Deep brain stimulation changes basal ganglia output nuclei firing pattern in the dystonic hamster

Neurobiology of Disease

Volumn 38, Issue 2, 2010, Pages 288-298

  Leblois, Arthur ^a   Reese, René ^a,b   Labarre, David ^a   Hamann, Melanie ^c   Richter, Angelika ^c   Boraud, Thomas ^a   Meissner, Wassilios G ^a,d  

^a UMR 5287   (France)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d BORDEAUX UNIVERSITY HOSPITAL   (France)

Author keywords

Basal ganglia; Dystonia; Entopeduncular; Extracellular recordings; Stimulation; Substantia nigra

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN DEPTH RECORDING; BRAIN DEPTH STIMULATION; BRAIN NERVE CELL; CONTROLLED STUDY; DYSTONIA; ENTOPEDUNCULAR NUCLEUS; FEMALE; HAMSTER; HISTOLOGY; MALE; NONHUMAN; PRIORITY JOURNAL; SPECTROSCOPY; SPIKE; SUBSTANTIA NIGRA; SYMPTOM;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BASAL GANGLIA; CRICETINAE; DEEP BRAIN STIMULATION; DYSTONIA; ELECTRODES, IMPLANTED; ELECTROPHYSIOLOGY; ENTOPEDUNCULAR NUCLEUS; FEMALE; MALE; NEURONS; SIGNAL PROCESSING, COMPUTER-ASSISTED; SUBSTANTIA NIGRA;

EID: 77951207822     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.01.020     Document Type: Article

References (56)

1. Ackermans L., Temel Y., Cath D., van der Linden C., Bruggeman R., Kleijer M., Nederveen P., Schruers K., Colle H., Tijssen M.A., Visser-Vandewalle V. Deep brain stimulation in Tourette's syndrome: two targets?. Mov. Disord. 2006, 21:709-713.
2. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
3. Bar-Gad I., Elias S., Vaadia E., Bergman H. Complex locking rather than complete cessation of neuronal activity in the globus pallidus of a 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-treated primate in response to pallidal microstimulation. J. Neurosci. 2004, 24:7410-7419.
4. Bennay M., Gernert M., Richter A. Spontaneous remission of paroxysmal dystonia coincides with normalization of entopeduncular activity in dt(SZ) mutants. J. Neurosci. 2001, 21:RC153.
5. Berardelli A., Rothwell J.C., Hallett M., Thompson P.D., Manfredi M., Marsden C.D. The pathophysiology of primary dystonia. Brain 1998, 121(Pt 7):1195-1212.
6. Bolam J.P., Hanley J.J., Booth P.A., Bevan M.D. Synaptic organisation of the basal ganglia. J. Anat. 2000, 196(Pt 4):527-542.
7. Bressman S.B. Dystonia update. Clin. Neuropharmacol. 2000, 23:239-251.
8. Chen C.C., Kuhn A.A., Hoffmann K.T., Kupsch A., Schneider G.H., Trottenberg T., Krauss J.K., Wohrle J.C., Bardinet E., Yelnik J., Brown P. Oscillatory pallidal local field potential activity correlates with involuntary EMG in dystonia. Neurology 2006, 66:418-420.
9. Clarke N.P., Bevan M.D., Cozzari C., Hartman B.K., Bolam J.P. Glutamate-enriched cholinergic synaptic terminals in the entopeduncular nucleus and subthalamic nucleus of the rat. Neuroscience 1997, 81:371-385.
10. Coubes P., Roubertie A., Vayssiere N., Hemm S., Echenne B. Treatment of DYT1-generalised dystonia by stimulation of the internal globus pallidus. Lancet 2000, 355:2220-2221.
11. DeLong M.R. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990, 13:281-285.
12. Deniau J.M., Menetrey A., Charpier S. The lamellar organization of the rat substantia nigra pars reticulata: segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections. Neuroscience 1996, 73:761-781.
13. Detante O., Vercueil L., Thobois S., Broussolle E., Costes N., Lavenne F., Chabardes S., Lebars D., Vidailhet M., Benabid A.L., Pollak P. Globus pallidus internus stimulation in primary generalized dystonia: a H215O PET study. Brain 2004, 127:1899-1908.
14. Dostrovsky J.O., Levy R., Wu J.P., Hutchison W.D., Tasker R.R., Lozano A.M. Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J. Neurophysiol. 2000, 84:570-574.
15. Edwards F.A., Konnerth A., Sakmann B. Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J. Physiol. 1990, 430:213-249.
16. Fahn S. Concept and classification of dystonia. Adv. Neurol. 1988, 50:1-8.
17. Galati S., Scarnati E., Mazzone P., Stanzione P., Stefani A. Deep brain stimulation promotes excitation and inhibition in subthalamic nucleus in Parkinson's disease. Neuroreport 2008, 19:661-666.
18. Garcia L., Audin J., D'Alessandro G., Bioulac B., Hammond C. Dual effect of high-frequency stimulation on subthalamic neuron activity. J. Neurosci. 2003, 23:8743-8751.
19. Gernert M., Hamann M., Bennay M., Löscher W., Richter A. Deficit of striatal parvalbumin-reactive GABAergic interneurons and decreased basal ganglia output in a genetic rodent model of idiopathic paroxysmal dystonia. J. Neurosci. 2000, 20:7052-7058.
20. Gernert M., Bennay M., Fedrowitz M., Rehders J.H., Richter A. Altered discharge pattern of basal ganglia output neurons in an animal model of idiopathic dystonia. J. Neurosci. 2002, 22:7244-7253.
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. Halliday D.M., Rosenberg J.R. On the application, estimation and interpretation of coherence and pooled coherence. J. Neurosci. Methods 2000, 100:173-174.
23. Hammond C., Ammari R., Bioulac B., Garcia L. Latest view on the mechanism of action of deep brain stimulation. Mov. Disord. 2008, 23:2111-2121.
24. Harnack D., Hamann M., Meissner W., Morgenstern R., Kupsch A., Richter A. High-frequency stimulation of the entopeduncular nucleus improves dystonia in dtsz hamsters. Neuroreport 2004, 15:1391-1393.
25. Hutchison W.D., Lang A.E., Dostrovsky J.O., Lozano A.M. Pallidal neuronal activity: implications for models of dystonia. Ann. Neurol. 2003, 53:480-488.
26. Kaneoke Y., Vitek J.L. Burst and oscillation as disparate neuronal properties. J. Neurosci. Methods 1996, 68:211-223.
27. Kita H., Kitai S.T. Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J. Comp. Neurol. 1987, 260:435-452.
28. Kupsch A., Benecke R., Muller J., Trottenberg T., Schneider G.H., Poewe W., Eisner W., Wolters A., Muller J.U., Deuschl G., Pinsker M.O., Skogseid I.M., Roeste G.K., Vollmer-Haase J., Brentrup A., Krause M., Tronnier V., Schnitzler A., Voges J., Nikkhah G., Vesper J., Naumann M., Volkmann J. Pallidal deep-brain stimulation in primary generalized or segmental dystonia. New Engl. J. Med. 2006, 355:1978-1990.
29. Labarre D., Meissner W., Boraud T. Measure of the regularity of events in stochastic point processes, application to neuron activity analysis. Proceedings of the IEEE International Conference on Acoustics, Speech and Signal Processing 2008, 489-492.
30. Lerma J., Morales M., Vicente M.A., Herreras O. Glutamate receptors of the kainate type and synaptic transmission. Trends Neurosci. 1997, 20:9-12.
31. Löscher W., Fisher J.E., Schmidt D., Fredow G., Honack D., Iturrian W.B. The sz mutant hamster: a genetic model of epilepsy or of paroxysmal dystonia?. Mov. Disord. 1989, 4:219-232.
32. McCairn K.W., Turner R.S. Deep brain stimulation of the globus pallidus internus in the parkinsonian primate: local entrainment and suppression of low-frequency oscillations. J. Neurophysiol. 2009, 101:1941-1960.
33. McIntyre C.C., Grill W.M., Sherman D.L., Thakor N.V. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J. Neurophysiol. 2004, 91:1457-1469.
34. Montgomery E.B. Effects of GPi stimulation on human thalamic neuronal activity. Clin. Neurophysiol. 2006, 117:2691-2702.
35. Mouroux M., Hassani O.K., Féger J. Electrophysiological study of the excitatory parafascicular projection to the subthalamic nucleus and evidence for ipsi- and controlateral controls. Neuroscience 1995, 67:399-407.
36. Pouzat C., Delescluse M., Viot P., Diebolt J. Improved spike-sorting by modeling firing statistics and burst-dependent spike amplitude attenuation: a Markov chain Monte Carlo approach. J. Neurophysiol. 2004, 91:2910-2928.
37. Pralong E., Pollo C., Villemure J.G., Debatisse D. Opposite effects of internal globus pallidus stimulation on pallidal neurones activity. Mov. Disord. 2007, 22:1879-1884.
38. Ranck J.B. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 1975, 98:417-440.
39. Reese R., Charron G., Nadjar A., Aubert I., Thiolat M.L., Hamann M., Richter A., Bezard E., Meissner W.G. High frequency stimulation of the entopeduncular nucleus sets the cortico-basal ganglia network to a new functional state in the dystonic hamster. Neurobiol. Dis. 2009, 35:399-405.
40. Richter A., Löscher W. Pathology of idiopathic dystonia: findings from genetic animal models. Prog. Neurobiol. 1998, 54:633-677.
41. Richter A., Löscher W. Animal models of paroxysmal dystonia. Adv. Neurol. 2002, 89:443-451.
42. Ruskin D.N., Bergstrom D.A., Kaneoke Y., Patel B.N., Twery M.J., Walters J.R. Multisecond oscillations in firing rate in the basal ganglia: robust modulation by dopamine receptor activation and anesthesia. J. Neurophysiol. 1999, 81:2046-2055.
43. Sharott A., Grosse P., Kuhn A.A., Salih F., Engel A.K., Kupsch A., Schneider G.H., Krauss J.K., Brown P. Is the synchronization between pallidal and muscle activity in primary dystonia due to peripheral afference or a motor drive?. Brain 2008, 131:473-484.
44. Silberstein P., Kühn A.A., Kupsch A., Trottenberg T., Krauss J.K., Wöhrle J.C., Mazzone P., Insola A., Di Lazarro V., Oliviero A., Aziz T., Brown P. Patterning of globus pallidus local field potentials differs between Parkinson's disease and dystonia. Brain 2003, 126:2597-2608.
45. Soares J., Kliem M.A., Betarbet R., Greenamyre J.T., Yamamoto B., Wichmann T. Role of external pallidal segment in primate parkinsonism: comparison of the effects of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced parkinsonism and lesions of the external pallidal segment. J. Neurosci. 2004, 24:6417-6426.
46. Starr P.A., Rau G.M., Davis V., Marks W.J., Ostrem J.L., Simmons D., Lindsey N., Turner R.S. Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson's disease and normal macaque. J. Neurophysiol. 2005, 93:3165-3176.
47. Steigerwald F., Potter M., Herzog J., Pinsker M., Kopper F., Mehdorn H., Deuschl G., Volkmann J. Neuronal activity of the human subthalamic nucleus in the parkinsonian and nonparkinsonian state. J. Neurophysiol. 2008, 100:2515-2524.
48. Tang J.K., Moro E., Mahant N., Hutchison W.D., Lang A.E., Lozano A.M., Dostrovsky J.O. Neuronal firing rates and patterns in the globus pallidus internus of patients with cervical dystonia differ from those with Parkinson's disease. J. Neurophysiol. 2007, 98:720-729.
49. Trottenberg T., Volkmann J., Deuschl G., Kuhn A.A., Schneider G.H., Muller J., Alesch F., Kupsch A. Treatment of severe tardive dystonia with pallidal deep brain stimulation. Neurology 2005, 64:344-346.
50. Vidailhet M., Vercueil L., Houeto J.L., Krystkowiak P., Benabid A.L., Cornu P., Lagrange C., Tezenas du M.S., Dormont D., Grand S., Blond S., Detante O., Pillon B., Ardouin C., Agid Y., Destee A., Pollak P. Bilateral deep-brain stimulation of the globus pallidus in primary generalized dystonia. New Engl. J. Med. 2005, 352:459-467.
51. Vitek J.L. Pathophysiology of dystonia: a neuronal model. Mov. Disord. 2002, 17:49-62.
52. Vitek J.L., Chockkan V., Zhang J.Y., Kaneoke Y., Evatt M., DeLong M.R., Triche S., Mewes K., Hashimoto T., Bakay R.A. Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus. Ann. Neurol. 1999, 46:22-35.
53. Welter M.L., Mallet L., Houeto J.L., Karachi C., Czernecki V., Cornu P., Navarro S., Pidoux B., Dormont D., Bardinet E., Yelnik J., Damier P., Agid Y. Internal pallidal and thalamic stimulation in patients with Tourette syndrome. Arch. Neurol. 2008, 65:952-957.
54. Windels F., Bruet N., Poupard A., Urbain N., Chouvet G., Feuerstein C., Savasta M. 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. 2000, 12:4141-4146.
55. Windels F., Carcenac C., Poupard A., Savasta M. Pallidal origin of GABA release within the substantia nigra pars reticulata during high-frequency stimulation of the subthalamic nucleus. J. Neurosci. 2005, 25:5079-5086.
56. Zhuang P., Hallett M., Zhang X., Li J., Zhang Y., Li Y. Neuronal activity in the globus pallidus internus in patients with tics. J. Neurol. Neurosurg. Psychiatry 2009, 80:1075-1081.