Glutamate decarboxylase-67 messenger RNA expression in normal human basal ganglia and in Parkinson's disease

Neuroscience

Volumn 75, Issue 2, 1996, Pages 389-406

  Nisbet, A P ^a   Eve, D J ^a   Kingsbury, A E ^a   Daniel, S E ^a   Marsden, C D ^a   Lees, A J ^a   Foster, O J F ^b  

^a Institute of Neurology   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

globus pallidus; in situ hybridization; striatum; subthalamic nucleus

Indexed keywords

GLUTAMATE DECARBOXYLASE; MESSENGER RNA;

ADULT; AGED; ARTICLE; BASAL GANGLION; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; GLOBUS PALLIDUS; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; MALE; PARKINSON DISEASE; PRIORITY JOURNAL; SUBTHALAMIC NUCLEUS;

EID: 0030601701     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00299-0     Document Type: Article

References (111)

1. Agid Y., Ruberg M., Raisman R., Hirsch E. and Javoy-Agid F. (1990) The biochemistry of Parkinson's disease. In Parkinson's Disease (ed Stern G.) pp. 99-125. Chapman and Hall, Medical, London.
2. Aronin N., DiFiglia M., Graveland G. A., Schwartz W. J., Wu J. -Y. Localization of immunoreactive enkephalins in GABA synthesizing neurons of the rat neostriatum. Brain Res. 300:1984;376-380.
3. Augood S. J., Emson P. C., Mitchell I. J., Boyce S., Clarke C. E., Crossman A. R. Cellular localisation of enkephalin gene expression in MPTP-treated cynomolgus monkeys. Molec. Brain Res. 6:1989;85-92.
4. Aziz T. Z., Peggs D., Sambrook M. A., Crossman A. R. Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism in the primate. Movement Disord. 6:1991;288-292.
5. Barton A. J. L., Pearson R. C. A., Najlerahim A., Harrison P. J. Pre- and post-mortem influences on brain RNA. J. Neurochem. 61:1993;1-11.
6. Beach T. G., McGeer E. G. The distribution of substance P in the primate basal ganglia: an immunohistochemical study of baboon and human brain. Neuroscience. 13:1984;29-52.
7. Benson D. L., Isackson P. J., Hendry S. H., Jones E. G. Differential gene expression for glutamic acid decarboxylase and type II calcium-calmodulin-dependent protein kinase in basal ganglia, thalamus, and hypothalamus of the monkey. J. Neurosci. 11:1991;1540-1564.
8. Bergman H., Wichmann T., DeLong M. R. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science. 249:1990;1436-1438.
9. Besson M. J., Graybiel A. M., Quinn B. Co-expression of neuropeptides in the cat's striatum: an immunohistochemical study of substance P, dynorphin B and enkephalin. Neuroscience. 39:1990;33-58.
10. Bolam J. P., Powell J. F., Wu J. -Y., Smith A. D. 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. 237:1985;1-20.
11. Bolam J. P., Smith Y. The GABA and substance P input to dopaminergic neurones in the substantia nigra of the rat. Brain Res. 529:1990;57-78.
12. Bolam J. P., Somogyi P., Totterdell S., Smith A. D. A second type of striatonigral neuron: a comparison between retrogradely labelled and Golgi-stained neurons at the light and electron microscopic levels. Neuroscience. 6:1981;2141-2157.
13. Brene S., Lindefors N., Herrera Marschitz M., Persson H. Expression of dopamine D2 receptor and choline acetyltransferase mRNA in the dopamine deafferented rat caudate-putamen. Expl Brain Res. 83:1990;96-104.
14. Bu D. F., Erlander M. G., Hitz B. C., Tillakaratne N. J., Kaufman D. L., Wagner-McPherson C. B., Evans G. A., Tobin A. J. Two human decarboxylases, 65-KDa GAD and 67-KDa GAD are each encoded by a single gene. Proc. natn. Acad. Sci. U.S.A. 89:1992;2115-2119.
15. Carpenter M. B., Jayaraman A. Subthalamic nucleus of the monkey: connections and immunocytochemical features of afferents. J. Hirnforsch. 31:1990;653-668.
16. Celio M. R., Heizmann C. W. Calcium-binding protein parvalbumin as a neuronal marker. Nature. 293:1981;300-302.
17. Chang H. T., Kitai S. T. Large neostriatal neurons in the rat: an electron microscopic study of gold-toned Golgi-stained cells. Brain Res. Bull. 8:1982;631-643.
18. Chesselet M. -F., Robbins E. Characterization of striatal neurons expressing high levels of glutamic acid decarboxylase messenger RNA. Brain Res. 492:1989;237-244.
19. Chomczynski P., Sacchi N. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analyt. Biochem. 162:1987;156-159.
20. Consolo S., Wu C. F., Fusi R. D-1 receptor-linked mechanism modulates cholinergic neurotransmission in rat striatum. J. Pharmac. exp. Ther. 242:1987;300-305.
21. Cowan R. L., Wilson C. J., Emson P. C., Heizmann C. W. Parvalbumin-containing GABAergic interneurons in the rat neostriatum. J. comp. Neurol. 302:1990;197-205.
22. Dawson T. M., Bredt D. S., Fotuhi M., Hwang P. M., Snyder S. H. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. natn. Acad. Sci. U.S.A. 88:1991;7797-7801.
23. Dawson V. L., Dawson T. M., Wamsley J. K. Muscarinic and dopaminergic receptor subtypes on striatal cholinergic interneurons. Brain Res. Bull. 25:1990;903-912.
24. DeLong M. R. Primate models of movement disorders of basal ganglia origin. Trends. Neurosci. 13:1990;281-285.
25. DiFiglia M. Synaptic organization of cholinergic neurons in the monkey neostriatum. J. comp. Neurol. 255:1987;245-258.
26. Dubé L., Descarries L. Gabaergic spiny neurons in the neostriatum of the rat. Soc. Neurosci. Abstr. 12:1986;876.
27. Engber T. M., Susel Z., Kuo S., Gerfen C. R., Chase T. N. Levodopa replacement therapy alters enzyme activities in striatum and neuropeptide content in striatal output regions of 6-hydroxydopamine lesioned rats. Brain Res. 552:1991;113-118.
28. Erlander M. G., Tobin A. J. The structural and functional heterogeneity of glutamic acid decarboxylase: a review. Neurochem. Res. 16:1991;215-226.
29. Everitt B. J., Sirkia T. E., Roberts A. C., Jones G. H., Robbins T. W. Distribution and some projections of cholinergic neurons in the brain of the common marmoset, callithrix jacchus. J. comp. Neurol. 271:1988;533-558.
30. Feldblum S., Erlander M. G., Tobin A. J. Different distributions of GAD65 and GAD67 mRNAs suggest that the two glutamate decarboxylases play distinctive functional roles. J. Neurosci. Res. 34:1993;689-706.
31. Filion M., Tremblay L. and Bedard P. J. (1989) Excessive and unselective responses of medial pallidal neurons to both passive movement and striatal stimulation in monkeys with MPTP-induced parkinsonism. In Neural Mechanisms in Disorders of Movement (eds Crossman A. R. and Sambrook M. A.) pp. 157-164. John Libbey and Co, London, Paris.
32. Fisher R. S., Boylan M. K., Hull C. D., Buchwald N. A., Levine M. S. Branched projections of pallidal and peripallidal neurons to neocortex and neostriatum: a double-labelling study in the cat. Brain Res. 326:1985;156-159.
33. Gerfen C. R., McGinty J. F., Young W. S. Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridization histochemical analysis. J. Neurosci. 11:1991;1016-1031.
34. Gerfen C. R., Young W. S. Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridisation histochemistry and fluorescent retrograde tracing study. Brain Res. 460:1988;161-167.
35. Gonzales C., Kaufman D. L., Tobin A. J., Chesselet M. -F. Distribution of glutamic acid decarboxylase (Mr 67,000) in the basal ganglia of the rat: an immunohistochemical study with a selective cDNA-generated polyclonal antibody. J. Neurocytol. 20:1991;953-961.
36. Graybiel A. M., Ragsdale C. W. Jr. Fibre connections of the basal ganglia. Prog. Brain Res. 51:1979;239-283.
37. Griffiths P. D., Sambrook M. A., Perry R., Crossman A. R. Changes in benzodiazepine and acetylcholine receptors in the globus pallidus in Parkinson's disease. J. Neurol. Sci. 100:1990;131-136.
38. Haber S. N., Watson S. J. The comparative distribution of enkephalin, dynorphin and substance P in the human globus pallidus and basal forebrain. Neuroscience. 14:1985;1011-1024.
39. Herrero M. -T., Augood S. J., Hirsch E. C., Javoy-Agid F., Luquin M. R., Agid Y., Obeso J. A., Emson P. C. Effects of L-DOPA on preproenkephalin and preprotachykinin gene expression in the MPTP-treated monkey striatum. Neuroscience. 68:1995;1189-1198.
40. Herrero M. -T., Ruberg M., Hirsch E. C., Mouatt A., Tobin A. J., Agid Y., Obeso J. A., Javoy-Agid F. In situ hybridization of GAD mRNA in monkey and human brain: quantification at both regional and cellular levels. Neurosci. Lett. 157:1993;57-61.
41. Hirsch E. C., Graybiel A. M., Hersh L. B., Duyckaerts C., Agid Y. Striosomes and extrastriosomal matrix contain different amounts of immunoreactive choline acetyltransferase in the human striatum. Neurosci. Lett. 96:1989;145-150.
42. Jayaraman A. Topographical organization and morphology of peripallidal and pallidal cells projecting to the striatum in cats. Brain Res. 275:1983;279-286.
43. Johnson S. A., Morgan D. G., Finch C. E. Extensive postmortem stability of RNA from rat and human brain. J. Neurosci. Res. 16:1986;267-280.
44. Karlsen A. E., Hagopian W. A., Grubin C. E., Dube S., Disteche C. M., Adler D. A., Barmeier H., Mathewes S., Grant F. J., Foster D., Lernmark A. Cloning and primary structure of a human islet isoform of glutamic acid decarboxylase from chromosome 10. Proc. natn. Acad. Sci. U.S.A. 88:1991;8337-8341.
45. Kaufman D. L., Houser C. R., Tobin A. J. Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions. J. Neurochem. 56:1991;720-723.
46. Kingsbury A. E., Foster O. J. F., Nisbet A. P., Cairns N., Bray L., Eve D. J., Lees A. J., Marsden C. D. Tissue pH as an indicator of mRNA preservation in human post-mortem brain. Molec. Brain Res. 28:1995;311-318.
47. Kish S. J., Rajput A., Gilbert J., Rozdilsky B., Chang L. J., Shannak K., Hornykiewicz O. Elevated gamma-aminobutyric acid level in striatal but not extrastriatal brain regions in Parkinson's disease: correlation with striatal dopamine loss. Ann. Neurol. 20:1986;26-31.
48. Kish S. J., Shannak K., Hornykiewicz O. Uneven patterns of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. New Engl. J. Med. 318:1988;876-880.
49. Kita H., Kosaka T., Heizmann C. W. Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res. 536:1990;1-15.
50. Kopp N., Jordan D., Michel J. P., Pialat J., Veisseire M., Chazot G., Tommasi M. Topographic and chemical study of the GABA synthetizing enzyme in Parkinsonian syndromes. Ann. Pathol. 3:1983;327-331.
51. Kubota Y., Inagaki S., Shimada S., Kito S., Wu J. Y. Glutamate decarboxylase-like immunoreactive neurons in the rat caudate putamen. Brain Res. Bull. 18:1987;687-697.
52. Laitinen L. V. Ventroposterolateral (VPL) pallidotomy. New Trends Clin. Neuropharmac. 8:1994;23.
53. Laitinen L. V., Bergenheim A. T., Hariz M. I. Leksell's posteroventral pallidotomy in the treatment of Parkinson's disease. J. Neurosurg. 76:1992;53-61.
54. Le Moine C., Tison F., Bloch B. D2 dopamine receptor gene expression by cholinergic neurons in the rat striatum. Neurosci. Lett. 117:1990;248-252.
55. Levy R., Herrero M. -T., Ruberg M., Villares J., Faucheux B., Guridi J., Guillen J., Luquin M. R., Javoy-Agid F., Obeso J. A., Agid Y., Hirsch E. C. Effects of nigrostriatal denervation and L-DOPA therapy on the GABAergic neurons of the striatum in MPTP-treated monkeys and Parkinson's disease: an in situ hybridization study of GAD67 mRNA. Eur. J. Neurosci. 7:1995;1199-1209.
56. Lewis M. E., Wade T. R., Krause R. D. Quantitation and digital representation of in situ hybridization histochemistry. Meth. Enzym. 168:1989;808-821.
57. Limousin P., Pollak P., Huot J. C., Benazzouz A., Perret J. E. F., Benabid A. L. Improvement in Parkinson's disease by chronic subthalamic nucleus stimulation: 3 month follow up. Movement Disord. 9:1994;112.
58. Lindefors N., Brene S., Herrera Marschitz M., Persson H. Regulation of neuropeptide Y gene expression in rat brain. Ann. N. Y. Acad. Sci. 611:1990;175-185.
59. Lloyd K. G., Mohler H., Heits P., Hornykiewicz O.et al. Distribution of choline acetyltransferase and glutamate decarboxylase within the substantia nigra and in other brain regions from control and parkinsonian patients. J. Neurochem. 25:1975;789-795.
60. Maneuf Y. P., Mitchell I. J., Crossman A. R., Brotchie J. M. On the role of enkephalin co-transmission in the GABAergic striatal efferents to the globus pallidus. Expl Neurol. 125:1994;65-71.
61. Maniatis T., Fritsch E. F. and Sambrook J. (1982) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor.
62. McGeer P. L., McGeer E. G. Enzymes associated with the metabolism of catecholamines, acetyl choline and GABA in human controls and patients with Parkinson's disease and Huntington's chorea. J. Neurochem. 26:1976;65-76.
63. McLaughlin B. J., Wood J. G., Saito K., Barber R., Vaughn J. E., Roberts E., Wu J. -Y. The fine structural localisation of glutamate decarboxylase in synaptic terminals of rodent cerebellum. Brain Res. 76:1974;377-391.
64. Mercugliano M., Soghomonian J. -J., Qin Y., Nguyen H. Q., Feldblum S., Erlander M. G., Tobin A. J., Chesselet M. -F. Comparative distribution of messenger RNAs encoding glutamic acid decarboxylases (Mr 65,000 and Mr 67,000) in the basal ganglia of the rat. J. comp. Neurol. 318:1992;245-254.
65. Mesulam M. M., Mufson E. J., Levey A. I., Wainer B. H. Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience. 12:1984;669-686.
66. Monfort J. C., Javoy-Agid F., Hauw J. J., Dubois B., Agid Y. Brain glutamate decarboxylase in Parkinson's disease with particular reference to a premortem severity index. Brain. 108:1985;301-313.
67. Mugnaini E. and Oertel W. H. (1985) An atlas of the distribution of GABAergic neurons and terminals in the CNS as revealed by GAD immunohistochemistry. In Handbook of Neuroanatomy, Vol 4, Part 1 (eds Bjorklund A. and Hokfelt T.) pp. 436-608. Elsevier, Amsterdam.
68. Najlerahim A., Harrison P. J., Barton A. J. L., Heffernan J., Pearson R. C. A. Distribution of messenger RNAs encoding the enzymes glutaminase, aspartate aminotransferase and glutamic acid decarboxylase in rat brain. Molec. Brain Res. 7:1990;317-333.
69. Nauta H. J., Cuenod M. Perikaryal cell labeling in the subthalamic nucleus following the injection of 3H-gamma-aminobutyric acid into the pallidal complex: an autoradiographic study in cat. Neuroscience. 7:1982;2725-2734.
70. Nisbet A. P., Foster O. J. F., Kingsbury A., Eve D. J., Daniel S. E., Marsden C. D., Lees A. J. Pre-proenkephalin and pre-protachykinin mRNA expression in normal human basal ganglia and in Parkinson's disease. Neuroscience. 66:1995;361-376.
71. Nisbet A. P., Foster O. J. F., Kingsbury A., Lees A. J., Marsden C. D. Nitric oxide synthase mRNA expression in human subthalamic nucleus, striatum and globus pallidus: implications for basal ganglia function. Molec. Brain Res. 22:1994;329-332.
72. Nisbet A. P., Foster O. J. F., Kingsbury A., Marsden C. D., Lees A. J. Nitric oxide synthase mRNA expression in parkinsonian basal ganglia: A quantitative in situ hybridization study. Movement Disord. 9:1994;103.
73. Nisenbaum L. K., Kitai S. T., Crowley W. R., Gerfen C. R. Temporal dissociation between changes in striatal enkephalin and substance P messenger RNAs following striatal dopamine depletion. Neuroscience. 60:1994;927-937.
74. Oertel W. H., Mugnaini E. Immunocytochemical studies of GABAergic neurons in rat basal ganglia and their relations to other neuronal systems. Neurosci. Lett. 47:1984;233-238.
75. Oertel W. H., Nitsch C., Mugnaini E. Immunocytochemical demonstration of the GABA-ergic neurons in rat globus pallidus and nucleus entopeduncularis and their GABA-ergic innervation. Adv. Neurol. 40:1984;91-98.
76. Oertel W. H., Tappaz M. L., Berod A., Mugnaini E. Two-color immunohistochemistry for dopamine and GABA neurons in rat substantia nigra and zona incerta. Brain Res. Bull. 9:1982;463-474.
77. Parent A., Hazrati L.-N. and Smith Y. (1989) The subthalamic nucleus in primates. A neuroanatomical and immunohistochemical study. In Neural Mechanisms in Disorders of Movement (eds Crossman A. R. and Sambrook M. A.) pp. 29-35. John Libbey, London, Paris.
78. Pasik P., Pasik T., Holstein G. R., Hamori J. GABAergic elements in the neuronal circuits of the monkey neostriatum: a light and electron microscopic immunocytochemical study. J. comp. Neurol. 270:1988;157-170.
79. Pedneault S., Soghomonian J. -J. Glutamate decarboxylase (GAD65) mRNA levels in the striatum and pallidum of MPTP-treated monkeys. Molec. Brain Res. 25:1994;351-354.
80. Penny G. R., Afsharpour S., Kitai S. T. The glutamate decarboxylase-, leucine enkephalin-, methionine enkephalin- and substance P-immunoreactive neurons in the neostriatum of the rat and cat: evidence for a partial population overlap. Neuroscience. 17:1986;1011-1045.
81. Perret C. W., Marchbanks R. M., Whately S. A. Characterization of messenger RNA extracted post-mortem from the brains of schizophrenic, depressed and control subjects. J. Neurol. Neurosurg. Psychiat. 51:1988;325-331.
82. Perry T. L., Javoy-Agid F., Agid Y., Fibiger H. C. Striatal GABAergic neuronal activity is not reduced in Parkinson's disease. J. Neurochem. 40:1983;1120-1123.
83. Porrino L. J., Burns R. S., Crane A. M., Palombo E., Kopin I. J., Sokoloff L. Changes in local cerebral glucose utilization associated with Parkinson's syndrome induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in the primate. Life Sci. 40:1987;1657-1664.
84. Robertson G. S., Hubert G. W., Tham C. S., Fibiger H. C. Lesions of the mesotelencephalic dopamine system enhance the effects of selective dopamine D1 and D2 receptor agonists on striatal acetylcholine release. Eur. J. Pharmac. 219:1992;323-325.
85. Robertson R. G., Clarke C. A., Boyce S., Sambrook M. A., Crossman A. R. The role of striatopallidal neurones utilizing gamma-aminobutyric acid in the pathophysiology of MPTP-induced parkinsonism in the primate: evidence from [3H]flunitrazepam autoradiography. Brain Res. 531:1990;95-104.
86. Robertson R. G., Graham W. C., Sambrook M. A., Crossman A. R. Further investigations into the pathophysiology of MPTP-induced parkinsonism in the primate: an intracerebral microdialysis study of gamma-aminobutyric acid in the lateral segment of the globus pallidus. Brain Res. 563:1991;278-280.
87. Rouzaire Dubois B., Scarnati E., Hammond C., Crossman A. R., Shibazaki T. Microiontophoretic studies on the nature of the neurotransmitter in the subthalamo-entopeduncular pathway of the rat. Brain Res. 271:1983;11-20.
88. Ruberg M., Ploska A., Javoy-Agid F., Agid Y. Muscarinic binding and choline acetyltransferase activity in Parkinsonian subjects with reference to dementia. Brain Res. 232:1982;129-139.
89. Salin P., Mercugliano M., Chesselet M. -F. Differential effects of chronic treatment with haloperidol and clozapine on the level of preprosomatostatin mRNA in the striatum, nucleus accumbens, and frontal cortex of the rat. Cell molec. Neurobiol. 10:1990;127-144.
90. Sambrook M. A., Crossman A. R., Mitchell I., Robertson R. G., Clarke C. E. and Boyce S. (1989) Basal ganglia mechanisms mediating primate models of movement disorders. In Neural Mechanisms in Disorders of Movement (eds Crossman A. R. and Sambrook M. A.) pp. 123-143. John Libbey and Co Ltd, London.
91. Samuel D., Kumar U., Nieoullon A. Gamma-aminobutyric acid function in the rat striatum is under the double influence of nigrostriatal dopaminergic and thalamostriatal inputs: two modes of regulation? J. Neurochem. 51:1988;1704-1710.
92. Sandyk R., Snider S. R. Naloxone treatment of L-DOPA-induced dyskinesias in Parkinson's disease. Am. J. Psychiat. 143:1986;118.
93. Schwyn R. C., Fox C. A. The primate substantia nigra: a Golgi and electron microscope study. J. Hirnforsch. 15:1974;95-126.
94. Segovia J., Tillakaratne N. J., Whelan K., Tobin A. J., Gale K. Parallel increases in striatal glutamic acid decarboxylase activity and mRNA levels in rats with lesions of the nigrostriatal pathway. Brain Res. 529:1990;345-348.
95. Sellal F., Hirsch E., Lisovoski F., Mutschler V., Collard M., Marescaux C. Contralateral disappearance of parkinsonian signs after subthalamic hematoma. Neurology. 42:1992;255-256.
96. Smith Y., Parent A., Seguela A., Descarries L. Distribution of GABA-immunoreactive neurons in the basal ganglia of the squirrel monkey (Saimiri sciureus). J. comp. Neurol. 259:1987;50-64.
97. Soghomonian J. -J., Chesselet M. -F. Effects of nigrostriatal lesions on the levels of messenger RNAs encoding two isoforms of glutamate decarboxylase in the globus pallidus and entopeduncular nucleus of the rat. Synapse. 11:1992;124-133.
98. Soghomonian J. -J., Gonzales C., Chesselet M. -F. Messenger RNAs encoding glutamate-decarboxylases are differentially affected by nigrostriatal lesions in subpopulations of striatal neurons. Brain Res. 576:1992;68-79.
99. Soghomonian J. -J., Pedneault S., Audet G., Parent A. Increased glutamate decarboxylase mRNA levels in the striatum and pallidum of MPTP-treated primates. J. Neurosci. 14:1994;6256-6265.
100. Tanaka Y., Niijima K., Mizuno Y., Yoshida M. Changes in gamma-aminobutyrate, glutamate, aspartate, glycine, and taurine contents in the striatum after unilateral nigrostriatal lesions in rats. Expl Neurol. 91:1986;259-268.
101. Taylor M. D., de Ceballos M. L., Rose S., Jenner P., Marsden C. D. Effects of a unilateral 6-hydroxydopamine lesion and prolonged L-3,4-dihydroxyphenylalanine treatment on peptidergic systems in rat basal ganglia. Eur. J. Pharmac. 219:1992;183-192.
102. Trabucchi M., Bassi S., Fratolla L. Effect of naloxone on the "on-off" syndrome in patients receiving long-term levodopa therapy. Archs Neurol. 39:1982;120-121.
103. Vernier P., Julien J. F., Rataboul P., Fourrier O., Feuerstein C., Mallet J. Similar time course changes in striatal levels of glutamic acid decarboxylase and proenkephalin mRNA following dopaminergic deafferentation in the rat. J. Neurochem. 51:1988;1375-1380.
104. Vincent S. R., Johansson O. Striatal neurons containing both somatostatin- and avian pancreatic polypeptide (APP)-like immunoreactivities and NADPH-diaphorase activity: a light and electron microscopic study. J. comp. Neurol. 217:1983;264-270.
105. Vitek J. L., Hashimoto T., Kaneoke Y., Baron M., Turner R., Bakay R. A. E., DeLong M. R. Improvement of parkinsonian motor signsduring electrical stimulation of the pallidum. Movement Disord. 9:1994;102.
106. Voneida T. J. An experimental study of the course and destination of fibres arising in the head of the caudate nucleus in the cat and monkey. J. comp. Neurol. 115:1960;75-87.
107. Voorn P., Roest G., Groenewegen H. J. Increase of enkephalin and decrease of substance P immunoreactivity in the dorsal and ventral striatum of the rat after midbrain 6-hydroxydopamine lesions. Brain Res. 412:1987;391-396.
108. Wang H. Y., Zhou L. W., Friedman E., Weiss B. Differential regulation of release of acetylcholine in the striatum in mice following continuous exposure to selective D1 and D2 dopaminergic agonists. Neuropharmacology. 32:1993;85-91.
109. Waters C. M., Peck R., Rossor M., Reynolds G. P., Hunt S. P. Immunocytochemical studies on the basal ganglia and substantia nigra in Parkinson's disease and Huntington's chorea. Neuroscience. 25:1988;419-438.
110. Wood T. L., Frantz G. D., Menkes J. H., Tobin A. J. Regional distribution of messenger RNAs in postmortem human brain. J. Neurosci. Res. 16:1986;311-324.
111. Young W. S., Bonner T. I., Brann M. R. Mesencephalic dopamine neurons regulate the expression of neuropeptide mRNAs in the rat forebrain. Proc. natn. Acad. Sci. U.S.A. 83:1986;9827-9831.