High-Frequency Stimulation of the Subthalamic Nucleus Selectively Reverses Dopamine Denervation-Induced Cellular Defects in the Output Structures of the Basal Ganglia in the Rat

Journal of Neuroscience

Volumn 22, Issue 12, 2002, Pages 5137-5148

  Salin, Pascal ^a   Manrique, Christine ^a   Forni, Claude ^a   Kerkerian Le Goff, Lydia ^a  

^a CNRS   (France)

Author keywords

Deep brain stimulation; Glutamate decarboxylase; In situ hybridization; Pallidum; Parkinson's disease; Striatum; Substantia nigra; Subthalamic nucleus

Indexed keywords

CYTOCHROME C OXIDASE; ENKEPHALIN; GLUTAMATE DECARBOXYLASE; ISOPROTEIN; MESSENGER RNA; NEUROPEPTIDE; PROTEIN C FOS; PROTEIN SUBUNIT; SUBSTANCE P; DOPAMINE; GLUTAMATE DECARBOXYLASE 67; ISOENZYME; OXIDOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; CORPUS STRIATUM; DIATHERMY; DOPAMINERGIC ACTIVITY; ENTOPEDUNCULAR NUCLEUS; ENZYME ACTIVITY; ENZYME SUBSTRATE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GLOBUS PALLIDUS; HISTOCHEMISTRY; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; METABOLIC ACTIVATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; SUBSTANTIA NIGRA; SUBTHALAMIC NUCLEUS; ANIMAL; ANIMAL BEHAVIOR; BIOSYNTHESIS; CHEMISTRY; ELECTROSTIMULATION; GENETICS; HISTOLOGY; METABOLISM; PARKINSON DISEASE; WISTAR RAT;

ANIMALS; BASAL GANGLIA; BEHAVIOR, ANIMAL; CORPUS STRIATUM; DOPAMINE; ELECTRIC STIMULATION; ELECTRON TRANSPORT COMPLEX IV; ENKEPHALINS; ENTOPEDUNCULAR NUCLEUS; GLOBUS PALLIDUS; GLUTAMATE DECARBOXYLASE; ISOENZYMES; MALE; OXIDOPAMINE; PARKINSON DISEASE; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; RNA, MESSENGER; SUBSTANCE P; SUBSTANTIA NIGRA; SUBTHALAMIC NUCLEUS;

EID: 0037096324     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-12-05137.2002     Document Type: Article

References (53)

1. Alvarez L, Macias R, Guridi J, Lopez G, Alvarez E, Maragoto C, Teijeiro J, Torres A, Pavon N, Rodriguez-Oroz MC, Ochoa L, Hetherington H, Juncos J, DeLong MR, Obeso JA (2001) Dorsal subthalamotomy for Parkinson's disease. Mov Disord 16:72-78.
2. Aziz TZ, Peggs D, Sambrook MA, Crossman AR (1991) Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP)-induced parkinsonism in the primate. Mov Disord 6:288-292.
3. Benabid AL, Pollak P, Louveau A, Henry S, De Rougemont J (1987) Combined (thalamotomy and stimulation) stereotaxic surgery of the VIM thalamic nucleus for bilateral Parkinson's disease. Appl Neurophysiol 50:344-346.
4. Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, Perret J, De Rougemont J (1991) Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337:403-406.
5. Benabid AL, Krack PP, Benazzouz A, Limousin P, Koudsie A, Pollak P (2000) Deep brain stimulation of the subthalamic nucleus for Parkinson's disease: methodologic aspects and clinical criteria. Neurology 55:S40-44.
6. Benazzouz A, Gross C, Feger J, Boraud T, Bioulac B (1993) Reversal of rigidity and improvement in motor performance by subthalamic high-frequency stimulation in MPTP-treated monkeys. Eur J Neurosci 5:382-389.
7. Benazzouz A, Piallat B, Pollak P, Benabid AL (1995) Responses of substantia nigra pars reticulata and globus pallidus complex to high frequency stimulation of the subthalamic nucleus in rats: electrophysiological data. Neurosci Lett 189:77-80.
8. Benazzouz A, Gao DM, Ni ZG, Piallat B, Bouali-Benaouzzz R, Benabid AL (2000) Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat. Neuroscience 99:289-295.
9. Bergman H, Wichmann T, DeLong MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249:1436-1438.
10. Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II Neuronal activity in the MPTP model of parkinsonism J Neurophysiol 72:507-520.
11. Beurrier C, Bezard E, Bioulac B, Gross C (1997) Subthalamic stimulation elicits hemiballismus in normal monkey. NeuroReport 8:1625-1629.
12. Beurrier C, Bioulac B, Audin J, Hammond C (2001) High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J Neurophysiol 85:1351-1356.
13. Blandini F, Garcia-Osuna M, Greenamyre JT (1997) Subthalamic ablation reverses changes in basal ganglia oxidative metabolism and motor response to apomorphine induced by nigrostriatal lesion in rats. Eur J Neurosci 9:1407-1413.
14. Bruet N, Windels F, Bertrand A, Feuerstein C, Poupard A, Savasta M (2001) High frequency stimulation of the subthalamic nucleus increases the extracellular contents of striatal dopamine in normal and partially dopaminergic denervated rats. J Neuropathol Exp Neurol 60:15-24.
15. Burbaud P, Gross C, Benazzouz A, Coussemacq M, Bioulac B (1995) Reduction of apomorphine-induced rotational behaviour by subthalamic lesion in 6-OHDA lesioned rats is associated with a normalization of firing rate and discharge pattern of pars reticulata neurons. Exp Brain Res 105:48-58.
16. Delfs JM, Ciaramitaro VM, Parry TJ, Chesselet MF (1995) Subthalamic nucleus lesions: widespread effects on changes in gene expression induced by nigrostriatal dopamine depletion in rats. J Neurosci 15:6562-6575.
17. Gerfen CR, McGinty JF, Young WS 3rd (1991) Dopamine differentially regulates dynorphin, substance P, enkephalin expression in striatal neurons: in situ hybridization histochemical analysis. J Neurosci 11:1016-1031.
18. Grill WM, McIntyre CC (2001) Extracellular excitation of central neurons: implications for the mechanisms of deep brain stimulation. Thalamus and Related Systems 1:269-277.
19. Guridi J, Obeso JA (2001) The subthalamic nucleus, hemiballismus and Parkinson's disease: reappraisal of a neurosurgical dogma. Brain 124:5-19.
20. Guridi J, Herrero MT, Luquin MR, Guillen J, Ruberg M, Laguna J, Vila M, Javoy-Agid F, Agid Y, Hirsch E, Obeso JA (1996) Subthalamotomy in parkinsonian monkeys. Behavioral and biochemical analysis. Brain 119:1717-1727.
21. Hamada I, DeLong MR (1992) Excitotoxic acid lesions of the primate subthalamic nucleus result in transient dyskinesias of the contralateral limbs. J Neurophysiol 68:1850-1858.
22. Hajji MD, Salin P, Kerkerian-Le Goff L (1996) Chronic dizocilpine maleate (MK-801) treatment suppresses the effects of nigrostriatal dopamine deafferentation on enkephalin but not on substance P expression in the rat striatum. Eur J Neurosci 8:917-926.
23. Hassani OK, Mouroux M, Feger J (1996) Increased subthalamic neuronal activity after nigral dopaminergic lesion independent of disinhibition via the globus pallidus. Neuroscience 72:105-115.
24. Henderson JM, Annett LE, Ryan LJ, Chiang W, Hidaka S, Torres EM, Dunnett SB (1999) Subthalamic nucleus lesions induce deficits as well as benefits in the hemiparkinsonian rat. Eur J Neurosci 11:2749-2757.
25. Herrero MT, Levy R, Ruberg M, Luquin MR, Villares J, Guillen J, Faucheux B, Javoy-Agid F, Guridi J, Agid Y, Obeso JA, Hirsch EC (1996) Consequence of nigrostriatal denervation and L-dopa therapy on the expression of glutamic acid decarboxylase messenger RNA in the pallidum. Neurology 47:219-224.
26. Hirsch EC, Perier C, Orieux G, François C, Feger J, Yelnik J, Vila M, Levy R, Tolosa ES, Marin C, Herrero MT, Obeso JA, Agid Y (2000) Metabolic effects of nigrostriatal denervation in basal ganglia. Trends Neurosci 23:S78-S85.
27. Hollerman JR, Grace AA (1992) Subthalamic nucleus cell firing in the 6-OHDA treated rat: basal activity and response to haloperidol. Brain Res 590:291-299.
28. Hughes PE, Dragunow M (1995) Induction of immediate-early genes and the control of neurotransmitter-regulated gene-expression within the nervous system. Pharmacol Rev 47:133-178.
29. Kincaid AE, Albin RL, Newman SW, Penney JB, Young AB (1992) 6-hydroxydopamine lesions of the nigrostriatal pathway alter the expression of glutamate decarboxylase messenger RNA in the rat globus pallidus projection neurons. Neuroscience 51:705-718.
30. Kita H, Kitai ST (1987) Efferent projections of the subthalamic nucleus in the rat: Light and electron microscopic analysis with the PHA-L method. J Comp Neurol 260:435-452.
31. Krause M, Fogel W, Heck A, Hacke W, Bonsanto M, Trenkwalder C, Tronnier V (2001) Deep brain stimulation for the treatment of Parkinson's disease: subthalamic nucleus versus globus pallidus internus. J Neurol Neurosurg Psychiatry 70:464-470.
32. Kreiss DS, Mastropietro CW, Rawji SS, Walters JR (1997) The response of subthalamic nucleus neurons to dopamine receptor stimulation in a rodent model of Parkinson's disease, J Neurosci 17:6807-6819.
33. Lee MS, Marsden CD (1994) Movement disorders following lesions of the thalamus or subthalamic region. Mov Disord 9:493-507.
34. Liévens JC, Dutertre M, Forni C, Salin P, Kerkerian-Le Goff L (1997) Continuous administration of the glutamate uptake inhibitor L-transpyrrolidine-2, 4-dicarboxylate produces striatal lesion. Mol Brain Res 50:181-189.
35. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Broussolle E, Perret JE, Benabid AL (1995) Bilateral subthalamic nucleus stimulation for severe Parkinson's disease. Mov Disord 10:672-674.
36. Limousin P, Hoffmann D, Benazzouz A, Perret JE, Benabid AL (1996) Abnormal involuntary movements induced by subthalamic nucleus stimulation in parkinsonian patients. Mov Disord 1:231-235.
37. Miller WC, DeLong MR (1987) Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model of parkinsonism. In: The basal ganglia II (Carpenter MB, Jayaraman A, eds), pp 415-427, New York: Plenum.
38. Mouroux M, Hassani OK, Feger J (1995) Electrophysiological study of the excitatory parafascicular projection to the subthalamic nucleus and evidence for ipsi- and contralateral controls. Neuroscience 67:399-407.
39. Nieoullon A, Cheramy A, Glowinski J (1977) Interdependence of the nigrostriatal dopaminergic systems on the two sides of the brain in the cat. Science 198:416-418.
40. Ni Z, Bouali-Benaouzzz R, Gao D, Benabid AL, Benazzouz A (2000) Changes in the firing pattern of globus pallidus neurons after the degeneration of nigrostriatal pathway are mediated by the subthalamic nucleus in the rat. Eur J Neurosci 12:4338-4344.
41. Ni Z, Bouali-Benaouzzz R, Gao D, Benabid A, Benazzouz A (2001) Time-course of changes in firing rates and firing patterns of subthalamic nucleus neuronal activity after 6-OHDA-induced dopamine depletion in rats. Brain Res 899:142-147.
42. Paul G, Reum T, Meissner W, Marburger A, Sohr R, Morgenstern R, Kupsch A (2000) High frequency stimulation of the subthalamic nucleus influences striatal dopaminergic metabolism in the naive rat. NeuroReport 11:441-444.
43. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. New York: Academic.
44. Perier C, Agid Y, Hirsch EC, Feger J (2000) Ipsilateral and contralateral subthalamic activity after unilateral dopaminergic lesion. NeuroReport 11:3275-3278.
45. Pollak P, Benabid AL, Gross C, Gao DM, Laurent A, Benazzouz A, Hoffmann D, Gentil M, Perret J (1993) Effects of the stimulation of the subthalamic nucleus in Parkinson's disease. Rev Neurol (Paris) 149:175-176.
46. Robledo P, Feger J (1991) Acute monoaminergic depletion in the rat potentiates the excitatory effect of the subthalamic nucleus in the substantia nigra pars reticulata but not in the pallidal complex. J Neural Transm Gen Sect 86:115-126.
47. Salin P, Hajji MD, Kerkerian-Le Goff L (1996) Bilateral 6-hydroxy-dopamine-induced lesion of the nigrostriatal dopamine pathway reproduces the effects of unilateral lesion on substance P but not on enkephalin expression in rat basal ganglia. Eur J Neurosci 8:1746-1757.
48. Soghomonian JJ, Chesselet MF (1992) 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 11:124-133.
49. Vila M, Marin C, Ruberg M, Jimenez A, Raisman-Vozari R, Agid Y, Tolosa E, Hirsch E (1999) Systemic administration of NMDA and AMPA receptor antagonists reverses the neurochemical changes induced by nigrostriatal denervation in basal ganglia. J Neurochem 73:344-352.
50. Vila M, Perier C, Feger J, Yelnik J, Faucheux B, Ruberg M, Raisman-Vozari R, Agid Y, Hirsch EC (2000) Evolution of changes in neuronal activity in the subthalamic nucleus of rats with unilateral lesion of the substantia nigra assessed by metabolic and electrophysiological measurements. Eur J Neurosci 12:337-344.
51. Windels F, Bruet N, Poupard A, Urbain N, Chouvet G, Feuerstein C, Savasta M (2000) Effects of high frequency stimulation of subthalamic nucleus on extracellular glutamate and GABA in substantia nigra and globus pallidus in the normal rat. Eur J Neurosci 12:4141-4146.
52. Windels F, Bruet N, Poupard A, Feuerstein C, Bertrand A, Savasta M (2001) Evidence for a possible role of GABA in the therapeutical efficacy of high frequency stimulation of the subthalamic nucleus in Parkinson's disease: a microdialysis study in rats. Soc Neurosci Abstr 966.10.
53. Zhang WQ, Tilson HA, Nanry KP, Hudson PM, Hong JS, Stachowiak MK (1988) Increased dopamine release from striata of rats after unilateral nigrostriatal bundle damage. Brain Res 461:335-342.