Mechanisms of Action of Deep Brain Stimulation: A Review

Neuromodulation

Volumn 1, Issue , 2009, Pages 157-169

  Lee, Kendall H ^a   Blaha, Charles D ^b   Bledsoe, Jonathan M ^a  

^a MAYO CLINIC   (United States)

^b University of Memphis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79551503825     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-374248-3.00016-1     Document Type: Chapter

References (128)

1. A. Abosch, S. Kapur, A.E. Lang, D. Hussey, E. Sime, J. Miyasaki, et al. (2003) Stimulation of the subthalamic nucleus in Parkinson’s disease does not produce striatal dopamine release. Neurosurgery 53 1095-1102. discussion 1102–5
2. R.L. Albin, A.B. Young and J.B. Penney (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci. 12 366-375.
3. R.L. Albin, A.B. Young and J.B. Penney (1995) The functional anatomy of disorders of the basal ganglia. Trends Neurosci. 18 63-64.
4. M.E. Anderson, N. Postupna and M. Ruffo (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.
5. T. Bal and D.A. McCormick (1993) Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker. J. Physiol. 468 669-691.
6. T. Bal, M. Krosigk M. von and D.A. McCormick (1995) Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. J. Physiol. 483(Pt 3), 641-663.
7. T. Bal, M. Krosigk M. von. and D.A. McCormick (1995) Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro. J. Physiol. 483(Pt 3), 665-685.
8. J. Baufreton, J.F. Atherton, D.J. Surmeier and M.D. Bevan (2005) Enhancement of excitatory synaptic integration by GABAergic inhibition in the subthalamic nucleus. J. Neurosci. 25 8505-8517.
9. A.L. Benabid (2003) Deep brain stimulation for Parkinson’s disease. Curr. Opin. Neurobiol. 13 696-706.
10. A.L. Benabid, P.P. Krack, A. Benazzouz, P. Limousin, A. Koudsie and P. Pollak (2000) Deep brain stimulation of the subthalamic nucleus for Parkinson’s disease: methodologic aspects and clinical criteria. Neurology 55 S40-S44.
11. A.L. Benabid, P. Pollak, D. Gao, D. Hoffmann, P. Limousin, E. Gay, I. Payen and A. Benazzouz (1996) Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J. Neurosurg. 84 203-214.
12. A.L. Benabid, P. Pollak, C. Gross, D. Hoffmann, A. Benazzouz, D.M. Gao, A. Laurent, M. Gentil and J. Perret (1994) Acute and long-term effects of subthalamic nucleus stimulation in Parkinson’s disease. Stereotact. Funct. Neurosurg. 62 76-84.
13. A.L. Benabid, P. Pollak, A. Louveau, S. Henry and J. de Rougemont (1987) Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl. Neurophysiol. 50 344-346.
14. A. Benazzouz and M. Hallett (2000) Mechanism of action of deep brain stimulation. Neurology 55 S13-S16.
15. A. Benazzouz, D. Gao, Z. Ni and A.L. Benabid (2000) High frequency stimulation of the STN influences the activity of dopamine neurons in the rat. Neuroreport 11 1593-1596.
16. A. Benazzouz, B. Piallat, P. Pollak and A.L. Benabid (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.
17. H. Bergman, T. Wichmann and M.R. DeLong (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249 1436-1438.
18. H. Bergman, T. Wichmann, B. Karmon and M.R. DeLong (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 72 507-520.
19. B.P. Bergstrom and P.A. Garris (1999) Utility of a tripolar stimulating electrode for eliciting dopamine release in the rat striatum. J. Neurosci. Methods, 87 201-208.
20. C. Beurrier, B. Bioulac, J. Audin and C. Hammond (2001) High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J. Neurophysiol. 85 1351-1356.
21. M.D. Bevan and C.J. Wilson (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J. Neurosci. 19 7617-7628.
22. M.D. Bevan, P.J. Magill, N.E. Hallworth, J.P. Bolam and C.J. Wilson (2002) Regulation of the timing and pattern of action potential generation in rat subthalamic neurons in vitro by GABA-A IPSPs. J. Neurophysiol. 87 1348-1362.
23. M.D. Bevan, P.J. Magill, D. Terman, J.P. Bolam and C.J. Wilson (2002) Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci. 25 525-531.
24. R.G. Bittar, I. Kar-Purkayastha, S.L. Owen, R.E. Bear, A. Green, S. Wang and T.Z. Aziz (2005) Deep brain stimulation for pain relief: a meta-analysis. J. Clin. Neurosci. 12 515-519.
25. C.D. Blaha and A.G. Phillips (1996) A critical assessment of electrochemical procedures applied to the measurement of dopamine and its metabolites during drug-induced and species-typical behaviours. Behav. Pharmacol. 7 675-708.
26. P. Boon, K. Vonck, V. De Herdt, A. Van Dycke, M. Goethals, L. Goossens, et al. (2007) Deep brain stimulation in patients with refractory temporal lobe epilepsy. Epilepsia 48 1551-1560.
27. T. Boraud, E. Bezard, B. Bioulac and C. Gross (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.
28. P. Brown and D. Williams (2005) Basal ganglia local field potential activity: character and functional significance in the human. Clin. Neurophysiol. 116 2510-2519.
29. P. Brown, A. Kupsch, P.J. Magill, A. Sharott, D. Harnack and W. Meissner (2002) Oscillatory local field potentials recorded from the subthalamic nucleus of the alert rat. Exp. Neurol. 177 581-585.
30. N. Bruet, F. Windels, A. Bertrand, C. Feuerstein, A. Poupard and M. Savasta (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.
31. N. Bruet, F. Windels, C. Carcenac, C. Feuerstein, A. Bertrand, A. Poupard and M. Savasta (2003) Neurochemical mechanisms induced by high frequency stimulation of the subthalamic nucleus: increase of extracellular striatal glutamate and GABA in normal and hemiparkinsonian rats. J. Neuropathol. Exp. Neurol. 62 1228-1240.
32. M.B. Carpenter, S.C. Carleton, J.T. Keller and P. Conte (1981) Connections of the subthalamic nucleus in the monkey. Brain Res. 224 1-29.
33. DBS-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.
34. G. Deuschl, C. Schade-Brittinger, P. Krack, J. Volkmann, H. Schafer, K. Botzel, et al. (2006) A randomized trial of deep-brain stimulation for Parkinson’s disease. N. Engl. J. Med. 355 896-908.
35. J.O. Dostrovsky, R. Levy, J.P. Wu, W.D. Hutchison, R.R. Tasker and A.M. Lozano (2000) Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J. Neurophysiol. 84 570-574.
36. C. Dugast, M.F. Suaud-Chagny and F. Gonon (1994) Continuous in vivo monitoring of evoked dopamine release in the rat nucleus accumbens by amperometry. Neuroscience 62 647-654.
37. M. Filali, W.D. Hutchison, V.N. Palter, A.M. Lozano and J.O. Dostrovsky (2004) Stimulation-induced inhibition of neuronal firing in human subthalamic nucleus. Exp. Brain Res. 156 274-281.
38. G.L. Forster and C.D. Blaha (2003) Pedunculopontine tegmental stimulation evokes striatal dopamine efflux by activation of acetylcholine and glutamate receptors in the midbrain and pons of the rat. Eur. J. Neurosci. 17 751-762.
39. K. Fujimoto and H. Kita (1993) Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res. 609 185-192.
40. Gale, J., Lee, K., Amirnovin, R., Roberts, D., Williams, Z., Blaha, C. and Eskandar, E. (2008) Local stimulation-evoked dopamine release in the primate caudate putamen: evidence for the role of dopamine in plasticity. Submitted for publication.
41. L. Garcia, J. Audin, G. D’Alessandro, B. Bioulac and C. Hammond (2003) Dual effect of high-frequency stimulation on subthalamic neuron activity. J. Neurosci. 23 8743-8751.
42. P.A. Garris, M. Kilpatrick, M.A. Bunin, D. Michael, Q.D. Walker and R.M. Wightman (1999) Dissociation of dopamine release in the nucleus accumbens from intracranial self-stimulation. Nature 398 67-69.
43. A. Gillies, D. Willshaw and Z. Li (2002) Subthalamic-pallidal interactions are critical in determining normal and abnormal functioning of the basal ganglia. Proc. Biol. Sci. 269 545-551.
44. B.D. Greenberg, D.A. Malone, G.M. Friehs, A.R. Rezai, C.S. Kubu, P.F. Malloy, et al. (2006) Three-year outcomes in deep brain stimulation for highly resistant obsessive–compulsive disorder. Neuropsychopharmacology 31 2384-2396.
45. C. Hamani, J.A. Saint-Cyr, J. Fraser, M. Kaplitt and A.M. Lozano (2004) The subthalamic nucleus in the context of movement disorders. Brain 127 4-20.
46. C. Hammond, J.M. Deniau, A. Rizk and J. Feger (1978) Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat. Brain Res. 151 235-244.
47. D.E. Hardesty and H.A. Sackeim (2007) Deep brain stimulation in movement and psychiatric disorders. Biol. Psychiatry, 61 831-835.
48. T. Hashimoto, C.M. Elder, M.S. Okun, S.K. Patrick and J.L. Vitek (2003) Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J. Neurosci. 23 1916-1923.
49. O.K. Hassani, C. Francois, J. Yelnik and J. Feger (1997) Evidence for a dopaminergic innervation of the subthalamic nucleus in the rat. Brain Res. 749 88-94.
50. J. Herzog, U. Fietzek, W. Hamel, A. Morsnowski, F. Steigerwald, B. Schrader, et al. (2004) Most effective stimulation site in subthalamic deep brain stimulation for Parkinson’s disease. Mov. Disord. 19 1050-1054.
51. R. Hilker, J. Voges, M. Ghaemi, R. Lehrke, J. Rudolf, A. Koulousakis, et al. (2003) Deep brain stimulation of the subthalamic nucleus does not increase the striatal dopamine concentration in parkinsonian humans. Mov. Disord. 18 41-48.
52. M. Hodaie, R.A. Wennberg, J.O. Dostrovsky and A.M. Lozano (2002) Chronic anterior thalamus stimulation for intractable epilepsy. Epilepsia 43 603-608.
53. Y. Iribe, K. Moore, K.C. Pang and J.M. Tepper (1999) Subthalamic stimulation-induced synaptic responses in substantia nigra pars compacta dopaminergic neurons in vitro. J. Neurophysiol. 82 925-933.
54. Y. Kang and T. Futami (1999) Arrhythmic firing in dopamine neurons of rat substantia nigra evoked by activation of subthalamic neurons. J. Neurophysiol. 82 1632-1637.
55. U. Kim, T. Bal and D.A. McCormick (1995) Spindle waves are propagating synchronized oscillations in the ferret LGNd in vitro. J. Neurophysiol. 74 1301-1323.
56. H. Kita and S.T. Kitai (1987) Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J. Comp. Neurol. 260 435-452.
57. H. Kita, H.T. Chang and S.T. Kitai (1983) Pallidal inputs to subthalamus: intracellular analysis. Brain Res. 264 255-265.
58. S.T. Kitai and J.M. Deniau (1981) Cortical inputs to the subthalamus: intracellular analysis. Brain Res. 214 411-415.
59. M. Krosigk M.von, T. Bal and D.A. McCormick (1993) Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261 361-364.
60. M. Laruelle (2000) Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. J. Cereb. Blood Flow Metabol. 20 423-451.
61. K.H. Lee and D.A. McCormick (1996) Abolition of spindle oscillations by serotonin and norepinephrine in the ferret lateral geniculate and perigeniculate nuclei in vitro. Neuron 17 309-321.
62. K.H. Lee and D.A. McCormick (1997) Modulation of spindle oscillations by acetylcholine, cholecystokinin and 1S,3R-ACPD in the ferret lateral geniculate and perigeniculate nuclei in vitro. Neuroscience 77 335-350.
63. K.H. Lee, C.D. Blaha, B.T. Harris, S. Cooper, F.L. Hitti, J.C. Leiter, D.W. Roberts and U. Kim (2006) Dopamine efflux in the rat striatum evoked by electrical stimulation of the subthalamic nucleus: potential mechanism of action in Parkinson’s disease. Eur. J. Neurosci. 23 1005-1014.
64. K.H. Lee, C. Broberger, U. Kim and D.A. McCormick (2004) Histamine modulates thalamocortical activity by activating a chloride conductance in ferret perigeniculate neurons. Proc. Natl Acad. Sci. U S A 101 6716-6721.
65. K.H. Lee, S.Y. Chang, D.W. Roberts and U. Kim (2004) Neurotransmitter release from high-frequency stimulation of the subthalamic nucleus. J. Neurosurg. 101 511-517.
66. K.H. Lee, F.L. Hitti, M.H. Shalinsky, U. Kim, J.C. Leiter and D.W. Roberts (2005) Abolition of spindle oscillations and 3-Hz absence seizurelike activity in the thalamus by using high-frequency stimulation: potential mechanism of action. J. Neurosurg. 103 538-545.
67. K.H. Lee, K. Kristic, R. van Hoff, F.L. Hitti, C. Blaha, B. Harris, et al. (2007) High-frequency stimulation of the subthalamic nucleus increases glutamate in the subthalamic nucleus of rats as demonstrated by in vivo enzyme-linked glutamate sensor. Brain Res. 1162 121-219.
68. F.A. Lenz, C.J. Jaeger, M.S. Seike, Y.C. Lin and S.G. Reich (2002) Single-neuron analysis of human thalamus in patients with intention tremor and other clinical signs of cerebellar disease. J. Neurophysiol. 87 2084-2094.
69. F.A. Lenz, J.L. Vitek and M.R. DeLong (1993) Role of the thalamus in parkinsonian tremor: evidence from studies in patients and primate models. Stereotact. Funct. Neurosurg. 60 94-103.
70. R. Levy, W.D. Hutchison, A.M. Lozano and J.O. Dostrovsky (2000) High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J. Neurosci. 20 7766-7775.
71. R. Levy, A.E. Lang, J.O. Dostrovsky, P. Pahapill, J. Romas, J. Saint-Cyr, et al. (2001) Lidocaine and muscimol microinjections in subthalamic nucleus reverse Parkinsonian symptoms. Brain 124 2105-2118.
72. N. Lipsman, J.S. Neimat and A.M. Lozano (2007) Deep brain stimulation for treatment-refractory obsessive-compulsive disorder: the search for a valid target. Neurosurgery 61 1-11. discussion 11–13
73. A.M. Lozano (2000) Vim thalamic stimulation for tremor. Arch. Med. Res. 31 266-269.
74. A.M. Lozano and H. Eltahawy (2004) How does DBS work? Clin. Neurophysiol. 57(Suppl), 733-736.
75. R.J. Maciunas, B.N. Maddux, D.E. Riley, C.M. Whitney, M.R. Schoenberg, P.J. Ogrocki, et al. (2007) Prospective randomized double-blind trial of bilateral thalamic deep brain stimulation in adults with Tourette syndrome. J. Neurosurg. 107 1004-1014.
76. C. Magarinos-Ascone, J.H. Pazo, O. Macadar and W. Buno (2002) High-frequency stimulation of the subthalamic nucleus silences subthalamic neurons: a possible cellular mechanism in Parkinson’s disease. Neuroscience 115 1109-1117.
77. N. Maurice, J.M. Deniau, J. Glowinski and A.M. Thierry (1998) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J. Neurosci. 18 9539-9546.
78. N. Maurice, J.M. Deniau, A. Menetrey, J. Glowinski and A.M. Thierry (1998) Prefrontal cortex-basal ganglia circuits in the rat: involvement of ventral pallidum and subthalamic nucleus. Synapse 29 363-370.
79. N. Maurice, A.M. Thierry, J. Glowinski and J.M. Deniau (2003) Spontaneous and evoked activity of substantia nigra pars reticulata neurons during high-frequency stimulation of the subthalamic nucleus. J. Neurosci. 23 9929-9936.
80. H.S. Mayberg, A.M. Lozano, V. Voon, H.E. McNeely, D. Seminowicz, C. Hamani, et al. (2005) Deep brain stimulation for treatment-resistant depression. Neuron 45 651-660.
81. P. Mazzone (2003) Deep brain stimulation in Parkinson’s disease: bilateral implantation of globus pallidus and subthalamic nucleus. J. Neurosurg. Sci. 47 47-51.
82. P. Mazzone, A. Lozano, P. Stanzione, S. Galati, E. Scarnati, A. Peppe and A. Stefani (2005) Implantation of human pedunculopontine nucleus: a safe and clinically relevant target in Parkinson’s disease. Neuroreport 16 1877-1881.
83. D.A. McCormick and H.R. Feeser (1990) Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39 103-113.
84. C.C. McIntyre and N.V. Thakor (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.
85. C.C. McIntyre, W.M. Grill, D.L. Sherman and N.V. Thakor (2004) Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J. Neurophysiol. 91 1457-1469.
86. C.C. McIntyre, M. Savasta, B.L. Walter and J.L. Vitek (2004) How does deep brain stimulation work? Present understanding and future questions. J. Clin. Neurophysiol. 21 40-50.
87. C.C. McIntyre, M. Savasta, L. Kerkerian-Le Goff and J.L. Vitek (2004) Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin. Neurophysiol. 115 1239-1248.
88. W. Meissner, C. Guigoni, L. Cirilli, M. Garret, B.H. Bioulac, C.E. Gross, et al. (2007) Impact of chronic subthalamic high-frequency stimulation on metabolic basal ganglia activity: a 2-deoxyglucose uptake and cytochrome oxidase mRNA study in a macaque model of Parkinson’s disease. Eur. J. Neurosci. 25 1492-1500.
89. W. Meissner, D. Harnack, G. Paul, T. Reum, R. Sohr, R. Morgenstern and A. Kupsch (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.
90. W. Meissner, D. Harnack, R. Reese, G. Paul, T. Reum, M. Ansorge, et al. (2003) High-frequency stimulation of the subthalamic nucleus enhances striatal dopamine release and metabolism in rats. J. Neurochem. 85 601-609.
91. W. Meissner, A. Leblois, D. Hansel, B. Bioulac, C.E. Gross, A. Benazzouz and T. Boraud (2005) Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 128 2372-2382.
92. W. Meissner, T. Reum, G. Paul, D. Harnack, R. Sohr, R. Morgenstern and A. Kupsch (2001) Striatal dopaminergic metabolism is increased by deep brain stimulation of the subthalamic nucleus in 6-hydroxydopamine lesioned rats. Neurosci. Lett. 303 165-168.
93. I. Mintz, C. Hammond, B. Guibert and V. Leviel (1986) Stimulation of the subthalamic nucleus enhances the release of dopamine in the rat substantia nigra. Brain Res. 376 406-408.
94. E.B. Montgomery Jr. and K.B. Baker (2000) Mechanisms of deep brain stimulation and future technical developments. Neurol. Res. 22 259-266.
95. A. Nambu, H. Tokuno, I. Hamada, H. Kita, M. Imanishi, T. Akazawa, et al. (2000) Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J. Neurophysiol. 84 289-300.
96. T. Nimura, K. Yamaguchi, T. Ando, S. Shibuya, T. Oikawa, A. Nakagawa, et al. (2005) Attenuation of fluctuating striatal synaptic dopamine levels in patients with Parkinson disease in response to subthalamic nucleus stimulation: a positron emission tomography study. J. Neurosurg. 103 968-973.
97. P.A. Pahapill, R. Levy, J.O. Dostrovsky, K.D. Davis, A.R. Rezai, R.R. Tasker and A.M. Lozano (1999) Tremor arrest with thalamic microinjections of muscimol in patients with essential tremor. Ann. Neurol. 46 249-252.
98. A. Parent and L.N. Hazrati (1995) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res. Brain Res. Rev. 20 128-154.
99. A. Parent and L.N. Hazrati (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Brain Res. Rev. 20 91-127.
100. A. Parent and Y. Smith (1987) Organization of efferent projections of the subthalamic nucleus in the squirrel monkey as revealed by retrograde labeling methods. Brain Res. 436 296-310.
101. G. Paul, T. Reum, W. Meissner, A. Marburger, R. Sohr, R. Morgenstern, et al. (2000) High frequency stimulation of the subthalamic nucleus influences striatal dopaminergic metabolism in the naive rat. Neuroreport 11 441-444.
102. J.S. Perlmutter and J.W. Mink (2006) Deep brain stimulation. Annu. Rev. Neurosci. 29 229-257.
103. D. Plenz, M. Herrera-Marschitz and S.T. Kitai (1998) Morphological organization of the globus pallidus-subthalamic nucleus system studied in organotypic cultures. J. Comp. Neurol. 397 437-457.
104. L. Prensa, M. Cossette and A. Parent (2000) Dopaminergic innervation of human basal ganglia. J. Chem. Neuroanat. 20 207-213.
105. D. Rasche, P.C. Rinaldi, R.F. Young and V.M. Tronnier (2006) Deep brain stimulation for the treatment of various chronic pain syndromes. Neurosurg. Focus, 21 E8.
106. P. Robledo and J. Feger (1990) Excitatory influence of rat subthalamic nucleus to substantia nigra pars reticulata and the pallidal complex: electrophysiological data. Brain Res. 518 47-54.
107. M.G. Rosales, G. Flores, S. Hernandez, D. Martinez-Fong and J. Aceves (1994) Activation of subthalamic neurons produces NMDA receptor-mediated dendritic dopamine release in substantia nigra pars reticulata: a microdialysis study in the rat. Brain Res. 645 335-337.
108. J.A. Saint-Cyr, T. Hoque, L.C. Pereira, J.O. Dostrovsky, W.D. Hutchison, D.J. Mikulis, et al. (2002) Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J. Neurosurg. 97 1152-1156.
109. P. Salin, C. Manrique, C. Forni and L. Kerkerian-Le Goff (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. 22 5137-5148.
110. F. Sato, M. Parent, M. Levesque and A. Parent (2000) Axonal branching pattern of neurons of the subthalamic nucleus in primates. J. Comp. Neurol. 424 142-152.
111. T.E. Schlaepfer, M.X. Cohen, C. Frick, M. Kosel, D. Brodesser, N. Axmacher, et al. (2008) Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 33 368-377.
112. D. Schonfuss, T. Reum, P. Olshausen, T. Fischer and R. Morgenstern (2001) Modelling constant potential amperometry for investigations of dopaminergic neurotransmission kinetics in vivo. J. Neurosci. Methods, 112 163-172.
113. I.D. Smith and A.A. Grace (1992) Role of the subthalamic nucleus in the regulation of nigral dopamine neuron activity. Synapse 12 287-303.
114. Y. Smith and A. Parent (1988) Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity. Brain Res. 453 353-356.
115. O.C. Snead 3rd (1995) Basic mechanisms of generalized absence seizures. Ann. Neurol. 37 146-157.
116. C.H. Tai, T. Boraud, E. Bezard, B. Bioulac, C. Gross and A. Benazzouz (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.
117. Y. Temel, A. Blokland, H.W. Steinbusch and V. Visser-Vandewalle (2005) The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog. Neurobiol. 76 393-413.
118. E.Y. Uc and K.A. Follett (2007) Deep brain stimulation in movement disorders. Semin. Neurol. 27 170-182.
119. F.J. Urbano, E. Leznik and R.R. Llinas (2002) Cortical activation patterns evoked by afferent axons stimuli at different frequencies: an in vitro voltage sensitive dye imaging study. Thalamus Rel. Syst. 1 371-378.
120. B.J. Venton, K.P. Troyer and R.M. Wightman (2002) Response times of carbon fiber microelectrodes to dynamic changes in catecholamine concentration. Anal. Chem. 74 539-546.
121. J. Volkmann (2004) Deep brain stimulation for the treatment of Parkinson’s disease. J. Clin. Neurophysiol. 21 6-17.
122. N.D. Volkow, J.S. Fowler, G.J. Wang, S.L. Dewey, D. Schlyer, R. MacGregor, et al. (1993) Reproducibility of repeated measures of carbon-11-raclopride binding in the human brain. J. Nucl. Med. 34 609-613.
123. K. Vonck, P. Boon and D. Van Roost (2007) Anatomical and physiological basis and mechanism of action of neurostimulation for epilepsy. Acta Neurochir. 97(Suppl), 328-333.
124. L.Y. Wang and L.K. Kaczmarek (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394 384-388.
125. M. Weinberger, N. Mahant, W.D. Hutchison, A.M. Lozano, E. Moro, M. Hodaie, et al. (2006) Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson’s disease. J. Neurophysiol. 96 3248-3256.
126. T. Wichmann, H. Bergman and M.R. DeLong (1994) The primate subthalamic nucleus. I. Functional properties in intact animals. J. Neurophysiol. 72 494-506.
127. F. Windels, N. Bruet, A. Poupard, C. Feuerstein, A. Bertrand and M. Savasta (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. 72 259-267.
128. R.S. Zucker and W.G. Regehr (2002) Short-term synaptic plasticity. Annu. Rev. Physiol. 64 355-405.