Subthalamic nucleus-mediated excitotoxicity in Parkinson's disease: A target for neuroprotection

Annals of Neurology

Volumn 44, Issue 3 SUPPL. 1, 1998, Pages

  Rodriguez, M C ^a   Obeso, J A ^a,c   Olanow, C Warren ^b  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c Grupo Hospiten   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CONFERENCE PAPER; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; HUMAN; HYPOTHESIS; NEUROPROTECTION; NEUROTOXICITY; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA; SUBTHALAMIC NUCLEUS;

EID: 0031696407     PISSN: 03645134     EISSN: None     Source Type: Journal    
DOI: 10.1002/ana.410440726     Document Type: Conference Paper

References (144)

1. Feger J, Hassani LN, Mouroux M. The subthalamic nucleus and its connections: new electrophysiological and pharmacological data. Adv Neurol 1997;74:31-44
2. DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurol Sci 1990;13:281-285
3. Rinvik E, Ottersen OP. Terminals of subthalamonigral fibres are enriched with glutamate-like immunoreactivity: an electron microscopic, immunogold analysis in the cat. Neuroanatomy 1993;6:19-30
4. Scarnati E, Florio T. The pedunculopontine nucleus and related structures: functional organization. Adv Neurol 1997;74: 97-110
5. Rouzaire-Dubois B, Scarnati E. Pharmacological study of the cortical-induced excitation of subthalamic nucleus neurons in the rat: evidence for ammoacids as putative neurotransmitters. Neuroscience 1987;21:429-440
6. Sugimoto T, Hattori T. Confirmation of thalamosubthalamic projections by electron microscopic autoradiography. Brain Res 1983;264:335-339
7. Bevan MD, Bolam JP. Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J Neurosci 1995;15: 7105-7120
8. Lavoie B, Smith Y, Parent A. Dopaminergic innervation of the basal ganglia in the squirrel monkey as revealed by tyrosine hydroxylase immunohisrochemistry. J Comp Neurol 1994; 344:210-231
9. Blandini F, Greenamyre JT. Effect of subthalamic nucleus lesion on mitochondrial enzyme activity in rat basal ganglia. Brain Res 1995;669:59-66
10. Blandini F, Greenamyre JT. The effect of subthalamic nucleus lesion on mitochondrial enzyme activity in rat basal ganglia. Brain Res 1995;588:307-310
11. Blandini F, Porter RHP, Greenamyre JT. Autoradiographic study of mitochondrial complex I and glutamate receptors in the basal ganglia of rats after unilateral subthalamic lesion. Neurosci Lett 1995;186:99-102
12. Delfs JM, Ciaramitaro VM, Parry TJ, Chesselet MF. Subthalamic nucleus lesions: widespread effects on changes in gene expression induced by nigrostriatal dopamine depletion in rats. J Neurosci 1995;15:6562-6575
13. Guridi J, Herrero MT, Luquin MR, et al. Subthalamotomy in parkinsonian monkeys. Behavioral and biochemical analysis. Brain 1996;119:1717-1727
14. Mitchell IJ, Sambrook MA, Crossman AR. Subcortical changes in the regional uptake of [3H]-2-deoxyglucose in the brain of the monkey during experimental choreiform dyskinesia elicited by injection of a gamma-aminobutyric acid antagonist into the subthalamic nucleus. Brain 1985;108:405-422
15. Blandini F, Garcia-Osuna M, Greenamyre JT. Subthalamic ablation reverses changes in basal ganglia oxidative metabolism and motor response to apomorphine induced by nigrostriatal lesion in rats. Eur J Neurosci 1997;9:1407-1413
16. Hammond C, Deniau JM, Rizk A, Féger J. Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat. Brain Res 1978;151:235-244
17. Kita H, Kitai ST. Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res 1991;564:296-305
18. Feger J, Robledo P. The effects of activation or inhibition of the subthalamic nucleus on the metabolic and electrophysiological activities within the pallidal complex and substantia nigra in the rat. Eur J Neurosci 1991;3:947-952
19. Robledo P, Féger J. Excitatory influence of rat subthalamic nucleus to substantia nigra pars reticulata and the pallidal complex: electrophysiological data. Brain Res 1990;518:47-54
20. Ryan LJ, Sanders DJ. Subthalamic nucleus lesion regularizes firing patterns in globus pallidus and substantia nigra pars reticulata neurons in rats. Brain Res 1993;626:327-331
21. Hamada I, DeLong MR. Excitotoxic acid lesions of the primate subthalamic nucleus result in reduced pallidal neuronal activity during active holding. J Neurophysiol 1992;68:1859-1866
22. Nicoletti F, Bruno V, Casabona G, Knöpfel T. Metabotropic glutamate receptors: a new target for the therapy of neurode-generative disorders? Trends Neurol Sci 1996;19:267-271
23. Hollmann M, Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci 1994;17:31-108
24. Standaert DG, Testa CM, Young AB, Penney JB. Organization of N-methyl-D-aspartate glutamate receptor gene expression in the basal ganglia of the rat. J Comp Neurol 1994;343: 1-16
25. Choi DW. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1998;1:623-634
26. Meldrum B, Garthwaite J. Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Physiol Sci 1990;11: 379-387
27. Bergman H, Wichmann T, DeLong MR. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 1994;72:507-520
28. Smith Y, Charara A, Parent A. Synaptic innervation of midbrain dopaminergic neurons by glutamate-enriched terminals in the squirrel monkey. J Comp Neurol 1996;364:231-253
29. Charara A, Smith Y, Parent A. Glutamatergic inputs from the pedunculopontine nucleus to midbrain dopaminergic neurons in primates: Phaseolus vulgaris-leucoagglutinin anterograde labeling combined with postembedding glutamate and GABA immunohistochemistry. J Comp Neurol 1996;364:254-266
30. Scarnati E, Proia A, Campana E, Pacitti C. A microiontophoretic study on the nature of the putative synaptic neurotransmitter in the pedunculopontine-subthalamic nigra pars compacta excitatory pathway of the rat. Exp Brain Res 1986; 62:470-478
31. Lavoie B, Parent A. Pedunculopontine nucleus in the squirrel monkey: cholinergic and glutamatergic projection to the substantia nigra. J Comp Neurol 1994;344:232-241
32. Naito A, Kita H. The cortico-nigral projection in the rat: an anterograde tracing study with biotinylated dextran amine. Brain Res 1994;637:317-322
33. Gonzales C, Chesselet MF. Amygdalonigral pathway: an anterograde study in the rat with Phaseolus vulgarisleucoagglutinin (PHA-L). J Comp Neurol 1990;297:182-200
34. Chergui K, Charlety PJ, Akaoka H, et al. Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. Eur J Neurosci 1993;5: 137-144
35. Tong ZY, Overton PG, Clark D. Antagonism of NMDA receptors but not AMPA/kainate receptors blocks bursting in dopaminergic neurons induced by electrical stimulation of the prefrontal cortex. J Neural Transm 1996;103:889-904
36. Di Loreto S, Florio T, Scarnati E. Evidence that non-NMDA receptors are involved in the excitatory pathway from the pedunculopontine region to nigrostriatal dopaminergic neurons. Exp Brain Res 1992;89:79-86
37. Smith Y, Hazrati LN, Parent A. Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method. J Comp Neurol 1990; 294:306-323
38. Carpenter MB, Carleton SC, Keller JT, Conte P. Connections of the subthalamic nucleus in the monkey. Brain Res 1981; 224:1-29
39. Parent A, Smith Y. Organization of efferent projections of the subthalamic nucleus in the squirrel monkey as revealed by retrograde labeling methods. Brain Res 1987;436:296-310
40. Parent A, Hazrati LN. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Rev 1995;20:128-154
41. Paquet M, Tremblay M, Soghomonian JJ, Sminth Y. AMPA and NMDA glutamate receptor subunits in midbain dopaminergic neurons in the squirrel monkey: an immunohistochemical and in situ hybridization study. J Neurosci 1997;17:1377-1396
42. Gariano RF, Groves PM. Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortex. Brain Res 1988;462:194-198
43. Tong ZY, Overton PG, Clark D. Stimulation of the prefrontal cortex on the rat induces patterns of activity in midbrain dopaminergic neurons which resemble natural burst events. Synapse 1996;22:195-208
44. Hornykiewicz O. Dopamine (3-hydroxytyramine) and brain function. Pharmacol Rev 1966;18:925-964
45. Brown LL, Makman MH, Wolfson LI, Dvorkin B, Warner C, Katzman R. A direct role of dopamine in the rat subthalamic nucleus and an adjacent intrapeduncular area. Science 1979; 206:1416-1418
46. Canteras NS, Shammah-Lagnado SJ, Silva BA, Ricardo JA. Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res 1990;513:43-59
47. Hassani OK, François CH, Yelnik J, Féger J. Evidence for a dopaminergic innervation of the subthalamic nucleus in the rat. Brain Res 1997;749:88-94
48. Aller KA, Juncos JL, Rye DB. Anatomical investigation of the dopaminergic innervation of the rat subthalamic nucleus [abstract]. Soc Neurosci Abst 1997;23:197
49. Martres MP, Bouthenet ML, Sales N, Sokoloff P, Schwartz JC. Widespread distribution of brain dopamine receptors evidenced with [(125)I]iodosulpride, a highly selective ligand. Science 1985;228:752-755
50. Yokoyama C, Okamura H, Nakajima T, Taguchi JI, Ibata Y. Autoradiographic distribution of 3HYM901512, a high-affinity and selective antagonist ligand for the dopamine D2 receptor group, in the rat brain and spinal cord. J Comp Neurol 1994;344:121-136
51. Dawson TM, Barone P, Sidhu A, Wamsley JK, Chase TN. The D1 dopamine receptor in the rat brain: quantitative autoradiographic localization using an iodinated ligand. Neuroscience 1988;26:83-100
52. Chergui K, Akaoka H, Charléty PJ, Saunier CF, Buda M, Chouvet G. Subthalamic nucleus modulates burst firing of nigral dopamine neurones via NMDA receptors. Neurophysiology, basic and clinical. Neuroreport 1994;5:1185-1188
53. Chergui K, Charlety PJ, Akaoka H, et al. Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. Eur J Neurosci 1993;5: 137-144
54. Fetz EE. Temporal coding in neural populations? Science 1997;278:1901-1902
55. Gonon FG. Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 1988;24: 9-28
56. Hammond C, Deniau JM, Rizk A, Féger J. Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat. Brain Res 1978;151:235-244
57. Mintz I, Hammond C, Guibert B, Leviel V. Stimulation of the subthalamic nucleus enhances the release of dopamine in the rat substantia nigra. Brain Res 1986;376:406-408
58. Smith ID, Grace AA. Role of the subthalamic nucleus in the regulation of nigral dopamine neuron activity. Synapse 1992; 12:287-303
59. Charlety PJ, Grenhoff J, Chergui K, et al. Burst firing of mesencephalic dopamine neurons is inhibited by somatodendritic application of kynurenate. Acta Physiol Scand 1991;142:105-112
60. Overton P, Clark D. Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat. Synapse 1992;10:131-140
61. Afsharpour S. Topographical projections of the cerebral cortex to the subthalamic nucleus. J Comp Neurol 1985;236:14-28
62. Wichmann T, Bergman H, DeLong MR. The primate subthalamic nucleus. I. Functional properties in intact animals. J Neurophysiol 1994;72:494-506
63. Rodriguez MC, Gorospe A, Mozo A, et al. Characteristics of neuronal activity in the subthalamic nucleus and substantia nigra pars reticulata in Parkinson's disease [abstract]. Soc Neurosci Abst 1997;23:471
64. Kitai ST, Deniau JM. Cortical inputs to the subthalamus: intracellular analysis. Brain Res 1981;214:411-415
65. Tong ZY, Overton PG, Clark D. Antagonism of NMDA receptors but not AMPA/kainate receptors blocks bursting in dopaminergic neurons induced by electrical stimulation of the prefrontal cortex. J Neural Transm 1996;103:889-904
66. Fujimoto K, Kita H. Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res 1993;609:185-192
67. Ryan LJ, Clark KB. Alteration of neuronal responses in the subthalamic nucleus following globus pallidus and neostriatal lesions in rats. Brain Res Bull 1992;29:319-327
68. Albin RL, Aldridge JW, Young AB, Gilman S. Feline subthalamic nucleus neurons contain glutamate-like but not GABA-like or glycine-like immunoreactivity. Brain Res 1989;491: 185-188
69. Brown LL, Wolfson LI. Apomorphine increases glucose utilization on the substantia nigra, subthalamic nucleus and corpus striatum. Brain Res 1978;140:188-193
70. Mintz I, Hammond C, Féger J. Excitatory effect of iontophoretically applied dopamine on identified neurons of the rat subthalamic nucleus. Brain Res 1986;375:172-175
71. Kreiss DS, Walters JR. Dopamine D 2 receptor tone plays a critical role in dopamine D 1 receptor mediated excitatory effects on subthalamic nucleus neurons [abstract]. Soc Neurosci Abst 1997;23:746
72. Kreiss DS, Anderson LA, Walters JR. Apomorphine and dopamine D1 receptor agonists increase the firing rates of subthalamic nucleus neurons. Neuroscience 1996;72:863-876
73. Kreiss DS, Mastropietro WC, Rawji SS, Walters JR. The response of subthalamic nucleus to dopamine receptor stimulation in a rodent model of Parkinson's disease. J Neurosci 1997;17:6807-6819
74. Mitchell IJ, Clarke CE, Boyce S, et al. Neural mechanisms underlying parkinsonian symptoms based upon regional uptake of 2-deoxyglucose in monkeys exposed to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neuroscience 1989;32: 213-226
75. Obeso JA, Rodriguez MC, DeLong MR. Basal ganglia pathophysiology: a critical review. Adv Neurol 1997;74:3-18
76. Herrero MT, Levy R, Ruberg M, et al. Consequence of nigrostriatal denervation and L-dopa therapy on the expression of glutamic acid decarboxylase messenger RNA in the pallidum. Neurology 1996;47:219-224
77. Vila M, Herrero MT, Levy R, et al. Consequences of nigrostriatal denervation on the gamma-aminobutyric acidic neurons of substantia nigra pars reticulata and superior colliculus in parkinsonian syndromes. Neurology 1996;46:802-809
78. Vila M, Levy R, Herrero MT, et al. Consequence of nigrostriatal denervation on the functioning of basal ganglia in human and nonhuman primates: an in situ hybridization study of cytochrome oxidase subunit 1 mRNA. J Neurosci 1997;17: 765-773
79. Filion M, Tremblay L. Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 1991;547:142-151
80. Miller WL, DeLong MR. Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model of parkinsonism. In: Carpenter MB, Jayaraman A, eds. The basal ganglia II. New York: Plenum Press, 1987: 415-427
81. Wichmann T, Bergman H, DeLong MR. The primate subthalamic nucleus. III. Changes in motor behaviour and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J Neurophysiol 1994;71:521-526
82. Bergman H, Wichmann T, DeLong MR. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990;249:1436-1438
83. Aziz TZ, Peggs D, Sambrook MA, Crossman AR. Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1,2,3,6-tetrahydro-piridine (MPTP) induced parkinsonism in the primate. Mov Disord 1991;6:288-292
84. Brotchie JM, Mitchell IJ, Sambrook MA, Crossman AR. Alleviation of parkinsonism by antagonist of excitatory amino acid transmission in the medial segment of the globus pallidus in rat and primate. Mov Disord 1991;6:133-138
85. Limousin P, Pollak P, Benazzouz A, et al. Effect on parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 1995;345:91-95
86. Pollak P, Benabid AL, Limousine P, Benazzouz A. Chronic intracerebral stimulation in Parkinson's disease. Adv Neurol 1997;74:213-220
87. Obeso JA, Rodriguez MC, Gorospe A, et al. Surgical treatment of Parkinson's disease. In: Quinn N, ed. Parkinsonism. Clin Neurol 1997;6:125-146
88. Olanow CW, Germano IM, Brin MF, et al. Deep brain stimulation of the subthalamic nucleus for Parkinson's disease. Mov Disord 1996;11:598-599
89. Limousine P, Greene J, Pollak P, Rothwell J, Benabid AL, Frackowiak R. Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease. Ann Neurol 1997;42:283-291
90. Hassani OK, Mouroux M, Féger J. Increased subthalamic neuronal activity after nigral dopaminergic lesion independent of disinhibition via the globus pallidus. Neuroscience 1995;72: 105-115
91. Gerfen CR, Engber TR, Mahan LC, et al. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 1990;250:1429-1432
92. Michaels RL, Rothman SM. Glutamate neurotoxicity in vitro, antagonist pharmacology and intracellular calcium concentrations. J Neurosci 1990;10:283-292
93. Orrenius S, Burkitt MJ, Kass GE, et al. Calcium ions and oxidative cell injury. Ann Neurol 1992;32:33-42
94. Beckman JS, Beckman TW, Chen J, et al. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 1990;87:1620-1624
95. Dawson VL, Dawson TM, London ED, et al. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 1991;88:6368-6371
96. Dawson VL, Kizushi VM, Huang PL, et al. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J Neurosci 1996;16:2479-2487
97. Ayata C, Ayata G, Hara H, et al. Mechanisms of reduced striatal NMDA excitotoxicity in type I nitric oxide synthase knock-out mice. J Neurosci 1997;17:6908-6917
98. Nakao N, Frodl EV, Widner H, et al. Overexpressing Cu/Zn superoxide dismutase enhances survival of transplanted neurons in a rat model of Parkinson's disease. Nature 1995;1: 226-231
99. Ischiropoulos H, Zhu L, Chen J, et al. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch Biochem Biophys 1992;298:431-437
100. Zhang J, Dawson VL, Dawson TM, Snyder SH. Nitric oxide activation of poly (ADP-ribose) synthetase in neurotoxicity. Science 1994;263:687-689
101. Reif DW, Simmons RD. Nitric oxide mediates iron release from ferritin. Arch Biochem Biophys 1990;283:537-541
102. Olanow CW. A radical hypothesis for neurodegeneration. Trends Neurol Sci 1993;16:439-444
103. Schinder AF, Olson EC, Spitzer NC, Montal M. Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J Neurosci 1996;16:6125-6133
104. White RJ, Reynolds IJ. Mitochondrial depolarization in glutamate-stimulated neurons: an early signal to excitotoxin exposure. J Neurosci 1996;16:5688-5697
105. Tatton WG, Olanow CW. Apoptosis in neurodegeneration; role of mitochondria. Arch Biochem Biophys [in press]
106. Marchetti P, Castedo M, Susin SA, et al. Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 1996;184:1155-1160
107. Wadia JS, Chalmers-Redman ME, Ju WJH, et al. Mitochondrial membrane potential and nuclear changes in apoptosis caused by serum and nerve growth factor withdrawal: time course and modification by - (-) deprenyl. J Neurosci 1998; 18:932-947
108. ++ homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp Neurol 1993;121:1-13
109. Olanow CW, Tatton WG. Etiology and pathogenesis of Parkinson's disease. Annu Rev Neurosci [in press]
110. MacDonald JF, Nowak LM. Mechanisms of blockade of excitatory aminoacid receptor channels. Trends Pharmacol Sci 1990;11:167-171
111. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurons. Nature 1984;307:462-465
112. Beal MF. Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann Neurol 1992;31:119-130
113. Albin RL, Greenmayre JT. Alternative excitotoxic hypotheses. Neurology 1992;42:733-738
114. Novelli A, Reilly JA, Lysko PG, Henneberry RC. Glutamate becomes neurotoxic via the NMDA receptor when intracellular energy levels are reduced. Brain Res 1988;451:205-212
115. + neurotoxicity by N-methyl-D-aspartate antagonists. Nature 1991;349:414-418
116. Zuddas A, Oberto G, Vaglini F, et al. MK-801 prevents MPTP-induced parkinsonism in primates. J Neurochem 1992; 59:133-739
117. Lange KW, Löschmann PA, Sofic E, et al. The competitive NMDA antagonist CPP protects substantia nigra from MPTP-induced degeneration in primates. Arch Pharmacol 1993;348:586-592
118. Sonsalla PK, Zeevalk GD, Manzino L, et al. MK-801 fails to protect against the dopaminergic neuropathology produced by systemic 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mice or intranigral 1-methyl-4-phenylpyridinium in rats. J Neurochem 1992;58:1979-1982
119. Kupsch A, Loschmann PA, Sauer H. Do NMDA receptor antagonists protect against MPTP-toxicity? Biochemical and immunocytochemical analyses in black mice. Brain Res 1992; 592:74-83
120. + elimination in the mouse striatum. J Pharmacol Exp Ther 1993;267:1515-1520
121. Brouillet E, Beal MF. NMDA antagonists partially protect against MPTP neurotoxicity in mice. Neuroreport 1993;4: 387-390
122. Jones-Humble SA, Morgan PF, Cooper BR. The novel anti-convulsant lamotrigine prevents dopamine depletion in C57 black mice in the MPTP animal model of Parkinson's disease. Life Sci 1994;54:245-252
123. Barneoud P, Mazadier M, Miquet J-M, et al. Neuroprotective effects of riluzole on a model of Parkinson's disease in the rat. Neuroscience 1996;74:971-983
124. Boireau A, Dubedat P, Bordier F, et al. Riluzole and experimental parkinsonism: antagonism of MPTP-induced decrease in central dopamine levels in mice. Neuroreport 1994;5:2657-2660
125. Przedborski S. Role of nitric oxide in MPTP-induced dopaminergic neurotoxicity. Proc Natl Acad Sci USA 1996;93: 4565-4571
126. Shultz JB, Matthews JB, Muqit MMK, et al. Inhibition of neuronal nitric oxide synthase by 7-nitroindazole protects against MPTP-induced neurotoxicity in mice. J Neurochem 1995;64:936-939
127. Di Monte D, Royland JE, Anderson A, et al. Inhibition of monoamine oxidase contributes to the protective effect of 7-nitroindazole against MPTP neurotoxicity. J Neurochem 1997;69:1771-1773
128. + induced substantia nigra degeneration is attenuated in nNOS knockout mice. Neurobiol Dis 1997;4:114-121
129. Marey-Semper I, Gelman M, Lévi-Strauss M. A selective toxicity toward cultured mesencephalic dopaminergic neurons is induced by the synergistic effects of energetic metabolism impairment and NMDA receptor activation. J Neurosci 1995; 15:5912-5918
130. Schapira AHV, Cooper JM, Dexter D, et al. Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem 1990;54:823-827
131. Mizuno Y, Ohta S, Tanaka M, et al. Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease. Biochem Biophys Res Commun 1989;163:1450-1455
132. Piallat B, Benazzouz A, Benabid AL. Subthalamic nucleus lesion on rats prevents dopaminergic nigral neuron degeneration after striatal 6-OHDA injection: behavioural and immunohistochemical studies. Eur J Neurosci 1996;8:1408-1414
133. Saji M, Blau AD, Volpe BT. Prevention of transneuronal degeneration of neurons in the substantia nigra reticulata by ablation of the subthalamic nucleus. Exp Neurol 1996;141:120-129
134. Mufson EJ, Brandabur MM. Sparing of NADPH-diaphorase striatal neurons in Parkinson's and Alzheimer's diseases. Neuroreport 1994;5:705-708
135. Good PF, Hsu A, Werner P, et al. Protein nitration in Parkinson's disease. J Neuropathol Exp Neurol [in press]
136. Brooks DJ. The early diagnosis of Parkinson's disease. Ann Neurol 1998;44(Suppl 1):S10-S18 (this issue)
137. Olanow CW. A rationale for dopamine agonists as primary therapy for Parkinson's disease. Can J Neurosci 1992;19:108-112
138. Obeso JA, Grandas F, Vaamonde J, et al. Motor complications associated with chronic levodopa therapy in Parkinson's disease. Neurology 1993;43(Suppl 2):1459-1464
139. Obeso JA, Grandas F, Herrero MT, Horowsdi R. The role of pulsatile versus continuous dopamine receptor stimulation for functional recovery in Parkinson's disease. Eur J Neurosci 1994;6:889-897
140. Olanow CW. A rationale for using dopamine agonists as primary symptomatic therapy in Parkinson's disease. In: Olanow CW, Obeso JA, eds. Dopamine agonists in early Parkinson's disease. Royal Tunbridge Wells, UK: Wells Medical, 1997: 37-48
141. 3H]spiperone binding. Brain Res 1986;379:294-299
142. Montastruc JL, Rascol O, Senard JM, Rascol A. A randomized controlled study comparing bromocriptine to which levodopa was later added, with levodopa alone in previously untreated patients with Parkinson's disease: a five year follow up. J Neurol Neurosurg Psychiatry 1994;57:1034-1038
143. Olanow CW, Jenner P, Brooks D. Dopamine agonists and neuroprotection in Parkinson's disease. Ann Neurol 1998;44(Suppl 1):S167-S174 (this issue)
144. Olanow CW, Koller WC. An algorithm (decision tree) for the management of Parkinson's disease. Neurology 1998; 50(Suppl 3):S1-S57