Synaptic localization of GABA(A) receptor subunits in the striatum of the rat

Journal of Comparative Neurology

Volumn 416, Issue 2, 1999, Pages 158-172

  Fujiyama, Fumino ^a,d   Fritschy, Jean Marc ^b   Stephenson, F Anne ^c   Bolam, J Paul ^a  

^a MRC Anat Neuropharmacology Unit   (United Kingdom)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF LONDON   (United Kingdom)

^d SAGA UNIVERSITY   (Japan)

Author keywords

Basal ganglia; GABA; Immunolabeling; Synapses

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BASAL GANGLION; CORPUS STRIATUM; GLOBUS PALLIDUS; IMMUNOGOLD STAINING; MORPHOLOGY; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ASSAY; RAT; SYNAPSE;

ANIMALS; CEREBRAL CORTEX; CORPUS STRIATUM; FEMALE; MICROSCOPY, ELECTRON; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTORS, GABA-A; SYNAPSES;

EID: 0033540255     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000110)416:2<158::AID-CNE3>3.0.CO;2-L     Document Type: Article

References (96)

1. 2-subunit mRNA-containing neurons in the rat central nervous system. Neuroscience 47:45-61.
2. A receptor deduced from mutation-induced rectification. Neuroreport 5:285-288.
3. Baude A, Nusser Z, Roberts JDB, Mulvihill E, Mcilhinney RAJ, Somogyi P. 1993. The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
4. Baude A, Molnar E, Latawiec D, McIlhinney RAJ, Somogyi P. 1994. Synaptic and nonsynaptic localization of the GluR1 subunit of the AMPA-type excitatory amino acid receptor in the rat cerebellum. J Neurosci 14:2830-2843.
5. Baude A, Nusser Z, Molnar E, McIlhinney RAJ, Somogyi P. 1995. High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience 69:1031-1055.
6. Beckstead RM. 1983. A pallidostriatal projection in the cat and monkey. Brain Res Bull 11:629-632.
7. A receptor subtypes differentiated by γ subunit variants: prevalence, pharmacology and subunit architecture. Neuropharmacology 35:1413-1422.
8. Bennett BD, Bolam JP. 1993. Characterisation of calretinin-immunoreactive neurones in the rat striatum. Brain Res 609:137-148.
9. Bennett BD, Bolam JP. 1994a. Localisation of parvalbumin-immunoreactive structures in primate caudate-putamen. J Comp Neurol 347:340-356.
10. Bennett BD, Bolam JP. 1994b. Synaptic input and output of parvalbumin-immunoreactive neurones in the neostriatum of the rat. Neuroscience 62:707-719.
11. Bernard V, Bolam JP. 1998. Subcellular and subsynaptic distribution of the NR1 subunit of the NMDA receptor in the neostriatum and globus pallidus of the rat: co-localization at synapses with the GluR2/3 subunit of the AMPA receptor. Eur J Neurosci 10:3721-3736.
12. Bernard V, Somogyi P, Bolam JP. 1997. Cellular, subcellular, and subsynaptic distribution of AMPA-type glutamate receptor subunits in the neostriatum of the rat. J Neurosci 17:819-833.
13. Bevan MD, Booth PAC, Eaton SA, Bolam JP. 1998. Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J Neurosci 18:9438-9452.
14. Bolam JP, Bennett B. 1995. The microcircuitry of the neostriatum. In: Ariano M, Surmeier DJ, editors. Molecular and cellular mechanisms of neostriatal functions. Austin, TX: R.G. Landes; pp 1-19.
15. Bolam JP, Somogyi P, Totterdell S, Smith AD. 1981. A second type of striatonigral neuron: a comparison between retrogradely labelled and Golgi-stained neurons at the light and electron microscopic levels. Neuroscience 6:2141-2157.
16. 3H) γ aminobutyric acid: combination of Golgi-staining, autoradiography and electron microscopy. J Comp Neurol 213:121-134.
17. Bolam JP, Powell JF, Wu J-Y, Smith AD. 1985. Glutamate decarboxylase-immunoreactive structures in the rat neostriatum. A correlated light and electron microscopic study including a combination of Golgi-impregnation with immunocytochemistry. J Comp Neurol 237:1-20.
18. Bouyer JJ, Park DH, Joh TH, Pickel VM. 1984. Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res 302:267-275.
19. A receptors. J Physiol Lond 497:753-759.
20. 1-subunit-immunopositive neurons in the rat striatum. Brain Res 722:185-189.
21. A receptor subunit changes induced by unilateral 6-OHDA lesion of the nigrostriatal pathway. Mol Brain Res 48:243-250.
22. Clarke NP, Bolam JP. 1997. Colocalization of neurotransmitters in the basal ganglia of the rat. Br J Pharmacol 120:281P.
23. Clarke NP, Bolam JP. 1998. Distribution of glutamate receptor subunits at neurochemically characterized synapses in the entopeduncular nucleus and subthalamic nucleus of the rat. J Comp Neurol 397:403-420.
24. Cowan RL, Wilson CJ, Emson PC, Heizmann CW. 1990. Parvalbumin-containing GABAergic interneurons in the rat neostriatum. J Comp Neurol 302:197-205.
25. Dimova R, Vuillet J, Seite R. 1980. Study of the rat neostriatum using a combined Golgi-electron microscope technique and serial sections. Neuroscience 5:1581-1596.
26. A/benzodiazepine receptor. J Cell Biol 110:2043-2048.
27. Freund TF, Powell J, Smith AD. 1984. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 13:1189-1215.
28. A-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154-194.
29. 3-subunits with serotonergic and GABAergic neurons. Neuroscience 54:881-892.
30. A-receptor subtypes in cholinergic and parvalbumin-positive neurons of the rat and marmoset medial septum-diagonal band complex. Neuroscience 65:101-117.
31. Hanley JJ, Bolam JP. 1997. Synaptology of the nigrostriatal projection in relation to the compartmental organization of the neostriatum in the rat. Neuroscience 81:353-370.
32. Häring P, Stähli C, Schoch P, Takacs B, Staehelin T, Möhler H. 1985. Monoclonal antibodies reveal structural homogeneity of γ-aminobutyric acid/benzodiazepine receptors in different brain areas. Proc Natl Acad Sci USA 82:4837-4841.
33. A receptors in the rat basal forebrain: a cytochemical study with glutamic acid decarboxylase, choline acetyltransferase, calcium-binding proteins and nitric oxide synthase as second markers. Brain Res 692:215-226.
34. Hodgson AJ, Penke B, Erdei A, Chubb IW, Somogyi P. 1985. Antisera to γ-aminobutyric acid. I. Production and characterization using a new model system. J Histochem Cytochem 33:229-239.
35. Ingham CA, Hood SH, Taggart P, Arbuthnott GW. 1998. Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway. J Neurosci 18:4732-4743.
36. Izzo PN, Bolam JP. 1988. Cholinergic synaptic input to different parts of spiny striatonigral neurons in the rat. J Comp Neurol 269:219-234.
37. Jayaraman A. 1983. Topographic organization and morphology of peripallidal and pallidal cells projecting to the striatum in cats. Brain Res 275:279-286.
38. Kawaguchi Y. 1997. Neostriatal cell subtypes and their functional roles. Neurosci Res 27:1-8.
39. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC. 1995. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527-535.
40. Kharazia VN, Weinberg RJ. 1997. Tangential synaptic distribution of NMDA and AMPA receptors in rat neocortex. Neurosci Lett 238:41-44.
41. Kharazia VN, Phend KD, Rustioni A, Weinberg RJ. 1996. EM colocalization of AMPA and NMDA receptor subunits at synapses in rat cerebral cortex. Neurosci Lett 210:37-40.
42. Kita H. 1993. GABAergic circuits of the striatum. In: Arbuthnott GW, Emson PC, editors. Chemical signalling in the basal ganglia. Prog Brain Res 99:51-72.
43. Kita H, Kitai ST. 1988. Glutamate decarboxylase immunoreactive neurons in rat neostriatum: their morphological types and populations. Brain Res 447:346-352.
44. Kita H, Kitai ST. 1994. The morphology of globus pallidus projection neurons in the rat: an intracellular staining study. Brain Res 636:308-319.
45. Kita H, Kosaka T, Heizmann CW. 1990. Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 536:1-15.
46. Kubota Y, Mikawa S, Kawaguchi Y. 1993. Neostriatal GABAergic interneurones contain NOS, calretinin or parvalbumin. Neuroreport 5:205-208.
47. A receptor subunit messenger RNAs in the motor-related thalamic nuclei and basal ganglia of Macaca mulatto studied with in situ hybridization histochemistry. Neuroscience 85:179-204.
48. A receptor subunit expression in intrastriatal striatal grafts. Comparison between normal developing striatum and developing striatal grafts. Dev Brain Res 103:185-194.
49. Lujan R, Nusser Z, Roberts JDB, Shigemoto R, Somogyi P. 1996. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8:1488-1500.
50. A-receptor subtypes really occur in the brain? Trends Neurosci 19:139-143.
51. A receptor subtypes immunopurified from rat brain with α subunit-specific antibodies have unique pharmacological properties. Neuron 7:667-676.
52. Morello M, Reiner A, Sancesario G, Karle EJ, Bernardi G. 1997. Ultrastructural study of nitric oxide synthase-containing striatal neurons and their relationship with parvalbumin-containing neurons in rats. Brain Res 776:30-39.
53. Nambu A, Llinas R. 1997. Morphology of globus pallidus neurons: its correlation with electrophysiology in guinea pig brain slices. J Comp Neurol 377:85-94.
54. A and glutamate receptors in relation to transmitter release sites on the surface of cerebellar neurones. Prog Brain Res 114:109-127.
55. Nusser Z, Mulvihill E, Streit P, Somogyi P. 1994. Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61:421-427.
56. 2/3 subunits of the GABAA receptor in relation to specific GABAergic synapses in the dentate gyrus. Eur J Neurosci 7:630-646.
57. A receptors on cerebellar granule cells as determined by a quantitative immunogold method. J Neurosci 15:2948-2960.
58. Nusser Z, Sieghart W, Benke D, Fritschy JM, Somogyi P. 1996a. Differential synaptic localization of two major γ-aminobutyric acid type A receptor a subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA 93:11939-11944.
59. A receptor is concentrated in both inhibitory and excitatory synapses on cerebellar granule cells. J Neurosci 16:103-114.
60. A receptor number underlie variation in GABA mini amplitude. Neuron 19:697-709.
61. A receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18:1693-1703.
62. Ottersen OP, Landsend AS. 1997. Organization of glutamate receptors at the synapse. Eur J Neurosci 9:2219-2224.
63. Penny GR, Wilson CJ, Kitai ST. 1988. Relationship of the axonal and dendritic geometry of spiny prejection neurons to the compartmental organization of the neostriatum. J Comp Neurol 269:275-289.
64. A receptor subunits in the rat CNS. J Comp Neurol 326:193-216.
65. Pickel VM, Chan J. 1990. Spiny neurons lacking choline acetyltransferase immunoreactivity are major targets of cholinergic and catecholaminergic terminals in rat striatum. J Neurosci Res 25:263-280.
66. A receptors of adult cerebellum demonstrates two a subunits per receptor oligomer. J Biol Chem 270:21285-21290.
67. Popratiloff A, Weinberg RJ, Rustioni A. 1998. AMPA receptors at primary afferent synapses in substantia gelatinosa after sciatic nerve section. Eur J Neurosci 10:3220-3230.
68. Rajakumar N, Elisevich K, Flumerfelt BA. 1994. The pallidostriatal projection in the rat: a recurrent inhibitory loop? Brain Res 651:332-336.
69. A-receptor α1-subunit and parvalbumin immunolabeling. Exp Brain Res 121:215-221.
70. Rusakov DA, Harrison E, Stewart MG. 1998. Synapses in hippocampus occupy only 1-2% of cell membranes and are spaced less than half-micron apart: a quantitative ultrastructural analysis with discussion of the physiological implications. Neuropharmacology 37:513-521.
71. A receptors and benzodiazepine receptors as shown by monoclonal antibodies. Nature 314:168-171.
72. Shu SY, Peterson GM. 1988. Anterograde and retrograde axonal transport of Phaseolus vulgaris leucoagglutinin (PHA-L) from the globus pallidus to the striatum of the rat. J Neurosci Methods 25:175-180.
73. Smith AD, Bolam JP. 1990. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. Trends Neurosci 13:259-265.
74. A receptors. Trends Pharmacol Sci 16:162-168.
75. Smith Y, Bennett BD, Bolam JP, Parent A, Sadikot AF. 1994. Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey. J Comp Neurol 344:1-19.
76. Smith Y, Bevan MD, Shink E, Bolam JP. 1998. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86:353-387.
77. Somogyi P, Smith AD. 1979. Projection of neostriatal spiny neurons to the substantia nigra. Application of a combined Golgi-staining and horseradish peroxidase transport procedure at both light and electron microscopic levels. Brain Res 178:3-15.
78. Somogyi P, Hodgson AJ. 1985. Antisera to γ-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J Histochem Cytochem 33:249-57.
79. Somogyi P, Bolam JP, Smith AD. 1981. Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure. J Comp Neurol 195:567-584.
80. Somogyi P, Hodgson AJ, Chubb IW, Penke B, Erdei A. 1985. Antisera to γ-aminobutyric acid. II. Immunocytochemical application to the central nervous system. J Histochem Cytochem 33:240-248.
81. 2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology 35:1425-1444.
82. Spooren WPJM, Lynd-Balta E, Mitchell S, Haber SN. 1996. Ventral pallidostriatal pathway in the monkey: evidence for modulation of basal ganglia circuits. J Comp Neurol 370:295-312.
83. Staines WA, Fibiger HC. 1984. Collateral projections of neurons of the rat globus pallidus to the striatum and substantia nigra. Exp Brain Res 56:217-220.
84. Staines WA, Atmadja S, Fibiger HC. 1981. Demonstration of a pallidostriatal pathway by retrograde transport of HRP-labeled lectin. Brain Res 206:446-450.
85. A receptor. Biochem J 310:1-9.
86. A receptors. In: Chad J, Wheal H, editors. Molecular neurobiology: a practical approach. Oxford, UK: IRL Press; pp 183-204.
87. van der Kooy D, Coscina DV, Hattori T. 1981. Is there a non-dopaminergic nigrostriatal pathway? Neuroscience 6:345-357.
88. Wainer BH, Bolam JP, Freund TF, Henderson Z. Totterdell S, Smith AD. 1984. Cholinergic synapses in the rat brain: a correlated light and electron microscopic study employing a monoclonal antibody against choline acetyltransferase. Brain Res 308:69-76.
89. 1-subunit of the GABAA receptor in the rat. Neuroscience 80:775-792.
90. 2/3 subunits in the baboon brain. J Comp Neurol 397:297-325.
91. Walker RH, Arbuthnott GW, Wright AK. 1989. Electrophysiological and anatomical observations concerning the pallidostriatal pathway in the rat. Exp Brain Res 74:303-310.
92. A receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 9:533-548.
93. Wilson CJ, Groves PM. 1980. Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular injection of horseradish peroxidase. J Comp Neurol 194: 599-615.
94. A receptor subunit messenger mRNAs in the rat brain. 1. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040-1062.
95. Yung KKL, Smith AD, Levey AI, Bolam JP. 1996. Synaptic connections between spiny neurons of the direct and indirect pathways in the neostriatum of the rat: evidence from dopamine receptor and neuropeptide immunostaining. Eur J Neurosci 8:861-869.
96. 3) of GABAA receptor in the rat brain. J Comp Neurol 303:637-657.