Uncovering the mechanisms of deep brain stimulation for Parkinson's disease through functional imaging, neural recording, and neural modeling

Critical Reviews in Biomedical Engineering

Volumn 30, Issue 4-6, 2002, Pages 249-281

  McIntyre, Cameron C ^a   Thakor, Nitish V ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Basal ganglia; Cable model; Field potential; fMRI; PET; Thalamus

Indexed keywords

BRAIN; MATHEMATICAL MODELS; MEDICAL IMAGING; NEUROLOGY; PATIENT TREATMENT;

DEEP BRAIN STIMULATION (DBS);

DISEASES;

BASAL GANGLION; BIOMEDICAL ENGINEERING; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CENTRAL NERVOUS SYSTEM; FUNCTIONAL ASSESSMENT; HUMAN; HYPOTHESIS; MODEL; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; OSCILLATION; PARKINSON DISEASE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; THALAMUS;

BASAL GANGLIA; BRAIN; BRAIN MAPPING; ELECTRIC STIMULATION THERAPY; HUMANS; MAGNETIC RESONANCE IMAGING; MODELS, NEUROLOGICAL; NERVE NET; NEURAL PATHWAYS; NEURONS; PARKINSON DISEASE; PROSTHESES AND IMPLANTS; THALAMUS; TOMOGRAPHY, EMISSION-COMPUTED;

EID: 0038302982     PISSN: 0278940X     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevBiomedEng.v30.i456.20     Document Type: Review

References (157)

1. Gross RE, Lozano AM. Advances in neurostimulation for movement disorders. Neurol Res 2000; 22:247-258.
2. Benabid AL, Koudsie A, Pollak P, Kahane P, Chabardes S, Hirsch E, Marescaux C, Benazzouz A. Future prospects of brain stimulation. Neurol Res 2000; 22:237-246.
3. Benazzouz A, Hallett M. Mechanism of action of deep brain stimulation. Neurology 2000; 55(Suppl 6):S13-S16.
4. Grill WM, McIntyre CC. Extracellular excitation of central neurons: implications for the mechanisms of deep brain stimulation. Thalamus Related Syst 2001; 1:269-277.
5. Dostrovsky JO, Lozano AM. Mechanisms of deep brain stimulation. Mov Disord 2002; 17 (Suppl 3):S63-S68.
6. Zonenshayn M, Mogilner AY, Rezai AR. Neurostimulation and functional brain imaging. Neurol Res 2000; 22:318-325.
7. Vitek JL. Mechanisms of deep brain stimulation: excitation or inhibition. Mov Disord 2002; 17(Suppl 3):S69-S72.
8. Benabid AL, Benazzous A, Pollak P. Mechanisms of deep brain stimulation. Mov Disord 2002; 17 (Suppl 3):S73-S74.
9. Deuschl G, Raethjen J, Baron R, Lindemann M, Wilms H, Krack P. The pathophysiology of parkinsonian tremor: a review. J Neurol 2000; 247:V33-V48.
10. Benabid AL, Koudsie A, Benazzouz A, Vercueil L, Fraix V, Chabardes S, Lebas JF, Pollak P. Deep brain stimulation of the corpus luysi (subthalamic nucleus) and other targets in Parkinson's disease. Extension to new indications such as dystonia and epilepsy. J Neurol 2001; 248(Suppl 3):III37-III47.
11. Parent A, Hazrati LN. Functional anatomy of the basal ganglia. I. The cortico-basal gangliathalamo-cortical loop. Brain Res Rev 1995; 20:91-127.
12. Bergman H, Feingold A, Nini A, Raz A, Slovin H, Abeles M, Vaadia E. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci 1998; 21:32-38.
13. Smith Y, Bevan MD, Shink E, Bolam JP. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 1998; 86:353-387.
14. McGeorge AJ, Faull RL. The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 1989; 29:503-537.
15. Kemp JM, Powell TP. The site of termination of afferent fibres in the caudate nucleus. Phil Trans R Soc Lond B Biol Sci 1971; 262:413-427.
16. Kemp JM, Powell TP. The termination of fibres from the cerebral cortex and thalamus upon dendritic spines in the caudate nucleus: a study with the Golgi method. Phil Trans R Soc Lond B Biol Sci 1971; 262:429-439.
17. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, Monsma FJ Jr, Sibley DR. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 1990; 250:1429-1432.
18. Alexander GE, Crutcher MD. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 1990; 13:266-271.
19. DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 1990; 13:281-285.
20. Parent A, Hazrati LN. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Rev 1995; 20:128-154.
21. Shink E, Bevan MD, Bolam JP, Smith Y. The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey. Neuroscience 1996; 73:335-357.
22. Chesselet MF, Delfs JM. Basal ganglia and movement disorders: an update. Trends Neurosci 1996; 19:417-422.
23. Pahapill PA, Lozano AM. The pedunculopontine nucleus and Parkinson's disease. Brain 2000; 123:1767-1783.
24. Brooks DJ. The early diagnosis of Parkinson's disease. Ann Neurol 1998; 44:S10-S18.
25. Blandini F, Nappi G, Tassorelli C, Martignoni E. Functional changes of the basal ganglia circuitry in Parkinson's disease. Prog Neurobiol 2000; 62:63-88.
26. Obeso JA, Rodriguez-Oroz MC, Rodriguez M, Lanciego JL, Artieda J, Gonzalo N, Olanow CW. Pathophysiology of the basal ganglia in Parkinson's disease. Trends Neurosci 2000; 23: S8-S19.
27. Zimmermann R, Deuschl G, Hornig A, Schulte-Monting J, Fuchs G, Lucking CH. Tremors in Parkinson's disease: symptom analysis and rating. Chn Neuropharmacol 1994; 17:303-314.
28. McAuley JH, Marsden CD. Physiological and pathological tremors and rhythmic central motor control. Brain 2000; 123:1545-1567.
29. Lenz FA, Tasker RR, Kwan HC, Schnider S, Kwong R, Murayama Y, Dostrovsky JO, Murphy JT. Single unit analysis of the human ventral thalamic nuclear group: correlation of thalamic "tremor cells" with the 3-6 Hz component of parkinsonian tremor. J Neurosci 8:754-764,1988.
30. Lenz FA, Kwan HC, Dostrovsky JO, Tasker RR, Murphy JT, Lenz YE. Single unit analysis of the human ventral thalamic nuclear group. Activity correlated with movement. Brain 1990; 113:1795-1821.
31. Lenz FA, Kwan HC, Martin RL, Tasker RR, Dostrovsky JO, Lenz YE. Single unit analysis of the human ventral thalamic nuclear group. Tremor-related activity in functionally identified cells. Brain 1994; 117:531-543.
32. Zirh TA, Lenz FA, Reich SG, Dougherty PM. Patterns of bursting occurring in thalamic cells during parkinsonian tremor. Neuroscience 1998; 83:107-121.
33. Magnin M, Morel A, Jeanmonod D. Single-unit analysis of the pallidum, thalamus and subthalamic nucleus in parkinsonian patients. Neuroscience 2000; 96:549-564.
34. Jahnsen H, Llinas R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol 349:205-226, 1984.
35. Jahnsen H, Llinas R. Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol 349:227-247, 1984.
36. Miller WC, DeLong MR. Parkinsonian symptomatology. An anatomical and physiological analysis. Ann NY Acad Sci 515:287-302, 1988.
37. Filion M, Tremblay L. Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 1991; 547:142-151.
38. Bergman H, Wichmann T, Karmon B, DeLong MR. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 1994; 72:507-520.
39. Nini A, Feingold A, Slovin H, Bergman H. Neurons in the globus pallidus do not show correlated activity in the normal monkey, but phase-locked oscillations appear in the MPTP model of parkinsonism. J Neurophysiol 1995; 74:1800-1805.
40. Boraud T, Bezard E, Bioulac B, Gross C. 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 1996; 215:17-20.
41. Raz A, Vaadia E, Bergman H. 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 2000; 20:8559-8571.
42. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO. Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity. J Neurosci 2002; 22: 2855-2861.
43. Wichmann T, Bergman H, DeLong MR. 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 1994; 72:521-530.
44. Hutchison WD, Allan RJ, Opitz H, Levy R, Dostrovsky JO, Lang AE, Lozano AM. Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson's disease. Ann Neurol 1998; 44:622-628.
45. Rodriguez MC, Guridi OJ, Alvarez L, Mewes K, Macias R, Vitek J, DeLong MR, Obeso JA. The subthalamic nucleus and tremor in Parkinson's disease. Mov Disord 1998; 13(Suppl 3): 111-118.
46. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO. High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J Neurosci 2000; 20:7766-7775.
47. Magarinos-Ascone CM, Figueiras-Mendez R, Riva-Meana C, Cordoba-Fernandez A. Subthalamic neuron activity related to tremor and movement in Parkinson's disease. EurJ Neurosci 2000; 12:2597-2607.
48. Rodriguez-Oroz MC, Rodriguez M, Guridi J, Mewes K, Chockkman V, Vitek J, DeLong MR, Obeso JA. The subthalamic nucleus in Parkinson's disease: somatotopic organization and physiological characteristics. Brain 2001; 124:1777-1790.
49. Plenz D, Kital ST. A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 1999; 400:677-682.
50. Beurrier C, Congar P, Bioulac B, Hammond C. Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. J Neurosci 1999; 19:599-609.
51. Bevan MD, Wilson CJ. Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci 1999; 19:7617-7628.
52. Obeso JA, Olanow CW, Nutt JG. Levodopa motor complications in Parkinson's disease. Trends Neurosci 2000; 23:S2-S7.
53. Obeso JA, Olanow CW, Rodriguez-Oroz MC, Krack P, Kumar R, Lang AE. Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. N Engl J Med 2001; 345:956-963.
54. Hariz MI. Pallidotomy microelectrode targeting: neurophysiology-based target refinement. Neurosurgery 2000; 47:1472-1473.
55. Benabid AL, Pollak P, Gao D, Hoffmann D, Limousin P, Gay E, Payen I, Benazzouz A. Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J Neurosurg 1996; 84:203-214.
56. Guridi J, Rodriguez-Oroz MC, Lozano AM, Moro E, Albanese A, Nuttin B, Gybels J, Ramos E, Obeso JA. Targeting the basal ganglia for deep brain stimulation in Parkinson's disease. Neurology 2000; 55(Suppl 6):21-28.
57. Zonenshayn M, Rezai AR, Mogilner AY, Beric A, Sterio D, Kelly PJ. Comparison of anatomic and neurophysiological methods for subthalamic nucleus targeting. Neurosurgery 2000; 47: 282-292.
58. Sterio D, Zonenshayn M, Mogilner AY, Rezai AR, Kiprovski K, Kelly PJ, Beric A. Neurophysiological refinement of subthalamic nucleus targeting. Neurosurgery 2002; 50:58-67.
59. Benazzouz A, Breit S, Koudsie A, Pollak P, Krack P, Benabid AL. Intraoperative microrecordings of the subthalamic nucleus in Parkinson's disease. Mov Disord 2002; 17(Suppl 3): S145-S149.
60. Schrader B, Hamel W, Weinert D, Mehdorn HM. Documentation of electrode localization. Mov Disord 2002; 17(Suppl 3):S167-S174.
61. Volkmann J, Herzog J, Kopper F, Deuschl G. Introduction to the programming of deep brain stimulators. Mov Disord 2002; 17(Suppl 3):S181-S187.
62. Rizzone M, Lanotte M, Bergamasco B, Tavella A, Torre E, Faccani G, Melcarne A, Lopiano L. Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: effects of variation in stimulation parameters. J Neurol Neurosurg Psychiatry 2001; 71:215-219.
63. McIntyre CC, Grill WM. Finite element analysis of the current-density and electric field generated by metal microelectrodes. Ann Biomed Eng 2001; 29:227-235.
64. McCreery DB, Agnew WF, Yuen TG, Bullara L. Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation. IEEE Trans Biomed Eng 1990; 37: 996-1001.
65. Haberler C, Alesch F, Mazal PR, Pilz P, Jellinger K, Pinter MM, Hainfellner JA, Budka H. No tissue damage by chronic deep brain stimulation in Parkinson's disease. Ann Neurol 2000; 48: 372-376.
66. Henderson JM, Pell M, O'Sullivan DJ, McCusker EA, Fung VS, Hedges P, Halliday GM. Postmortem analysis of bilateral subthalamic electrode implants in Parkinson's disease. Mov Disord 2002; 17:133-137.
67. McIntyre CC, Grill WM, Sherman DL, Thakor NV. Model-based analysis of deep brain stimulation of the thalamus. Proc 24th Int Conf IEEE-EMBS, Houston, TX.
68. Basser PJ, Roth BJ. New currents in electrical stimulation of excitable tissues. Annu Rev Biomed Eng 2000; 2:377-397.
69. Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, Perret JE, de Rougemont J. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 1991; 337:403-406.
70. Holsheimer J, Demeulemeester H, Nuttin B, and De Sutter P. Identification of the target neuronal elements in electrical deep brain stimulation. Eur J Neurosci 2000; 12:4573-4577.
71. Benabid AL, Pollak P, Louveau A, Henry S, de Rougemont J. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol 50:344-346, 1987.
72. Koller W, Pahwa R, Busenbark K, Hubble J, Wilkinson S, Lang A, Tuite P, Sime E, Lazano A, Hauser R, Malapira T, Smith D, Tarsy D, Miyawaki E, Norregaard T, Kormos T, Olanow CW. High-frequency unilateral thalamic stimulation in the treatment of essential and parkinsonian tremor. Ann Neurol 1997; 42:292-299.
73. Limousin P, Speelman JD, Gielen F, Janssens M. Multicentre European study of thalamic stimulation in parkinsonian and essential tremor. J Neurol Neurosurg Psychiatry 1999; 66: 289-296.
74. Laitinen LV, Bergenheim AT, Hariz MI. Leksell's posteroventral pallidotomy in the treatment of Parkinson's disease. J Neurosurg 76:53-61, 1992.
75. Siegfried J, Lippitz B. Bilateral chronic electrostimulation of ventroposterolateral pallidum: a new therapeutic approach for alleviating all parkinsonian symptoms. Neurosurgery 1994; 35: 1126-1129.
76. Ghika J, Villemure JG, Fankhauser H, Favre J, Assal G, Ghika-Schmid F. Efficiency and safety of bilateral contemporaneous pallidal stimulation (deep brain stimulation) in levodopa-responsive patients with Parkinson's disease with severe motor fluctuations: a 2-year follow-up review. J Neurosurg 1998; 89:713-718.
77. Siegfried J, Taub E, Wellis GN. Long-term electrostimulation of the ventroposterolateral pallidum in the treatment of Parkinson's disease. Adv Neurol 1999; 80:623-626.
78. Durif F, Lemaire JJ, Debilly B, Dordain G. Acute and chronic effects of anteromedial globus pallidus stimulation in Parkinson's disease. J Neurol Neurosurg Psychiatry 1999; 67:315-322.
79. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Broussolle E, Perret JE, Benabid AL. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 1995; 345:91-95.
80. Alegret M, Junque C, Valldeoriola F, Vendrell P, Pilleri M, Rumia J, Tolosa E. Effects of bilateral subthalamic stimulation on cognitive function in Parkinson disease. Arch Neurol 2001; 58: 1223-1227.
81. Perozzo P, Rizzone M, Bergamasco B, Castelli L, Lanotte M, Tavella A, Torre E, Lopiano L. Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: comparison of pre- and postoperative neuropsychological evaluation. J Neurol Sci 2001; 192:9-15.
82. Raichle ME. Cognitive neuroscience. Bold insights. Nature 2001; 412:128-130.
83. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001; 412:150-157.
84. Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Nad Acad Sci USA 1990; 87:9868-9872.
85. Phelps ME. Positron emission tomography provides molecular imaging of biological processes. Proc Nad Acad Sci USA 2000; 97:9226-9233.
86. Jacobs RE, Cherry SR. Complementary emerging techniques: high-resolution PET and MRI. Curr Opin Neurobiol 2001; 11:621-629.
87. Rees G, Friston K, Koch C. A direct quantitative relationship between the functional properties of human and macaque V5. Nat Neurosci 2000; 3:716-723.
88. Friston KJ, Mechelli A, Turner R, Price CJ. Nonlinear responses in fMRI: the Balloon model, Volterra kernels, and other hemodynamics. Neuroimage 2000; 12:466-477.
89. Mechelli A, Price CJ, Friston KJ. Nonlinear coupling between evoked rCBF and BOLD signals: a simulation study of hemodynamic responses. Neuroimage 2001; 14:862-872.
90. Mintun MA, Lundstrom BN, Snyder AZ, Vlassenko AG, Shulman GL, Raichle ME. Blood flow and oxygen delivery to human brain during functional activity: theoretical modeling and experimental data. Proc Natl Acad Sci USA 2001; 98:6859-6864.
91. Shulman RG, Hyder F, Rothman DL, Shulman RG, Hyder F, Rothman DL. Cerebral energetics and the glycogen shunt: neurochemical basis of functional imaging. Proc Natl Acad Sci USA 2001; 98:6417-6422.
92. Tagamets MA, Horwitz B. Interpreting PET and fMRI measures of functional neural activity: the effects of synaptic inhibition on cortical activation in human imaging studies. Brain Res Bull 2001; 54:267-273.
93. Arthurs OJ, Boniface S. How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci 2002; 25:27-31.
94. Mathiesen C, Caesar K, Akgoren N, Lauritzen M. Modification of activity-dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex. J Physiol 1998; 512:555-566.
95. Deiber MP, Pollak P, Passingham R, Landais P, Gervason C, Cinotti L, Friston K, Frackowiak R, Mauguiere F, Benabid AL. Thalamic stimulation and suppression of parkinsonian tremor. Evidence of a cerebellar deactivation using positron emission tomography. Brain 1993; 116: 267-279.
96. Rezai AR, Lozano AM, Crawley AP, Joy ML, Davis KD, Kwan CL, Dostrovsky JO, Tasker RR, Mikulis DJ. Thalamic stimulation and functional magnetic resonance imaging: localization of cortical and subcortical activation with implanted electrodes. Technical note. J Neurosurg 1999; 90:583-590.
97. Ceballos-Baumann AO, Boecker H, Fogel W, Alesch F, Bartenstein P, Conrad B, Diederich N, von Falkenhayn I, Moringlane JR, Schwaiger M, Tronnier VM. Thalamic stimulation for essential tremor activates motor and deactivates vestibular cortex. Neurology 2001; 56:1347-1354.
98. Davis KD, Taub E, Houle S, Lang AE, Dostrovsky JO, Tasker RR, Lozano AM. Globus pallidus stimulation activates the cortical motor system during alleviation of parkinsonian symptoms. Nat Med 1997; 3:671-674.
99. Fukuda M, Mentis M, Ghilardi MF, Dhawan V, Antonini A, Hammerstad J, Lozano AM, Lang A, Lyons K, Koller W, Ghez C, Eidelberg D. Functional correlates of pallidal stimulation for Parkinson's disease. Ann Neurol 2001; 49:155-164.
100. Fukuda M, Mentis MJ, Ma Y, Dhawan V, Antonini A, Lang AE, Lozano AM, Hammerstad J, Lyons K, Koller WC, Moeller JR, Eidelberg D. Networks mediating the clinical effects of pallidal brain stimulation for Parkinson's disease: a PET study of resting-state glucose metabolism. Brain 2001; 124:1601-1609.
101. Limousin P, Greene J, Pollak P, Rothwell J, Benabid AL, Frackowiak R. Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease. Ann Neurol 1997; 42:283-291.
102. Ceballos-Baumann AO, Boecker H, Bartenstein P, von Falkenhayn I, Riescher H, Conrad B, Moringlane JR, Alesch F. A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch Neurol 1999; 56:997-1003.
103. Jech R, Urgosik D, Tintera J, Nebuzelsky A, Krasensky J, Liscak R, Roth J, Ruzicka E. Functional magnetic resonance imaging during deep brain stimulation: a pilot study in four patients with Parkinson's disease. Mov Disord 2001; 16:1126-1132.
104. Antonini A, Kazumata K, Feigin A, Mandel F, Dhawan V, Margouleff C, Eidelberg D. Differential diagnosis of parkinsonism with [18F]fluorodeoxyglucose and PET. Mov Disord 1998; 13:268-274.
105. Benazzouz A, Piallat B, Pollak P, Benabid AL. Responses of substantia nigra pars reticulata and globus pallidus complex to high frequency stimulation of the subthalamic nucleus in rats: electrophysiological data. Neurosci Lett 1995; 189:77-80.
106. Benazzouz A, Gao DM, Ni ZG, Piallat B, Bouali-Benazzouz R, Benabid AL. 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 2000; 99:289-295.
107. Dostrovsky JO, Levy R, Wu JP, Hutchison WD, Tasker RR, Lozano AM. Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J Neurophysiol 2000; 84: 570-574.
108. Wu YR, Levy R, Ashby P, Tasker RR, Dostrovsky JO. Does stimulation of the GPi control dyskinesia by activating inhibitory axons? Mov Disord 2001; 16:208-216.
109. Hashimoto T, Elder CM, Vitek JL. A template subtraction method for stimulus artifact removal in high-frequency deep brain stimulation. J Neurosci Methods 2002; 113:181-186.
110. 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.
111. 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.
112. Hashimoto T, Elder CM, DeLong MR, Vitek JL. Responses of pallidal neurons to electrical stimulation of the subthalamic nucleus in experimental parkinsonism. Soc Neurosci Abstr.
113. Sterio D, Rezai A, Mogilner A, Zonenshayn M, Gracies JM, Kathirithamby K, Beric A. Neurophysiological modulation of the subthalamic nucleus by pallidal stimulation in Parkinson's disease. J Neurol Neurosurg Psychiatry 2002; 72:325-328.
114. Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 1975; 98:417-440.
115. Gustafsson B, Jankowska E. Direct and indirect activation of nerve cells by electrical pulses applied extracellularly. J Physiol 1976; 258:33-61.
116. Nowak LG, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp Brain Res 1998; 118:477-488.
117. Nowak LG, Bullier J. 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 1998; 118:489-500.
118. McNeal DR. Analysis of a model for excitation of myelinated nerve. IEEE Trans Biomed Eng 1976; 23:329-337.
119. Rattay F. Analysis of models for external stimulation of axons. IEEE Trans Biomed Eng 1986; 33:974-977.
120. Rattay F. Analysis of models for extracellular fiber stimulation. IEEE Trans Biomed Eng 1989; 36:676-682.
121. Rattay F, Aberham M. Modeling axon membranes for functional electrical stimulation. IEEE Trans Biomed Eng 1993; 40:1201-1209.
122. Rijkhoff NJ, Holsheimer J, Koldewijn EL, Struijk JJ, van Kerrebroeck PE, Debruyne FM, Wijkstra H. Selective stimulation of sacral nerve roots for bladder control: a study by computer modeling. IEEE Trans Biomed Eng 1994; 41:413-424.
123. Frijns JH, de Snoo SL, ten Kate JH. Spatial selectivity in a rotationally symmetric model of the electrically stimulated cochlea. Hear Res 1996; 95:33-48.
124. Choi AQ, Cavanaugh JK, Durand DM. Selectivity of multiple-contact nerve cuff electrodes: a simulation analysis. IEEE Trans Biomed Eng 2001; 48:165-172.
125. Rall W, Burke RE, Holmes WR, Jack JJ, Redman SJ, Segev I. Matching dendritic neuron models to experimental data. Physiol Rev 1992; 72(Suppl 4):S159-S186.
126. Rattay F. Analysis of the electrical excitation of CNS neurons. IEEE Trans Biomed Eng 1998; 45:766-772.
127. Rattay F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 1999; 89:335-346.
128. Greenberg RJ, Velte TJ, Humayun MS, Scarlatis GN, de Juan E Jr. A computational model of electrical stimulation of the retinal ganglion cell. IEEE Trans Biomed Eng 1999; 46: 505-514.
129. McIntyre CC, Grill WM. Excitation of central nervous system neurons by nonuniform electric fields. Biophys J 1999; 76:878-888.
130. McIntyre CC, Grill WM. Selective microstimulation of central nervous system neurons. Ann Biomed Eng 28:219-233, 2000.
131. McIntyre CC, Grill WM. Extracellular stimulation of central neurons: influence of stimulus waveform and frequency on neuronal output. J Neurophysiol 2002; 88:1592-1604.
132. Baldissera F, Lundberg A, Udo M. Stimulation of pre- and postsynaptic elements in the red nucleus. Exp Brain Res 15:151-167, 1972.
133. Montgomery EB Jr, Baker KB. Mechanisms of deep brain stimulation and future technical developments. Neurol Res 2000; 22:259-266.
134. Tass PA. Desynchronizing double-pulse phase resetting and application to deep brain stimulation. Biol Cybernet 2001; 85:343-354.
135. Titcombe MS, Glass L, Guehl D, Beuter A. Dynamics of parkinsonian tremor during deep brain stimulation. Chaos 2001; 11:766-773.
136. Bikson M, Lian J, Hahn PJ, Stacey WC, Sciortino C, Durand DM. Suppression of epilepti-form activity by high frequency sinusoidal fields in rat hippocampal slices. J Physiol 2001; 531: 181-191.
137. Beurrier C, Bioulac B, Audin J, Hammond C. High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J Neurophysiol 2001; 85: 1351-1356.
138. Nakanishi H, Kita H, Kitai ST. Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res 437:45-55, 1987.
139. Pape HC, McCormick DA. Electrophysiological and pharmacological properties of interneurons in the cat dorsal lateral geniculate nucleus. Neuroscience 1995; 68:1105-1125.
140. Oertel WH, Mugnaini E. Immunocytochemical studies of GABAergic neurons in rat basal ganglia and their relations to other neuronal systems. Neurosci Lett 1984; 47:233-238.
141. Shink E, Smith Y. 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 1995; 358:119-141.
142. Ashby P, Kim YJ, Kumar R, Lang AE, Lozano AM. Neurophysiological effects of stimulation through electrodes in the human subthalamic nucleus. Brain 1999; 122:1919-1931.
143. Miles R, Wong RK. Unitary inhibitory synaptic potentials in the guinea-pig hippocampus in vitro. J Physiol 1984; 356:97-113.
144. Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J Neurosci 2001; 21:1033-1038.
145. Wang LY, Kaczmarek LK. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 1998; 394:384-388.
146. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 2002; 64:355-405.
147. Kumar R, Dagher A, Hutchison WD, Lang AE, Lozano AM. Globus pallidus deep brain stimulation for generalized dystonia: clinical and PET investigation. Neurology 1999; 53: 871-874.
148. Vercueil L, Pollak P, Fraix V, Caputo E, Moro E, Benazzouz A, Xie J, Koudsie A, Benabid AL. Deep brain stimulation in the treatment of severe dystonia. J Neurol 2001; 248:695-700.
149. Krauss JK, Loher TJ, Pohle T, Weber S, Taub E, Barlocher CB, Burgunder JM. Pallidal deep brain stimulation in patients with cervical dystonia and severe cervical dyskinesias with cervical myelopathy. J Neurol Neurosurg Psychiatry 2002; 72:249-256.
150. Ghika J, Villemure JG, Miklossy J, Temperli P, Pralong E, Christen-Zaech S, Pollo C, Maeder P, Bogousslavsky J, Vingerhoets F. Postanoxic generalized dystonia improved by bilateral Voa thalamic deep brain stimulation. Neurology 2002; 58:311-313.
151. Joel D. Deep brain stimulation in Huntington's disease: globus pallidus externus or substantia nigra pars compacta. Mov Disord 2002; 17:431-432.
152. Nuttin B, Cosyns P, Demeulemeester H, Gybels J, Meyerson B. Electrical stimulation in anterior limbs of internal capsules in patients with obsessive-compulsive disorder. Lancet 1999; 354: 1526.
153. Velasco F, Velasco M, Jimenez F, Velasco AL, Brito F, Rise M, Carrillo-Ruiz JD. Predictors in the treatment of difficult-to-control seizures by electrical stimulation of the centromedian thalamic nucleus. Neurosurgery 2000; 47:295-304.
154. Depaulis A, Vergnes M, Marescaux C. Endogenous control of epilepsy: the nigral inhibitory system. Prog Neurobiol 1994; 42:33-52.
155. Vercueil L, Benazzouz A, Deransart C, Bressand K, Marescaux C, Depaulis A, Benabid AL. High-frequency stimulation of the subthalamic nucleus suppresses absence seizures in the rat: comparison with neurotoxic lesions. Epilepsy Res 1998; 31:39-46.
156. Loddenkemper T, Pan A, Neme S, Baker KB, Rezai AR, Dinner DS, Montgomery EB Jr, Luders HO. Deep brain stimulation in epilepsy. J Clin Neurophysiol 2001; 18:514-532.
157. Mirski MA, Rossell LA, Terry JB, Fisher RS. Anticonvulsant effect of anterior thalamic high frequency electrical stimulation in the rat. Epilepsy Res 1997; 28:89-100.