How Does Deep Brain Stimulation Work? Present Understanding and Future Questions

Journal of Clinical Neurophysiology

Volumn 21, Issue 1, 2004, Pages 40-50

  McIntyre, Cameron C ^a   Savasta, Marc ^b   Walter, Benjamin L ^c   Vitek, Jerrold L ^c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIV GRENOBLE ALPES   (France)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Basal ganglia; High frequency stimulation; Movement disorders

Indexed keywords

BASAL GANGLION; BRAIN DEPTH STIMULATION; CENTRAL NERVOUS SYSTEM; DEPOLARIZATION; DYSTONIA; EPILEPSY; ESSENTIAL TREMOR; HUMAN; MENTAL DISEASE; MICRODIALYSIS; NERVE CELL NETWORK; OBSESSIVE COMPULSIVE DISORDER; PARKINSON DISEASE; REVIEW; SYNAPTIC INHIBITION; THALAMUS;

BASAL GANGLIA; ELECTRIC STIMULATION THERAPY; HUMANS; MOVEMENT DISORDERS; NERVE NET; NEURAL INHIBITION; NEURAL NETWORKS (COMPUTER); NEURONS; SYNAPTIC TRANSMISSION; THALAMUS; TREATMENT OUTCOME;

EID: 1942517467     PISSN: 07360258     EISSN: None     Source Type: Journal    
DOI: 10.1097/00004691-200401000-00006     Document Type: Review

References (92)

1. Alexander G, Crutcher M. (1990) Functional architecture of basal ganglia circuits. Neural substrates of parallel processing. Trends Neurosci. 13:266-271.
2. 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.
3. Ashby P, Kim YJ, Kumar R, Lang AE, Lozano AM. (1999) Neurophysiological effects of stimulation through electrodes in the human subthalamic nucleus. Brain. 122:1919-1931.
4. Baker DA, Xi ZX, Shen H, Swanson CJ, Kalivas PW. (2002) The origin and neuronal function of in vivo nonsynaptic glutamate. J Neurosci. 22:9134-1941.
5. Baldissera F, Lundberg A, Udo M. (1972) Stimulation of pre- and postsynaptic elements in the red nucleus. Exp Brain Res. 15:151-167.
6. Benabid AL, Benazzous A, Pollak P. (2002) Mechanisms of deep brain stimulation. Mov Disord. 17(suppl 3):S73-S74.
7. Benabid AL, Pollak P, Gao D, Hoffmann D, Limousin P, Gay E, Payen I, Benazzouz A. (1996) Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J Neurosurg. 84:203-214.
8. Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, Perret JE, de Rougemont J. (1991) Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet. 337:403-406.
9. Benabid AL, Pollak P, Louveau A, Henry S, de Rougemont J. (1987) Combined (thalamotomy, stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol. 50:344-346.
10. Benazzouz A, Gao DM, Ni ZG, Piallat B, Bouali-Benazzouz 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.
11. 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.
12. Bergman H, Feingold A, Nini A, Raz A, Slovin H, Abeles M, Vaadia E. (1998) Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. 21:32-38.
13. 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.
14. Bikson M, Lian J, Hahn PJ, Stacey WC, Sciortino C, Durand DM. (2001) Suppression of epileptiform activity by high frequency sinusoidal fields in rat hippocampal slices. J Physiol. 531:181-191.
15. 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.
16. 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.
17. Ceballos-Baumann AO, Boecker H, Fogel W, Alesch F, Bartenstein P, Conrad B, Diederich N, von Falkenhayn I, Moringlane JR, Schwaiger M, Tronnier VM. (2001) Thalamic stimulation for essential tremor activates motor and deactivates vestibular cortex. Neurology. 56:1347-1354.
18. Coubes P, Roubertie A, Vayssiere N, Hemm S, Echenne B. (2000) Treatment of DYT1-generalised dystonia by stimulation of the internal globus pallidus. Lancet. 355:2220-2221.
19. Davis KD, Taub E, Houle S, Lang AE, Dostrovsky JO, Tasker RR, Lozano AM. (1997) Globus pallidus stimulation activates the cortical motor system during alleviation of parkinsonian symptoms (comment). Nat Med. 3:671-674.
20. 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. 15:6562-75.
21. DeLong MR. (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13:281-285.
22. Destexhe A, Neubig M, Ulrich D, Huguenard J. (1998) Dendritic low-threshold calcium currents in thalamic relay cells. J Neurosci. 18:3574-3588.
23. Deuschl G, Raethjen J, Lindemann M, Krack P. (2001) The pathophysiology of tremor. Muscle Nerve. 24:716-735.
24. 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.
25. Dostrovsky JO, Lozano AM. (2002) Mechanisms of deep brain stimulation. Mov Disord. 17(suppl 3):63-68.
26. Dostrovsky JO, Patra S, Hutchison WD, Palter VN, Filali M, Lozano AM. (2002) Effects of stimulation in human thalamus on activity of nearby thalamic neurons. Abstr Soc Neurosci. 62:14.
27. Fukuda M, Mentis M, Ghilardi MF, Dhawan V, Antonini A, Hammerstad J, Lozano AM, Lang A, Lyons K, Koller W, Ghez C, Eidelberg D. (2001) Functional correlates of pallidal stimulation for Parkinson's disease (comment). Ann Neurol. 49:155-164.
28. Gabriels LA, Cosyns PR, Meyerson BA, Andreewitch S, Sunaert SG, Maes AF, Dupont PJ, Gybels JM, Gielen F, Demeulemeester HG. (2003) Long-term electrical capsular stimulation in patients with obsessive-compulsive disorder. Neurosurgery. 52:1263-1274.
29. Garcia L, Audin J, D'Alessandro G, Bioulac B, Hammond C. (2003) Dual effect of high-frequency stimulation on subthalamic neuron activity. J Neurosci. 23:8743-8751.
30. Grill WM, McIntyre CC. (2001) Extracellular excitation of central neurons: implications for the mechanisms of deep brain stimulation. Thalamus Rel Syst. 1:269-277.
31. Gross RE, Lozano AM. (2000) Advances in neurostimulation for movement disorders. Neurol Res. 22:247-258.
32. 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. Behavioural and biochemical analysis. Brain. 119:1717-1727.
33. Gustafsson B, Jankowska E. (1976) Direct and indirect activation of nerve cells by electrical pulses applied extracellularly. J Physiol. 258:33-61.
34. Hamel W, Fietzek U, Morsnowski A, Schrader B, Herzog J, Weinert D, Pfister G, Muller D, Volkmann J, Deuschl G, Mehdom HM. (2003) Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: evaluation of active electrode contacts. J Neurol Neurosurg Psych. 74:1036-1046.
35. 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.
36. Hashimoto T, Elder CM, Vitek JL. (2002) A template subtraction method for stimulus artifact removal in high-frequency deep brain stimulation. J Neurosci Methods. 113:181-186.
37. Haslinger B, Boecker H, Buchel C, Vesper J, Tronnier VM, Pfister R, Alesch F, Moringlane JR, Krauss JK, Conrad B, Schwaiger M, Ceballos-Baumann AO. (2003) Differential modulation of subcortical target and cortex during deep brain stimulation. Neuroimage. 18:517-524.
38. Hilker R, Voges J, Thiel A, Ghaemi M, Herholz K, Sturm V, Heiss WD. (2002) Deep brain stimulation of the subthalamic nucleus versus levodopa challenge in Parkinson's disease: measuring the on- and off-conditions with FDG-PET. J Neural Transm. 109:1257-1264.
39. Hodaie M, Wennberg RA, Dostrovsky JO, Lozano AM. (2002) Chronic anterior thalamus stimulation for intractable epilepsy. Epilepsia. 43:603-608.
40. Jankowska E, Padel Y, Tanaka R. (1975) The mode of activation of pyramidal tract cells by intracortical stimuli. J Physiol. 249:617-636.
41. Jech R, Urgosik D, Tintera J, Nebuzelsky A, Krasensky J, Liscak R, Roth J, Ruzicka E. (2001) Functional magnetic resonance imaging during deep brain stimulation: a pilot study in four patients with Parkinson's disease. Mov Disord. 16:1126-1132.
42. Jech R. (2002) Effects of deep brain stimulation of the STN and Vim nuclei inder resting state and during simple movement task. A functional MRI study at 1.5 Tesla. Mov Disord. 17:S173.
43. Kiss ZHT, Mooney DM, Renaud L, Hu B. (2002) Neuronal response to local electrical stimulation in rat thalamus: physiological implications for mechanisms of deep brain stimulation. Neuroscience. 113:137-143.
44. Krack P, Fraix V, Mendes A, Benabid AL, Pollak P. (2002) Postoperative management of subthalamic nucleus stimulation for Parkinson's disease. Mov Disord. 17(suppl 3):188-197.
45. Kuncel AM, Cooper SE, Snyder EB, Montgomery EB, Grill WM. (2003) Effects of stimulus parameter combinations on tremor reduction and side effects by thalamic deep brain stimulation in essential tremor. Abstr Soc Neurosci. 29:921.15.
46. Lee DC, McIntyre CC, Grill WM. (2003) Extracellular electrical stimulation of central neurons: quantitative studies. In: Finn WE, Lopresti PG, eds. Handbook of neuroprosthetic methods. Boca Raton, FL: CRC Press,.
47. Lian J, Bikson M, Sciortino C, Stacey WC, Durand DM. (2003) Local suppression of epileptiform activity by electrical stimulation in rat hippocampus in vitro. J Physiol. 547:427-434.
48. Magarinos-Ascone C, Pazo JH, Macadar O, Buno W. (2002) High-frequency stimulation of the subthalamic nucleus silences subthalamic neurons: a possible cellular mechanism in Parkinson's disease. Neuroscience. 115:1109-1117.
49. 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.
50. McIntyre CC, Grill WM, Sherman DL, Thakor NV. (2004a) Deep brain stimulation of thalamocortical relay neurons: model-based analysis of activation and inhibition. J Neurophysiol. (in press).
51. McIntyre CC, Grill WM. (1999) Excitation of central nervous system neurons by nonuniform electric fields. Biophys J. 76:878-888.
52. McIntyre CC, Grill WM. (2002) Extracellular stimulation of central neurons: influence of stimulus waveform and frequency on neuronal output. J Neurophysiol. 88:1592-1604.
53. McIntyre CC, Grill WM. (2000) Selective microstimulation of central nervous system neurons. Ann Biomed Eng. 28:219-233.
54. McIntyre CC, Mori S, Sherman DL, Thakor NV, Vitek JL. (2004b) Electric field and stimulating influence generated by deep brain stimulation of the subthalamic nucleus. Clin Neurophysiol. (in press).
55. McIntyre CC, Richardson AG, Grill WM. (2002) Modeling the excitability of mammalian nerve fibers: influence of after potentials on the recovery cycle. J Neurophysiol. 87:995-1006.
56. McIntyre CC, Thakor NV. (2002) Uncovering the mechanisms of deep brain stimulation for Parkinson's disease through functional imaging, neural recording, and neural modeling. Crit Rev Biomed Eng. 30:249-281.
57. McNeal DR. (1976) Analysis of a model for excitation of myelinated nerve. IEEE Trans Biomed Eng. 23:329-337.
58. Meissner W, Harnack D, Paul G, Reum T, Sohr R, Morgenstern R, Kupsch A. (2002) Deep brain stimulation of subthalamic neurons increases striatal dopamine metabolism and induces contralateral circling in freely moving 6-hydroxydopamine-lesioned rats. Neurosci Lett. 328:105-108.
59. Meissner W, Harnack D, Reese R, Paul G, Reum T, Ansorge M, Kusserow H, Winter C, Morgenstern R, Kupsch A. (2003) High-frequency stimulation of the subthalamic nucleus enhances striatal dopamine release and metabolism in rats. J Neurochem. 85:601-609.
60. Montgomery EB, Baker KB. (2000) Mechanisms of deep brain stimulation and future technical developments. Neurol Res. 22:259-266.
61. Moro E, Esselink RJ, Xie J, Hommel M, Benabid AL, Pollak P. (2002) The impact on Parkinson's disease of electrical parameter settings in STN stimulation. Neurology. 59:706-713.
62. Nowak LG, Bullier J. (1998a) Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp Brain Res. 118:477-488.
63. Nowak LG, Bullier J. (1998b) Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. II. Evidence from selective inactivation of cell bodies and axon initial segments. Exp Brain Res. 118:489-500.
64. Obeso JA, Olanow CW, Rodriguez-Oroz MC, Krack P, Kumar R, Lang AE. (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.
65. O'Suilleabhain PE, Frawley W, Giller C, Dewey RB Jr. (2003) Tremor response to polarity, voltage, pulsewidth and frequency of thalamic stimulation. Neurology. 60:786-790.
66. Perlmutter JS, Mink JW, Bastian AJ, Zackowski K, Hershey T, Miyawaki E, Koller W, Videen TO. (2002) Blood flow responses to deep brain stimulation of thalamus. Neurology. 58:1388-1394.
67. Rattay F, Aberham M. (1993) Modeling axon membranes for functional electrical stimulation. IEEE Trans Biomed Eng. 40:1201-1209.
68. Rattay F. (1986) Analysis of models for external stimulation of axons. IEEE Trans Biomed Eng. 33:974-977.
69. Rattay F. (1999) The basic mechanism for the electrical stimulation of the nervous system. Neuroscience. 89:335-346.
70. Rezai AR, Finelli D, Nyenhuis JA, Hrdlicka G, Tkach J, Sharan A, Rugieri P, Stypulkowski PH, Shellock FG. (2002) Neurostimulation systems for deep brain stimulation: in vitro evaluation of magnetic resonance imaging-related heating at 1.5 tesla. J Magn Reson Imaging. 15:241-250.
71. Rezai AR, Lozano AM, Crawley AP, Joy ML, Davis KD, Kwan CL, Dostrovsky JO, Tasker RR, Mikulis DJ. (1999) Thalamic stimulation and functional magnetic resonance imaging: localization of cortical and subcortical activation with implanted electrodes. Technical note. J Neurosurg. 90:583-590.
72. Rizzone M, Lanotte M, Bergamasco B, Tavella A, Torre E, Faccani G, Melcarne A, Lopiano L. (2001) Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: effects of variation in stimulation parameters. J Neurol Neurosurg Psychiatry. 71:215-219.
73. Saint-Cyr JA, Hoque T, Pereira LC, Dostrovsky JO, Hutchison WD, Mikulis DJ, Abosch A, Sime E, Lang AE, Lozano AM. (2002) Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J Neurosurg. 97:1152-1166.
74. Salin P, Manrique C, Forni C, Kerkerian-Le Goff L. (2002) 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. J Neurosci. 15:5137-148.
75. Savasta M, Windels F, Bruet N, Bertrand A, Poupard A. (2002) Neurochemical modifications induced by high frequency stimulation of subthalamic nucleus in rats. In: Nicholson L, Faull, R, eds. The basal ganglia VII. New York: Kluwer Academic/Plenum Publishers:581-90. Advances in behavioral biology. series; vol. 52.
76. Schlatlenbrand G, Bailey P. (1959) Introduction to stereotaxis, with an atlas of the human brain.. 2nd ed. New York: Grune and Stratton, Inc.
77. Starr PA, Christine CW, Theodosopoulos PV, Lindsey N, Byrd D, Mosley A, Marks WJ. (2002) Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imaging-verified lead locations. J Neurosurg. 97:370-387.
78. Su PC, Ma Y, Fukuda M, Mentis MJ, Tseng HM, Yen RF, Liu HM, Moeller JR, Eidelberg D. (2001) Metabolic changes following subthalamotomy for advanced Parkinson's disease. Ann Neurol. 50:514-520.
79. 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. 17:1820-1830.
80. Tuch DS, Wedeen VJ, Dale AM, George JS, Belliveau JW. (2001) Conductivity tensor mapping of the human brain using diffusion tensor MR1. Proc Natl Acad Sci. 98:11697-11701.
81. Urbano FJ, Leznik E, Llinas RR. (2002) Cortical activation patterns evoked by afferent axons stimuli at different frequencies: an in vitro voltage-sensitive dye imaging study. Thalamus Rel Syst. 1:371-8.
82. Vitek JL, Giroux M. (2000) Physiology of hypokinetic and hyperkinetic movement disorders: model for dyskinesia. Ann Neurol. 47(suppl 1):S131-S140.
83. Vitek JL. (2002) Mechanisms of deep brain stimulation: excitation or inhibition. Mov Disord. 17(suppl 3):69-72.
84. Voges J, Volkmann J, Allert N, Lehrke R, Koulousakis A, Freund HJ, Sturm V. (2002) Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position. J Neurosurg. 96:269-279.
85. Volkmann J, Herzog J, Kopper F, Deuschl G. (2002) Introduction to the programming of deep brain stimulators. Mov Disord. 17(suppl 3):181-187.
86. Wang LY, Kaczmarek LK. (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature. 394:384-388.
87. Windels F, Bruet N, Poupard A, Feuerstein C, Bertrand A, Savasta M. (2003) Influence of the frequency parameter on extracellular glutamate and gamma-aminobutyric acid in substantia nigra and globus pallidus during electrical stimulation of subthalamic nucleus in rats. J Neurosci Res. 2:259-267.
88. 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.
89. 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.
90. Yelnik J, Damier P, Demeret S, Gervais D, Bardinet E, Bejjani BP, Francois C, Houeto JL, Amule I, Dormont D, Galanaud D, Pidoux B, Cornu P, Agid Y. (2003) Localization of stimulating electrodes in patients with Parkinson disease by using a three-dimensional atlas-magnetic resonance imaging coregistration method. J Neurosurg. 99:89-99.
91. Yianni J, Bain P, Giladi N, Auca M, Gregory R, Joint C, Nandi D, Stein J, Scott R, Aziz T. (2003) Globus pallidus internus deep brain stimulation for dystonic conditions: a prospective audit. Mov Disord. 18:436-442.
92. Zucker RS, Regehr WG. (2002) Short-term synaptic plasticity. Annu Rev Physiol. 64:355-405.