8:267-274.
102. Scherzer CB, Landwehrmeyer GB, Kerner JA, Counihan TJ, Kosinski CM, Standaert DG, Daggett LP, Velicelebi G, Penney JR, Young AB. 1998. Expression of N-methyl-D-aspartate receptor subunit mRNAs in the human brain: hippocampus and cortex. J Comp Neurol 390:75-90.
103. Seeburg PH. 1993. The molecular biology of mammalian glutamate receptor channels. Trends Neurosci 16:359-365.
104. Shirokawa T, Nishigoiori A, Kimura F, Tsumoto T. 1989. Actions of excitatory amino acid antagonists on synaptic potentials of layer II/III neurons of the cat's visual cortex. Exp Brain Res 78:489-500.
105. Sommer B, Seeburg PH. 1992. Glutamate receptor channels: novel properties and new clones. Trends Pharmacol Sci 13:291-296.
106. Sommer B, Keinänen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Köhler M, Takagi T, Sakmann B, Seeburg PH. 1990. Flip and flop: a cell specific functional switch in glutamate operated channels of the CNS. Science 249:1580-1585.
107. Sommer B, Burnashev N, Verdoorn TA, Keinänen K, Sakmann B, Seeburg PH. 1992. A glutamate receptor channel with high affinity for domoate and kainate. EMBO J 11:1651-1656.
108. Stern P, Behe P, Schoepfer R, Colquhoun D. 1992. Single-channel conductances of NMDA receptors expressed from cloned cDNAs: comparison with native receptors. Proc R Soc Lond B 250:271-277.
109. Stewart MG, Siucinska E, Kossut M, Davies H. 1993. Loss of glutamate immunoreactivity from mouse first somatosensory (SI) cortex following neonatal vibrissal lesion. Brain Res 621:331-338.
110. Suchanek B, Seeburg PH, Sprengel R. 1995. Gene structure of the murine N-methyl D-aspartate receptor subunit NR2C. J Biol Chem 270:41-44.
111. Sugihara H, Moriyoshi K, Ishii T, Masu M, Nakanishi S. 1992. Structures and properties of seven isoforms of the NMDA receptor generated by alternative splicing. Biochem Biophys Res Commun 185:826-832.
112. Sutor B, Hablitz JJ. 1989. EPSPs in rat neocortical neurons in vitro. II. Involvement of N-methyl-D-aspartate receptors in the generation of EPSPs. J Neurophysiol 61:621-634.
113. Tamura H, Hicks TP, Hata Y, Tsumoto T, Yamatodani A. 1990. Release of glutamate and aspartate from the visual cortex of the cat following activation of afferent pathways. Exp Brain Res 80:447-455.
114. Thomson AM. 1986. A magnesium-sensitive post-synaptic potential in rat cerebral cortex resembles neuronal responses to N-methyl-aspartate. J Physiol (Lond) 370:531-549.
115. Thomson AM, West DC. 1993. Fluctuations in pyramid-pyramid excitatory postsynaptic potentials modified by presynaptic firing pattern and postsynaptic membrane potential using paired intracellular recordings in rat neocortex. Neuroscience 54:329-346.
116. Thomson AM, Deuchars J, West DC. 1993. Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically, and self-facilitation, mediated postsynaptically. J Neurophysiol 70:2354-2369.
117. Tighilet B, Jones EG. 1996. Molecular and neurochemical changes occurring in the glutamate receptors and type II calcium-calmodulin-dependent protein kinase in adult monkey visual cortex. Soc Neurosci Abstr 390:278-297.
118. Tighilet B, Huntsman MM, Hashikawa T, Murray KD, Isackson PJ, Jones EG. 1997. Cell-specific expression of type II calcium/calmodulin dependent protein kinase isoforms and glutamate receptors in normal and visually deprived lateral geniculate nucleus of monkeys. J Comp Neurol 390:278-297.
119. Tsumoto T. 1990. Excitatory amino acid transmitters and their receptors in neural circuits of the cerebral cortex. Neurosci Res 9:79-102.
120. Tsumoto T, Masui H, Sato H. 1986. Excitatory amino acid transmitters in neuronal circuits of the cat visual cortex. J Neurophysiol 55:469-480.
121. 3H] kainic acid binding sites in the rat forebrain. Eur J Neurosci 86:361-371.
122. Verdoorn TA, Burnashev N, Monyer H, Seeburg PH, Sakmann B. 1991. Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252:1715-1718.
123. Vickers JC, Huntley GW, Edwards AM, Moran T, Rogers SW, Heinemann SF, Morrison JH. 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.
124. Vickers JC, Huntley GW, Hof PR, Bederson J, De Felipe J, Morrison JH. 1995. Immunocytochemical localization of non-NMDA ionotropic excitatory amino acid receptor subunits in human neocortex. Brain Res 671:175-180.
125. Wafford KA, Bain CJ, Le Bourdelles B, Whiting PJ, Kemp JA. 1993. Preferential co-assembly of recombinant NMDA receptors composed of three different subunits. NeuroReport 4:1347-1349.
126. Watanabe M, Mishina M, Inoue Y. 1994. Distinct spatiotemporal expressions of five NMDA receptor channel subunit mRNAs in the cerebellum. J Comp Neurol 343:513-519.
127. Wenzel A, Scheurer L, Künzi R, Fritschy JM, Mohler H, Benke D. 1995. Distribution of NMDA receptor subunit proteins NR2A, 2B, 2C and 2D in rat brain. NeuroReport 7:45-48.
128. Werner P, Voigt M, Keinänen K, Wisden W, Seeburg PH. 1991. Cloning of a putative high-affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature 361:742-744.
129. Wisden W, Seeburg PH. 1993. A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13:3582-3598.
130. 2+ permeable AMPA/kainate channels display distinct receptor immunore-activity and are GABAergic. Neurobiol Dis 1:43-49.