![[PDF]](/pb-assets/Icons/adobe-pdf-icon-1498649896243.png){kind=icon}
Abstract
Deep brain stimulation (DBS), applying high-frequency electrical stimulation to deep brain structures, has now provided an effective therapeutic option for treatment of various neurological and psychiatric disorders. DBS targeting the internal segment of the globus pallidus, subthalamic nucleus, and thalamus is used to treat symptoms of movement disorders, such as Parkinson’s disease, dystonia, and tremor. However, the mechanism underlying the beneficial effects of DBS remains poorly understood and is still under debate: Does DBS inhibit or excite local neuronal elements? In this short review, we would like to introduce our recent work on the physiological mechanism of DBS and propose an alternative explanation: DBS dissociates input and output signals, resulting in the disruption of abnormal information flow through the stimulation site.
References
Section:
| Albin, RL, Young, AB, Penney, JB. 1989. The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–75. Google Scholar, Crossref, Medline, ISI | |
| 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 89:1150–60. Google Scholar, Crossref, Medline, ISI | |
| Anderson, TR, Hu, B, Iremonger, K, Kiss, ZH. 2006. Selective attenuation of afferent synaptic transmission as a mechanism of thalamic deep brain stimulation-induced tremor arrest. J Neurosci 26:841–50. Google Scholar, Crossref, Medline, ISI | |
| 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 6:288–92. Google Scholar, Crossref, Medline, ISI | |
| 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 24:7410–9. Google Scholar, Crossref, Medline, ISI | |
| Baron, MS, Vitek, JL, Bakay, RA, Green, J, McDonald, WM, Cole, SA, and others. 2000. Treatment of advanced Parkinson’s disease by unilateral posterior GPi pallidotomy: 4-year results of a pilot study. Mov Disord 15:230–7. Google Scholar, Crossref, Medline, ISI | |
| Baron, MS, Wichmann, T, Ma, D, DeLong, MR. 2002. Effects of transient focal inactivation of the basal ganglia in parkinsonian primates. J Neurosci 22:592–9. Google Scholar, Medline, ISI | |
| Benabid, AL, Pollak, P, Gao, D, Hoffmann, D, Limousin, P, Gay, E, and others. 1996. Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J Neurosurg 84:203–14. Google Scholar, Crossref, Medline, ISI | |
| Benabid, AL, Pollak, P, Gervason, C, Hoffmann, D, Gao, DM, Hommel, M, and others. 1991. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337:403–6. Google Scholar, Crossref, Medline, ISI | |
| Benabid, AL, Pollak, P, Gross, C, Hoffmann, D, Benazzouz, A, Gao, DM, and others. 1994. Acute and long-term effects of subthalamic nucleus stimulation in Parkinson’s disease. Stereotact Funct Neurosurg 62:76–84. Google Scholar, Crossref, Medline | |
| 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 5:382–9. Google Scholar, Crossref, Medline, ISI | |
| Bergman, H, Feingold, A, Nini, A, Raz, A, Slovin, H, Abeles, M, and others. 1998. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci 21:32–8. Google Scholar, Crossref, Medline, ISI | |
| Bergman, H, Wichmann, T, DeLong, MR. 1990. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249:1436–8. Google Scholar, Crossref, Medline, ISI | |
| Bergman, H, Wichmann, T, Karmon, B, DeLong, MR. 1994. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72:507–20. Google Scholar, Medline, ISI | |
| 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 85:1351–6. Google Scholar, Medline, ISI | |
| 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. Google Scholar, Crossref, Medline, ISI | |
| Boraud, T, Bezard, E, Bioulac, B, Gross, CE. 2000. Ratio of inhibited-to-activated pallidal neurons decreases dramatically during passive limb movement in the MPTP-treated monkey. J Neurophysiol 83:1760–3. Google Scholar, Medline, ISI | |
| Boraud, T, Bezard, E, Guehl, D, Bioulac, B, Gross, C. 1998. Effects of L-DOPA on neuronal activity of the globus pallidus externalis (GPe) and globus pallidus internalis (GPi) in the MPTP-treated monkey. Brain Res 787:157–60. Google Scholar, Crossref, Medline, ISI | |
| Brown, P . 2003. Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson’s disease. Mov Disord 18:357–63. Google Scholar, Crossref, Medline, ISI | |
| Brown, P, Oliviero, A, Mazzone, P, Insola, A, Tonali, P, Di Lazzaro, V. 2001. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J Neurosci 21:1033–8. Google Scholar, Medline, ISI | |
| Brown, P, Williams, D. 2005. Basal ganglia local field potential activity: character and functional significance in the human. Clin Neurophysiol 116:2510–9. Google Scholar, Crossref, Medline, ISI | |
| Chiken, S, Nambu, A. 2013. High-frequency pallidal stimulation disrupts information flow through the pallidum by GABAergic inhibition. J Neurosci 33:2268–80. Google Scholar, Crossref, Medline, ISI | |
| Chiken, S, Shashidharan, P, Nambu, A. 2008. Cortically evoked long-lasting inhibition of pallidal neurons in a transgenic mouse model of dystonia. J Neurosci 28:13967–77. Google Scholar, Crossref, Medline, ISI | |
| 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 345:956–63. Google Scholar, Crossref, Medline, ISI | |
| Degos, B, Deniau, JM, Chavez, M, Maurice, N. 2013. Subthalamic nucleus high-frequency stimulation restores altered electrophysiological properties of cortical neurons in parkinsonian rat. PloS One 8:e83608. Google Scholar, Crossref, Medline, ISI | |
| Degos, B, Deniau, JM, Thierry, AM, Glowinski, J, Pezard, L, Maurice, N. 2005. Neuroleptic-induced catalepsy: electrophysiological mechanisms of functional recovery induced by high-frequency stimulation of the subthalamic nucleus. J Neurosci 25:7687–96. Google Scholar, Crossref, Medline, ISI | |
| DeLong, MR . 1990. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281–5. Google Scholar, Crossref, Medline, ISI | |
| Deniau, JM, Degos, B, Bosch, C, Maurice, N. 2010. Deep brain stimulation mechanisms: beyond the concept of local functional inhibition. Eur J Neurosci 32:1080–91. Google Scholar, Crossref, Medline, ISI | |
| Do, MT, Bean, BP. 2003. Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39:109–20. Google Scholar, Crossref, Medline, ISI | |
| 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 84:570–4. Google Scholar, Medline, ISI | |
| Dostrovsky, JO, Lozano, AM. 2002. Mechanisms of deep brain stimulation. Mov Disord 17(suppl 3):S63–8. Google Scholar, Crossref, Medline, ISI | |
| Erez, Y, Czitron, H, McCairn, K, Belelovsky, K, Bar-Gad, I. 2009. Short-term depression of synaptic transmission during stimulation in the globus pallidus of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primates. J Neurosci 29:7797–802. Google Scholar, Crossref, Medline, ISI | |
| Filali, M, Hutchison, WD, Palter, VN, Lozano, AM, Dostrovsky, JO. 2004. Stimulation-induced inhibition of neuronal firing in human subthalamic nucleus. Exp Brain Res 156:274–81. Google Scholar, Crossref, Medline, ISI | |
| Filion, M, Tremblay, L. 1991. Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 547:142–51. Google Scholar, Medline, ISI | |
| Galati, S, Mazzone, P, Fedele, E, Pisani, A, Peppe, A, Pierantozzi, M, and others. 2006. Biochemical and electrophysiological changes of substantia nigra pars reticulata driven by subthalamic stimulation in patients with Parkinson’s disease. Eur J Neurosci 23:2923–8. Google Scholar, Crossref, Medline, ISI | |
| Gatev, P, Darbin, O, Wichmann, T. 2006. Oscillations in the basal ganglia under normal conditions and in movement disorders. Mov Disord 21:1566–77. Google Scholar, Crossref, Medline, ISI | |
| Gerfen, CR, Engber, TM, Mahan, LC, Susel, Z, Chase, TN, Monsma, FJ, and others. 1990. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250:1429–32. Google Scholar, Crossref, Medline, ISI | |
| Gradinaru, V, Mogri, M, Thompson, KR, Henderson, JM, Deisseroth, K. 2009. Optical deconstruction of parkinsonian neural circuitry. Science 324:354–9. Google Scholar, Crossref, Medline, ISI | |
| Hammond, C, Bergman, H, Brown, P. 2007. Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci 30:357–64. Google Scholar, Crossref, Medline, ISI | |
| 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 23:1916–23. Google Scholar, Medline, ISI | |
| Heimer, G, Bar-Gad, I, Goldberg, JA, Bergman, H. 2002. Dopamine replacement therapy reverses abnormal synchronization of pallidal neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of parkinsonism. J Neurosci 22:7850–5. Google Scholar, Medline, ISI | |
| Heimer, G, Rivlin-Etzion, M, Bar-Gad, I, Goldberg, JA, Haber, SN, Bergman, H. 2006. Dopamine replacement therapy does not restore the full spectrum of normal pallidal activity in the 1-methyl-4-phenyl-1,2,3,6-tetra-hydropyridine primate model of Parkinsonism. J Neurosci 26:8101–14. Google Scholar, Crossref, Medline, ISI | |
| Johnson, MD, McIntyre, CC. 2008. Quantifying the neural elements activated and inhibited by globus pallidus deep brain stimulation. J Neurophysiol 100:2549–63. Google Scholar, Crossref, Medline, ISI | |
| Kita, H, Kita, T. 2011. Cortical stimulation evokes abnormal responses in the dopamine-depleted rat basal ganglia. J Neurosci 31:10311–22. Google Scholar, Crossref, Medline, ISI | |
| Kringelbach, ML, Jenkinson, N, Owen, SL, Aziz, TZ. 2007. Translational principles of deep brain stimulation. Nat Rev Neurosci 8:623–35. Google Scholar, Crossref, Medline, ISI | |
| 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 205:251–61. Google Scholar, Crossref, Medline, ISI | |
| Laitinen, LV, Bergenheim, AT, Hariz, MI. 1992. Ventroposterolateral pallidotomy can abolish all parkinsonian symptoms. Stereotact Funct Neurosurg 58:14–21. Google Scholar, Crossref, Medline, ISI | |
| Leblois, A, Meissner, W, Bezard, E, Bioulac, B, Gross, CE, Boraud, T. 2006. Temporal and spatial alterations in GPi neuronal encoding might contribute to slow down movement in Parkinsonian monkeys. Eur J Neurosci 24:1201–8. Google Scholar, Crossref, Medline, ISI | |
| Leblois, A, Reese, R, Labarre, D, Hamann, M, Richter, A, Boraud, T, and others. 2010. Deep brain stimulation changes basal ganglia output nuclei firing pattern in the dystonic hamster. Neurobiol Dis 38:288–98. Google Scholar, Crossref, Medline, ISI | |
| Lee, KH, Chang, SY, Roberts, DW, Kim, U. 2004. Neurotransmitter release from high-frequency stimulation of the subthalamic nucleus. J Neurosurg 101:511–7. Google Scholar, Crossref, Medline, ISI | |
| Levy, R, Hutchison, WD, Lozano, AM, Dostrovsky, JO. 2000. High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J Neurosci 20:7766–75. Google Scholar, Medline, ISI | |
| Levy, R, Lang, AE, Dostrovsky, JO, Pahapill, P, Romas, J, Saint-Cyr, J, and others. 2001. Lidocaine and muscimol microinjections in subthalamic nucleus reverse Parkinsonian symptoms. Brain 124:2105–18. Google Scholar, Crossref, Medline, ISI | |
| Li, Q, Ke, Y, Chan Danny, CW, Qian, Z-M, Yung Ken, KL, Ko, H, and others. 2012. Therapeutic deep brain stimulation in parkinsonian rats directly influences motor cortex. Neuron 76:1030–41. Google Scholar, Crossref, Medline, ISI | |
| Li, S, Arbuthnott, GW, Jutras, MJ, Goldberg, JA, Jaeger, D. 2007. Resonant antidromic cortical circuit activation as a consequence of high-frequency subthalamic deep-brain stimulation. J Neurophysiol 98:3525–37. Google Scholar, Crossref, Medline, ISI | |
| Limousin, P, Pollak, P, Benazzouz, A, Hoffmann, D, Le Bas, JF, Broussolle, E, and others. 1995. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345:91–5. Google Scholar, Crossref, Medline, ISI | |
| Liu, Y, Postupna, N, Falkenberg, J, Anderson, ME. 2008. High frequency deep brain stimulation: what are the therapeutic mechanisms? Neurosci Biobehav Rev 32:343–51. Google Scholar, Crossref, Medline, ISI | |
| Luo, J, Kaplitt, MG, Fitzsimons, HL, Zuzga, DS, Liu, Y, Oshinsky, ML, and others. 2002. Subthalamic GAD gene therapy in a Parkinson’s disease rat model. Science 298:425–9. Google Scholar, Crossref, Medline, ISI | |
| Mallet, N, Ballion, B, Le Moine, C, Gonon, F. 2006. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci 26:3875–84. Google Scholar, Crossref, Medline, ISI | |
| 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 23:9929–36. Google Scholar, Medline, ISI | |
| 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 101:1941–60. Google Scholar, Crossref, Medline, ISI | |
| 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. Google Scholar, Crossref, Medline, ISI | |
| Meissner, W, Leblois, A, Hansel, D, Bioulac, B, Gross, CE, Benazzouz, A, and others. 2005. Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 128:2372–82. Google Scholar, Crossref, Medline, ISI | |
| 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: Carpenter, MB, Jayaraman, A editors. The basal ganglia II: structure and functions—current concepts. New York: Plenum. p 415–27. Google Scholar, Crossref | |
| Miocinovic, S, Parent, M, Butson, CR, Hahn, PJ, Russo, GS, Vitek, JL, and others. 2006. Computational analysis of subthalamic nucleus and lenticular fasciculus activation during therapeutic deep brain stimulation. J Neurophysiol 96:1569–80. Google Scholar, Crossref, Medline, ISI | |
| Montgomery, EB 2006. Effects of GPi stimulation on human thalamic neuronal activity. Clin Neurophysiol 117:2691–702. Google Scholar, Crossref, Medline, ISI | |
| 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. Google Scholar, Crossref, Medline | |
| Nambu, A . 2008. Seven problems on the basal ganglia. Curr Opin Neurobiol 18:595–604. Google Scholar, Crossref, Medline, ISI | |
| Nambu, A, Chiken, S, Shashidharan, P, Nishibayashi, H, Ogura, M, Kakishita, K, and others. 2011. Reduced pallidal output causes dystonia. Front Syst Neurosci 5:89. Google Scholar, Crossref, Medline | |
| Nambu, A, Tachibana, T, Chiken, S. 2015. Cause of parkinsonian symptoms: firing rate, firing pattern or dynamic activity changes? Basal Ganglia 5:1–6. Google Scholar, Crossref, ISI | |
| Nambu, A, Tokuno, H, Hamada, I, Kita, H, Imanishi, M, Akazawa, T, and others. 2000. Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J Neurophysiol 84:289–300. Google Scholar, Medline, ISI | |
| Nambu, A, Tokuno, H, Takada, M. 2002. Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci Res 43:111–7. Google Scholar, Crossref, Medline, ISI | |
| Nishibayashi, H, Ogura, M, Kakishita, K, Tanaka, S, Tachibana, Y, Nambu, A, and others. 2011. Cortically evoked responses of human pallidal neurons recorded during stereotactic neurosurgery. Mov Disord 26:469–76. Google Scholar, Crossref, Medline, ISI | |
| Ostrem, JL, Starr, PA. 2008. Treatment of dystonia with deep brain stimulation. Neurotherapeutics 5:320–30. Google Scholar, Crossref, Medline, ISI | |
| Perlmutter, JS, Mink, JW. 2006. Deep brain stimulation. Annu Rev Neurosci 29:229–57. Google Scholar, Crossref, Medline, ISI | |
| 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 33:169–73. Google Scholar, Crossref, Medline, ISI | |
| Raz, A, Vaadia, E, Bergman, H. 2000. Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of parkinsonism. J Neurosci 20:8559–71. Google Scholar, Medline, ISI | |
| Reese, R, Leblois, A, Steigerwald, F, Potter-Nerger, M, Herzog, J, Mehdorn, HM, and others. 2011. Subthalamic deep brain stimulation increases pallidal firing rate and regularity. Exp Neurol 229:517–21. Google Scholar, Crossref, Medline, ISI | |
| Shi, LH, Luo, F, Woodward, DJ, Chang, JY. 2006. Basal ganglia neural responses during behaviorally effective deep brain stimulation of the subthalamic nucleus in rats performing a treadmill locomotion test. Synapse 59:445–57. Google Scholar, Crossref, Medline, ISI | |
| Shin, DS, Samoilova, M, Cotic, M, Zhang, L, Brotchie, JM, Carlen, PL. 2007. High frequency stimulation or elevated K+ depresses neuronal activity in the rat entopeduncular nucleus. Neuroscience 149:68–86. Google Scholar, Crossref, Medline, ISI | |
| 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 358:119–41. Google Scholar, Crossref, Medline, ISI | |
| 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. Google Scholar, Crossref, Medline, ISI | |
| Soares, J, Kliem, MA, Betarbet, R, Greenamyre, JT, Yamamoto, B, Wichmann, T. 2004. 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 24:6417–26. Google Scholar, Crossref, Medline, ISI | |
| Starr, PA, Rau, GM, Davis, V, Marks, WJ, Ostrem, JL, Simmons, D, and others. 2005. Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson’s disease and normal macaque. J Neurophysiol 93:3165–76. Google Scholar, Crossref, Medline, ISI | |
| 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 34:1470–84. Google Scholar, Crossref, Medline, ISI | |
| Tai, CH, Boraud, T, Bezard, E, Bioulac, B, Gross, C, Benazzouz, A. 2003. Electrophysiological and metabolic evidence that high-frequency stimulation of the subthalamic nucleus bridles neuronal activity in the subthalamic nucleus and the substantia nigra reticulata. FASEB J 17:1820–30. Google Scholar, Crossref, Medline, ISI | |
| Tang, JK, Moro, E, Mahant, N, Hutchison, WD, Lang, AE, Lozano, AM, and others. 2007. Neuronal firing rates and patterns in the globus pallidus internus of patients with cervical dystonia differ from those with Parkinson’s disease. J Neurophysiol 98:720–9. Google Scholar, Crossref, Medline, ISI | |
| Vitek, JL . 2008. Deep brain stimulation: how does it work? Cleve Clin J Med 75(suppl 2):S59–65. Google Scholar, Crossref, Medline | |
| Vitek, JL, Chockkan, V, Zhang, JY, Kaneoke, Y, Evatt, M, DeLong, MR, and others. 1999. Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus. Ann Neurol 46:22–35. Google Scholar, Crossref, Medline, ISI | |
| Vitek, JL, Zhang, J, Hashimoto, T, Russo, GS, Baker, KB. 2012. External pallidal stimulation improves parkinsonian motor signs and modulates neuronal activity throughout the basal ganglia thalamic network. Exp Neurol 233:581–6. Google Scholar, Crossref, Medline, ISI | |
| Welter, ML, Houeto, JL, Bonnet, AM, Bejjani, PB, Mesnage, V, Dormont, D, and others. 2004. Effects of high-frequency stimulation on subthalamic neuronal activity in parkinsonian patients. Arch Neurol 61:89–96. Google Scholar, Crossref, Medline | |
| Wichmann, T, Delong, MR. 2006. Deep brain stimulation for neurologic and neuropsychiatric disorders. Neuron 52:197–204. Google Scholar, Crossref, Medline, ISI | |
| Wichmann, T, Kliem, MA, Soares, J. 2002. Slow oscillatory discharge in the primate basal ganglia. J Neurophysiol 87:1145–8. Google Scholar, Crossref, Medline, ISI | |
| Wichmann, T, Soares, J. 2006. Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in parkinsonism. J Neurophysiol 95:2120–33. Google Scholar, Crossref, Medline, ISI | |
| Wu, YR, Levy, R, Ashby, P, Tasker, RR, Dostrovsky, JO. 2001. Does stimulation of the GPi control dyskinesia by activating inhibitory axons? Mov Disord 16:208–16. Google Scholar, Crossref, Medline, ISI | |
| Zhuang, P, Li, Y, Hallett, M. 2004. Neuronal activity in the basal ganglia and thalamus in patients with dystonia. Clin Neurophysiol 115:2542–57. Google Scholar, Crossref, Medline, ISI |
