High-frequency pallidal stimulation disrupts information flow through the pallidum by GABAergic inhibition

Journal of Neuroscience

Volumn 33, Issue 6, 2013, Pages 2268-2280

  Chiken, Satomi ^a   Nambu, Atsushi ^a  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL) PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR; 6 NITRO 7 SULFAMOYLBENZO [F] QUINOXALINE 2, 3 DIONE; [3 (3, 4 DICHLOROBENZYLAMINO) PROPYL] (DIETHOXYMETHYL) PHOSPHINIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; ELECTRODE; ELECTROSTIMULATION; EVOKED RESPONSE; GABAERGIC TRANSMISSION; GLOBUS PALLIDUS; HAPLORHINI; HISTOLOGY; NERVE CELL INHIBITION; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; SPIKE WAVE; WAKEFULNESS;

ANIMALS; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; FEMALE; GABAERGIC NEURONS; GLOBUS PALLIDUS; MACACA; MACACA MULATTA; MALE; NEURAL INHIBITION;

EID: 84873321643     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4144-11.2013     Document Type: Article

References (59)

1. Anderson ME, Postupna N, Ruffo M (2003) Effects of high-frequency stimulation in the internal globus pallidus on the activity of thalamic neurons in the awake monkey. J Neurophysiol 89:1150-1160. CrossRef Medline
2. Bar-Gad I, Elias S, Vaadia E, Bergman H (2004) 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 24:7410-7419. CrossRef Medline
3. 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. CrossRef Medline
4. Boraud T, Bezard E, Bioulac B, Gross C (1996) High frequency stimulation of the internal Globus Pallidus (GPi) simultaneously improves parkinsonian symptoms and reduces the firing frequency of GPi neurons in the MPTP-treated monkey. Neurosci Lett 215:17-20. CrossRef Medline
5. Charara A, Pare JF, Levey AI, Smith Y (2005) Synaptic and extrasynaptic GABA-A and GABA-B receptors in the globus pallidus: an electron microscopic immunogold analysis in monkeys. Neuroscience 131:917-933. CrossRef Medline
6. Chiken S, Shashidharan P, Nambu A (2008) Cortically evoked long-lasting inhibition of pallidal neurons in a transgenic mouse model of dystonia. J Neurosci 28:13967-13977. CrossRef Medline
7. Coubes P, Cif L, El Fertit H, Hemm S, Vayssiere N, Serrat S, Picot MC, Tuffery S, Claustres M, Echenne B, Frerebeau P (2004) Electrical stimulation of the globus pallidus internus in patients with primary generalized dystonia: long-term results. J Neurosurg 101:189-194. CrossRef Medline
8. Dostrovsky JO, Levy R, Wu JP, Hutchison WD, Tasker RR, Lozano AM (2000) Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J Neurophysiol 84:570-574. Medline
9. Filali M, Hutchison WD, Palter VN, Lozano AM, Dostrovsky JO (2004) Stimulation-induced inhibition of neuronal firing in human subthalamic nucleus. Exp Brain Res 156:274-281. CrossRef Medline
10. Galati S, Mazzone P, Fedele E, Pisani A, Peppe A, Pierantozzi M, Brusa L, Tropepi D, Moschella V, Raiteri M, Stanzione P, Bernardi G, Stefani A (2006) Biochemical and electrophysiological changes of substantia nigra pars reticulata driven by subthalamic stimulation in patients with Parkinson's disease. Eur J Neurosci 23:2923-2928. CrossRef Medline
11. Galvan A, Wichmann T (2007) GABAergic circuits in the basal ganglia and movement disorders. Prog Brain Res 160:287-312. CrossRef Medline
12. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K (2009) Optical deconstruction of parkinsonian neural circuitry. Science 324: 354-359. CrossRef Medline
13. Hashimoto T, Elder CM, Vitek JL (2002) Atemplate subtraction method for stimulus artifact removal in high-frequency deep brain stimulation. J Neurosci Methods 113:181-186. CrossRef Medline
14. Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL (2003) Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci 23:1916-1923. Medline
15. Jankowska E, Padel Y, Tanaka R (1975) The mode of activation of pyramidal tract cells by intracortical stimuli. J Physiol 249:617-636. Medline
16. Johnson MD, McIntyre CC (2008) Quantifying the neural elements activated and inhibited by globus pallidus deep brain stimulation. J Neurophysiol 100:2549-2563. CrossRef Medline
17. Kaneda K, Kita H (2005) Synaptically released GABA activates both preand postsynaptic GABAB receptors in the rat globus pallidus. J Neurophysiol 94:1104-1114. CrossRef Medline
18. Kita H, Kita T (2011) Cortical stimulation evokes abnormal responses in the dopamine-depleted rat basal ganglia. J Neurosci 31:10311-10322. CrossRef Medline
19. Kita H, Nambu A, Kaneda K, Tachibana Y, Takada M (2004) Role of ionotropic glutamatergic and GABAergic inputs on the firing activity of neurons in the external pallidum in awake monkeys. J Neurophysiol 92:3069-3084. CrossRef Medline
20. Kita H, Chiken S, Tachibana Y, Nambu A (2006) Origins of GABAA and GABAB receptor-mediated responses of globus pallidus induced after stimulation of the putamen in the monkey. J Neurosci 26:6554-6562. CrossRef Medline
21. Lafreniere-Roula M, Kim E, Hutchison WD, Lozano AM, Hodaie M, Dostrovsky JO (2010) High-frequency microstimulation in human globus pallidus and substantia nigra. Exp Brain Res 205:251-261. CrossRef Medline
22. Leblois A, Reese R, Labarre D, Hamann M, Richter A, Boraud T, Meissner WG (2010) Deep brain stimulation changes basal ganglia output nuclei firing pattern in the dystonic hamster. Neurobiol Dis 38:288-298. CrossRef Medline
23. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Broussolle E, Perret JE, Benabid AL (1995) Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345:91-95. CrossRef Medline
24. Logothetis NK, Augath M, Murayama Y, Rauch A, Sultan F, Goense J, Oeltermann A, Merkle H (2010) The effects of electrical microstimulation on cortical signal propagation. Nat Neurosci 13:1283-1291. CrossRef Medline
25. Maltête D, Jodoin N, Karachi C, Houeto JL, Navarro S, Cornu P, Agid Y, Welter ML (2007) Subthalamic stimulation and neuronal activity in the substantia nigra in Parkinson's disease. J Neurophysiol 97:4017-4022. CrossRef Medline
26. Maurice N, Thierry AM, Glowinski J, Deniau JM (2003) Spontaneous and evoked activity of substantia nigra pars reticulata neurons during high-frequency stimulation of the subthalamic nucleus. J Neurosci 23:9929-9936. Medline
27. McCairn KW, Turner RS (2009) Deep brain stimulation of the globus pallidus internus in the parkinsonian primate: local entrainment and suppression of low-frequency oscillations. J Neurophysiol 101:1941-1960. CrossRef Medline
28. McIntyre CC, Grill WM (1999) Excitation of central nervous system neurons by nonuniform electric fields. Biophys J 76:878-888. CrossRef Medline
29. McIntyre CC, Savasta M, Walter BL, Vitek JL (2004) How does deep brain stimulation work? Present understanding and future questions. J Clin Neurophysiol 21:40-50. Medline
30. Meissner W, Leblois A, Hansel D, Bioulac B, Gross CE, Benazzouz A, Boraud T (2005) Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 128:2372-2382. CrossRef Medline
31. Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381-425. CrossRef Medline
32. Montgomery EB Jr (2006) Effects of GPi stimulation on human thalamic neuronal activity. Clin Neurophysiol 117:2691-2702. CrossRef Medline
33. Moran A, Stein E, Tischler H, Belelovsky K, Bar-Gad I (2011) Dynamic stereotypic responses of basal ganglia neurons to subthalamic nucleus high-frequency stimulation in the parkinsonian primate. Front Syst Neurosci 5:21. CrossRef Medline
34. Nambu A, Yoshida S, Jinnai K (1990) Discharge patterns of pallidal neurons with input from various cortical areas during movement in the monkey. Brain Res 519:183-191. CrossRef Medline
35. Nambu A, Tokuno H, Hamada I, Kita H, Imanishi M, Akazawa T, Ikeuchi Y, Hasegawa N (2000) Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J Neurophysiol 84:289-300. Medline
36. Nambu A, Kaneda K, Tokuno H, Takada M (2002a) Organization of corticostriatal motor inputs in monkey putamen. J Neurophysiol 88: 1830-1842. Medline
37. Nambu A, Tokuno H, Takada M (2002b) Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci Res 43: 111-117. CrossRef Medline
38. Nishibayashi H, Ogura M, Kakishita K, Tanaka S, Tachibana Y, Nambu A, Kita H, Itakura T (2011) Cortically evoked responses of human pallidal neurons recorded during stereotactic neurosurgery. Mov Disord 26: 469-476. CrossRef Medline
39. Obeso JA, Olanow CW, Rodriguez-Oroz MC, Krack P, Kumar R, Lang AE, The Deep-Brain Stimulation for Parkinson's Disease Study Group (2001) Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. N Engl J Med 345: 956-963. CrossRef Medline
40. Ostrem JL, Starr PA (2008) Treatment of dystonia with deep brain stimulation. Neurotherapeutics 5:320-330. CrossRef Medline
41. Pralong E, Debatisse D, Maeder M, Vingerhoets F, Ghika J, Villemure JG (2003) Effect of deep brain stimulation of GPI on neuronal activity of the thalamic nucleus ventralis oralis in a dystonic patient. Neurophysiol Clin 33:169-173. CrossRef Medline
42. Reese R, Leblois A, Steigerwald F, Pötter-Nerger M, Herzog J, Mehdorn HM, Deuschl G, Meissner WG, Volkmann J (2011) Subthalamic deep brain stimulation increases pallidal firing rate and regularity. Exp Neurol 229: 517-521. CrossRef Medline
43. Rosin B, Slovik M, Mitelman R, Rivlin-Etzion M, Haber SN, Israel Z, Vaadia E, Bergman H (2011) Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron 72:370-384. CrossRef Medline
44. Shink E, Smith Y (1995) Differential synaptic innervation of neurons in the internal and external segments of the globus pallidus by the GABA- and glutamate-containing terminals in the squirrel monkey. J Comp Neurol 358:119-141. CrossRef Medline
45. Smith Y, Wichmann T, DeLong MR (1994) Synaptic innervation of neurones in the internal pallidal segment by the subthalamic nucleus and the external pallidum in monkeys. J Comp Neurol 343:297-318. CrossRef Medline
46. Starr PA, Rau GM, Davis V, Marks WJ Jr, Ostrem JL, Simmons D, Lindsey N, Turner RS (2005) Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson's disease and normal macaque. J Neurophysiol 93:3165-3176. CrossRef Medline
47. Tachibana Y, Kita H, Chiken S, Takada M, Nambu A (2008) Motor cortical control of internal pallidal activity through glutamatergic and GABAergic inputs in awake monkeys. Eur J Neurosci 27:238-253. CrossRef Medline
48. Tachibana Y, Iwamuro H, Kita H, Takada M, Nambu A (2011) Subthalamo-pallidal interactions underlying parkinsonian neuronal oscillations in the primate basal ganglia. Eur J Neurosci 34:1470-1484. CrossRef Medline
49. Vidailhet M, Vercueil L, Houeto JL, Krystkowiak P, Lagrange C, Yelnik J, Bardinet E, Benabid AL, Navarro S, Dormont D, Grand S, Blond S, Ardouin C, Pillon B, Dujardin K, Hahn-Barma V, Agid Y, Destée A, Pollak P, French SPIDY Study Group (2007) Bilateral, pallidal, deep-brain stimulation in primary generalised dystonia: a prospective 3 year follow-up study. Lancet Neurol 6:223-229. CrossRef Medline
50. Vitek JL (2008) Deep brain stimulation: how does it work? Cleve Clin J Med 75;suppl 2:S59-S65. CrossRef Medline
51. Vitek JL, Hashimoto T, Peoples J, DeLong MR, Bakay RA (2004) Acute stimulation in the external segment of the globus pallidus improves parkinsonian motor signs. Mov Disord 19:907-915. CrossRef Medline
52. Wichmann T (2000) A digital averaging method for removal of stimulus artifacts in neurophysiologic experiments. J Neurosci Methods 98:57-62. CrossRef Medline
53. Wichmann T, DeLong MR (2006) Deep brain stimulation for neurologic and neuropsychiatric disorders. Neuron 52:197-204. CrossRef Medline
54. Wichmann T, Bergman H, DeLong MR (1994) The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J Neurophysiol 72:521-530. Medline
55. 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. CrossRef Medline
56. Windels F, Carcenac C, Poupard A, Savasta M (2005) Pallidal origin of GABA release within the substantia nigra pars reticulata during high-frequency stimulation of the subthalamic nucleus. J Neurosci 25:5079-5086. CrossRef Medline
57. Wu YR, Levy R, Ashby P, Tasker RR, Dostrovsky JO (2001) Does stimulation of the GPi control dyskinesia by activating inhibitory axons? Mov Disord 16:208-216. CrossRef Medline
58. Yelnik J, Damier P, Bejjani BP, François C, Gervais D, Dormont D, Arnulf I, Bonnet AM, Cornu P, Pidoux B, Agid Y (2000) Functional mapping of the human globus pallidus: contrasting effect of stimulation in the internal and external pallidum in Parkinson's disease. Neuroscience 101:77-87. CrossRef Medline
59. Yoshida S, Nambu A, Jinnai K (1993) The distribution of the globus pallidus neurons with input from various cortical areas in the monkey. Brain Res 611:170-174. CrossRef Medline