High frequency stimulation of the subthalamic nucleus impacts adult neurogenesis in a rat model of Parkinson's disease

Neurobiology of Disease

Volumn 42, Issue 3, 2011, Pages 284-291

  Khaindrava, Vitaly ^a,b   Salin, Pascal ^a   Melon, Christophe ^a   Ugrumov, Michael ^b   Kerkerian Le Goff, Lydia ^a   Daszuta, Annie ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b P K ANOKHIN INSTITUTE OF NORMAL PHYSIOLOGY   (Russian Federation)

Author keywords

Adult neurogenesis; Deep brain stimulation; Hippocampus; Olfactory bulb; Parkinson; Subthalamic nucleus

Indexed keywords

BROXURIDINE; DOPAMINE; DOUBLECORTIN; KI 67 ANTIGEN; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DISEASE ASSOCIATION; DISEASE MODEL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MOOD DISORDER; MOTOR DYSFUNCTION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; OLFACTORY BULB; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SMELLING DISORDER; SUBTHALAMIC NUCLEUS; SUBVENTRICULAR ZONE; THALAMOCORTICAL TRACT;

ANALYSIS OF VARIANCE; ANIMALS; DEEP BRAIN STIMULATION; DISEASE MODELS, ANIMAL; DOPAMINE; ELECTRODES, IMPLANTED; IMMUNOHISTOCHEMISTRY; MALE; NEUROGENESIS; PARKINSON DISEASE; RATS; RATS, WISTAR; SUBTHALAMIC NUCLEUS;

EID: 79954629314     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.01.018     Document Type: Article

References (61)

1. Abrous D.N., Koehl M., Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 2005, 85:523-569.
2. Arias-Carrion O., Verdugo-Diaz L., Feria-Velasco A., Millan-Aldaco D., Gutierrez A., Hernandez-Cruz A., Drucker-Colin R. Neurogenesis in the subventricular zone following transcranial magnetic field stimulation and nigrostriatal lesions. J. Neurosci. Res. 2004, 78:16-28.
3. Bacci J.J., Absi H., Manrique C., Baunez C., Salin P., Kerkerian-Le Goff L. Differential effects of prolonged high frequency stimulation and of excitotoxic lesion of the subthalamic nucleus on dopamine denervation-induced cellular defects in the rat striatum and globus pallidus. Eur. J. Neurosci. 2004, 20:3331-3341.
4. Baker S.A., Baker K.A., Hagg T. Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. Eur. J. Neurosci. 2004, 20:575-579.
5. Banasr M., Hery M., Printemps R., Daszuta A. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 2004, 29:450-460.
6. Belzunegui S., Izal-Azcarate A., San Sebastian W., Garrido-Gil P., Vazquez-Claverie M., Lopez B., Marcilla I., Luquin M.R. Striatal carotid body graft promotes differentiation of neural progenitor cells into neurons in the olfactory bulb of adult hemiparkisonian rats. Brain Res. 2008, 1217:213-220.
7. Benabid A.L., Chabardes S., Mitrofanis J., Pollak P. Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease. Lancet Neurol. 2009, 8:67-81.
8. Borta A., Hoglinger G.U. Dopamine and adult neurogenesis. J. Neurochem. 2007, 100:587-595.
9. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 2003, 467:1-10.
10. Bruet N., Windels F., Bertrand A., Feuerstein C., Poupard A., Savasta M. 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. 2001, 60:15-24.
11. Bruet N., Windels F., Carcenac C., Feuerstein C., Bertrand A., Poupard A., Savasta M. Neurochemical mechanisms induced by high frequency stimulation of the subthalamic nucleus: increase of extracellular striatal glutamate and GABA in normal and hemiparkinsonian rats. J. Neuropathol. Exp. Neurol. 2003, 62:1228-1240.
12. Chaudhuri K.R., Schapira A.H. Non-motor symptoms of Parkinson's disease: dopaminergic pathophysiology and treatment. Lancet Neurol. 2009, 8:464-474.
13. Czeh B., Welt T., Fischer A.K., Erhardt A., Schmitt W., Muller M.B., Toschi N., Fuchs E., Keck M.E. Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol. Psychiatry 2002, 52:1057-1065.
14. Deierborg T., Soulet D., Roybon L., Hall V., Brundin P. Emerging restorative treatments for Parkinson's disease. Prog. Neurobiol. 2008, 85:407-432.
15. De Groot C. The rat forebrain in stereotaxic coordinate 1959, Verhandelingen der Koninklijke Nederlandse Akademic van Wetenschappen, Amsterdam.
16. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 2006, 59:1116-1127.
17. Gasbarri A., Verney C., Innocenzi R., Campana E., Pacitti C. Mesolimbic dopaminergic neurons innervating the hipppocampal formation in the rat: a combined retrograde tracing and immunohistochemical study. Brain Res. 1994, 668:71-79.
18. Garcia L., D'Alessandro G., Bioulac B., Hammond C. High-frequency stimulation in Parkinson's disease: more or less?. Trends Neurosci. 2005, 28:209-216.
19. Geraerts M., Krylyshkina O., Debyser Z., Baekelandt V. Concise review: therapeutic strategies for Parkinson disease based on the modulation of adult neurogenesis. Stem Cells 2007, 25:263-270.
20. Germano I.M., Gracies J.M., Weisz D.J., Tse W., Koller W.C., Olanow C.W. Unilateral stimulation of the subthalamic nucleus in Parkinson disease: a double-blind 12-month evaluation study. J. Neurosurg. 2004, 101:36-42.
21. Gradinaru V., Mogri M., Thompson K.R., Henderson J.M., Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science 2009, 324:354-359.
22. Gubellini P., Eusebio A., Oueslati A., Melon C., Kerkerian-Le Goff L., Salin P. Chronic high-frequency stimulation of the subthalamic nucleus and L-DOPA treatment in experimental parkinsonism: effects on motor behaviour and striatal glutamate transmission. Eur. J. Neurosci. 2006, 24:1802-1814.
23. Gubellini P., Salin P., Kerkerian-Le Goff L., Baunez C. Deep brain stimulation in neurological diseases and experimental models: from molecule to complex behavior. Prog. Neurobiol. 2009, 89:79-123.
24. Haehner A., Boesveldt S., Berendse H.W., Mackay-Sim A., Fleischmann J., Silburn P.A., Johnston A.N., Mellick G.D., Herting B., Reichmann H., Hummel T. Prevalence of smell loss in Parkinson's disease-a multicenter study. Parkinsonism Relat. Disord. 2009, 15:490-494.
25. Harnack D., Meissner W., Jira J.A., Winter C., Morgenstern R., Kupsch A. Placebo-controlled chronic high-frequency stimulation of the subthalamic nucleus preserves dopaminergic nigral neurons in a rat model of progressive Parkinsonism. Exp. Neurol. 2008, 210:257-260.
26. He X.J., Yamauchi H., Uetsuka K. Nakayama H Neurotoxicity of MPTP to migrating neuroblasts: studies in acute and subacute mouse models of Parkinson's disease. Neurotoxicology 2008, 29:413-420.
27. Henning J., Koczan D., Glass A., Karopka T., Pahnke J., Rolfs A., Benecke R., Gimsa U. Deep brain stimulation in a rat model modulates TH, CaMKIIa and Homer1 gene expression. Eur. J. Neurosci. 2007, 25:239-250.
28. Hoglinger G.U., Rizk P., Muriel M.P., Duyckaerts C., Oertel W.H., Caille I., Hirsch E.C. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 2004, 7:726-735.
29. Lacombe E., Khaindrava V., Melon C., Oueslati A., Kerkerian-Le Goff L., Salin P. Different functional basal ganglia subcircuits associated with anti-akinetic and dyskinesiogenic effects of antiparkinsonian therapies. Neurobiol. Dis. 2009, 36:116-125.
30. Lindefors N., Ungerstedt U. Bilateral regulation of glutamate tissue and extracellular levels in caudate-putamen by midbrain dopamine neurons. Neurosci. Lett. 1990, 115:248-252.
31. Liu B.F., Gao E.J., Zeng X.Z., Ji M., Cai Q., Lu Q., Yang H., Xu Q.Y. Proliferation of neural precursors in the subventricular zone after chemical lesions of the nigrostriatal pathway in rat brain. Brain Res. 2006, 1106:30-39.
32. Lohle M., Storch A., Reichmann H. Beyond tremor and rigidity: non-motor features of Parkinson's disease. J. Neural Transm. 2009, 116:1483-1492.
33. Madsen T.M., Treschow A., Bengzon J., Bolwig T.G., Lindvall O., Tingstrom A. Increased neurogenesis in a model of electroconvulsive therapy. Biol. Psychiatry 2000, 47:1043-1049.
34. McIntyre C.C., Savasta M., Kerkerian-Le Goff L., Vitek J.L. Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin. Neurophysiol. 2004, 115:1239-1248.
35. Meissner W., Harnack D., Reese R., Paul G., Reum T., Ansorge M., Kusserow H., Winter C., Morgenstern R., Kupsch A. High-frequency stimulation of the subthalamic nucleus enhances striatal dopamine release and metabolism in rats. J. Neurochem. 2003, 85:601-609.
36. Ming G.L., Song H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 2005, 28:223-250.
37. Oizumi H., Hayashita-Kinoh H., Hayakawa H., Arai H., Furuya T., Ren Y.R., Yasuda T., Seki T., Mizuno Y., Mochizuki H. Alteration in the differentiation-related molecular expression in the subventricular zone in a mouse model of Parkinson's disease. Neurosci. Res. 2008, 60:15-21.
38. Park J.H., Enikolopov G. Transient elevation of adult hippocampal neurogenesis after dopamine depletion. Exp. Neurol. 2010, 222:267-276.
39. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, New York.
40. Perera T.D., Coplan J.D., Lisanby S.H., Lipira C.M., Arif M., Carpio C., Spitzer G., Santarelli L., Scharf B., Hen R., Rosoklija G., Sackeim H.A., Dwork A.J. Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J. Neurosci. 2007, 27:4894-4901.
41. Perlmutter J.S., Mink J.W. Deep brain stimulation. Annu. Rev. Neurosci. 2006, 29:229-257.
42. Sahay A., Hen R. Adult hippocampal neurogenesis in depression. Nat. Neurosci. 2007, 10:1110-1115.
43. Scatton B., Simon H., Le Moal M., Bischoff S. Origin of dopaminergic innervation of the rat hippocampal formation. Neurosci. Lett. 1980, 18:125-131.
44. Scott B.W., Wojtowicz J.M., Burnham W.M. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp. Neurol. 2000, 165:231-236.
45. Soumier A., Banasr M., Kerkerian-Le-Goff L.K., Daszuta A. Region- and phase-dependent effects of 5-HT(1A) and 5-HT(2C) receptor activation on adult neurogenesis. Eur. Neuropsychopharmacol. 2010, 20:336-345.
46. Soumier A., Banasr M., Lortet S., Masmejean F., Bernard N., Kerkerian-Le-Goff L., Gabriel C., Millan M.J., Mocaer E., Daszuta A. Mechanisms contributing to the phase-dependent regulation of neurogenesis by the novel antidepressant, agomelatine, in the adult rat hippocampus. Neuropsychopharmacology 2009, 34:2390-2403.
47. Spieles-Engemann A.L., Behbehani M.M., Collier T.J., Wohlgenant S.L., Steece-Collier K., Paumier K., Daley B.F., Gombash S., Madhavan L., Mandybur G.T., Lipton J.W., Terpstra B.T., Sortwell C.E. Stimulation of the rat subthalamic nucleus is neuroprotective following significant nigral dopamine neuron loss. Neurobiol. Dis. 2010, 39:105-115.
48. Steiner B., Kupsch A., Siebert E., Hosmann K., Klempin F., Morgenstern R., Winter C. Unilateral lesion of the subthalamic nucleus transiently provokes bilateral subacute glial cell proliferation in the adult rat substantia nigra. Neurosci. Lett. 2008, 430:103-108.
49. Suzuki K., Okada K., Wakuda T., Shinmura C., Kameno Y., Iwata K., Takahashi T., Suda S., Matsuzaki H., Iwata Y., Hashimoto K., Mori N. Destruction of dopaminergic neurons in the midbrain by 6-hydroxydopamine decreases hippocampal cell proliferation in rats: reversal by fluoxetine. PLoS ONE 2010, 5:e9260.
50. Temel Y., Boothman L.J., Blokland A., Magill P.J., Steinbusch H.W., Visser-Vandewalle V., Sharp T. Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc. Natl Acad. Sci. USA 2007, 104:17087-17092.
51. Temel Y., Tan S., Vlamings R., Sesia T., Lim L.W., Lardeux S., Visser-Vandewalle V., Baunez C. Cognitive and limbic effects of deep brain stimulation in preclinical studies. Front. Biosci. 2009, 14:1891-1901.
52. Temel Y., Visser-Vandewalle V., Kaplan S., Kozan R., Daemen M.A., Blokland A., Schmitz C., Steinbusch H.W. Protection of nigral cell death by bilateral subthalamic nucleus stimulation. Brain Res. 2006, 1120:100-105.
53. Toda H., Hamani C., Fawcett A.P., Hutchison W.D., Lozano A.M. The regulation of adult rodent hippocampal neurogenesis by deep brain stimulation. J. Neurosurg. 2008, 108:132-138.
54. Uc E.Y., Follett K.A. Deep brain stimulation in movement disorders. Semin. Neurol. 2007, 27:170-182.
55. Voon V., Krack P., Lang A.E., Lozano A.M., Dujardin K., Schupbach M., Thobois S., Tamma F., Herzog J., Samanta J., Kubu C., Rossignol H., Poon Y.Y., Saint-Cyr J.A., Ardouin C., Moro E. Parkinson's disease, DBS and suicide: a role for serotonin?. Brain 2009, Jun 24.
56. Wallace B.A., Ashkan K., Heise C.E., Foote K.D., Torres N., Mitrofanis J., Benabid A.L. Survival of midbrain dopaminergic cells after lesion or deep brain stimulation of the subthalamic nucleus in MPTP-treated monkeys. Brain 2007, 130:2129-2145.
57. Winner B., Geyer M., Couillard-Despres S., Aigner R., Bogdahn U., Aigner L., Kuhn G., Winkler J. Striatal deafferentation increases dopaminergic neurogenesis in the adult olfactory bulb. Exp. Neurol. 2006, 197:113-121.
58. Wojtowicz J.M., Kee N. BrdU assay for neurogenesis in rodents. Nat. Protoc. 2006, 1:1399-1405.
59. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.
60. Zhao X.D., Cao Y.Q., Liu H.H., Li F.Q., You B.M., Zhou X.P. Long term high frequency stimulation of STN increases dopamine in the corpus striatum of hemiparkinsonian rhesus monkey. Brain Res. 2009, 1286:230-238.
61. Ziemssen T., Reichmann H. Non-motor dysfunction in Parkinson's disease. Parkinsonism Relat. Disord. 2007, 13:323-332.