Latest view on the mechanism of action of deep brain stimulation

Movement Disorders

Volumn 23, Issue 15, 2008, Pages 2111-2121

  Hammond, Constance ^a   Ammari, Rachida ^a,b   Bioulac, Bernard ^b   Garcia, Liliana ^b  

^a INSERM   (France)

^b UMR 5287   (France)

Author keywords

Antidromic spikes; DBS; Dystonia; Electrophysiology; OCD; Parkinson

Indexed keywords

LEVODOPA;

ANTIDROMIC STIMULATION; BASAL GANGLION; BRAIN DEPTH STIMULATION; CELL ACTIVATION; CELL PROTECTION; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; DRUG DOSE REDUCTION; DRUG MECHANISM; DYSTONIA; EVOKED BRAIN STEM RESPONSE; HUMAN; MOLECULAR MECHANICS; NERVE CELL NETWORK; NERVE CELL STIMULATION; NEUROLOGIC DISEASE; NEUROPROTECTION; NOCICEPTIVE STIMULATION; NONHUMAN; OBSESSIVE COMPULSIVE DISORDER; OUTCOME ASSESSMENT; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SENSORY NERVE CONDUCTION; SUBTHALAMIC NUCLEUS; THALAMOCORTICAL TRACT;

BRAIN; DEEP BRAIN STIMULATION; HUMANS; NERVOUS SYSTEM DISEASES; NEURONS;

EID: 61449264860     PISSN: 08853185     EISSN: 15318257     Source Type: Journal    
DOI: 10.1002/mds.22120     Document Type: Review

References (88)

1. Hassler R, Riechert T, Mundinger F, Umbach W, Ganglberger JA. Physiological observations in stereotaxic operations in extrapyramidal motor disturbances. Brain 1960;83:337-350.
2. Benabid AL, Pollak P, Gervason C, et al. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 1991;337:403-406.
3. Limousin P, Pollak P, Benazzouz A, et al. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 1995;345:91-95.
4. Benabid AL, Deuschl G, Lang AE, Lyons KE, Rezai AR. Deep brain stimulation for Parkinson's disease. Mov Disord 2006;21 (Suppl 14):S168-S170.
5. Rezai AR, Kopell BH, Gross RE, et al. Deep brain stimulation for Parkinson's disease: surgical issues. Mov Disord 2006;21 (Suppl 14):S197-S218.
6. 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.
7. Coubes P, Cif L, El FH, et al. Electrical stimulation of the globus pallidus internus in patients with primary generalized dystonia: long-term results. J Neurosurg 2004;101:189-194.
8. Aouizerate B, Cuny E, Martin-Guehl C, et al. Deep brain stimulation of the ventral caudate nucleus in the treatment of obsessive-compulsive disorder and major depression. Case report. J Neurosurg 2004;101:682-686.
9. Lipsman N, Neimat JS, Lozano AM. Deep brain stimulation for treatment-refractory obsessive-compulsive disorder: the search for a valid target. Neurosurgery 2007;61:1-11.
10. Houeto JL, Karachi C, Mallet L, et al. Tourette's syndrome and deep brain stimulation. J Neurol Neurosurg Psychiatry 2005;76: 992-995.
11. Visser-Vandewalle V. DBS in Tourette syndrome: rationale, current status and future prospects. Acta Neurochir Suppl 2007;97 (Part 2):215-222.
12. Ressler KJ, Mayberg HS. Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nat Neurosci 2007;10:1116-1124.
13. Priori A, Foffani G, Pesenti A, et al. Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease. Exp Neurol 2004;189:369-379.
14. 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.
15. Sharott A, Magill PJ, Harnack D, Kupsch A, Meissner W, Brown P. Dopamine depletion increases the power and coherence of β-oscillations in the cerebral cortex and subthalamic nucleus of the awake rat. Eur J Neurosci 2005;21:1413-1422.
16. Gatev P, Darbin O, Wichmann T. Oscillations in the basal ganglia under normal conditions and in movement disorders. Mov Disord 2006;21:1566-1577.
17. Uhlhaas PJ, Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 2006;52:155-168.
18. Hammond C, Bergman H, Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci 2007;30:357-364.
19. McIntyre CC, Grill WM. Excitation of central nervous system neurons by nonuniform electric fields. Biophys J 1999;76:878-888.
20. Montgomery EB, Jr, Baker KB. Mechanisms of deep brain stimulation and future technical developments. Neurol Res 2000;22: 259-266.
21. Windels F, Bruet N, Poupard A, et al. 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.
22. Garcia L, Audin J, D'Alessandro G, Bioulac B, Hammond C. Dual effect of high-frequency stimulation on subthalamic neuron activity. J Neurosci 2003;23:8743-8751.
23. Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci 2003;23:1916-1923.
24. McCracken CB, Grace AA. High-frequency deep brain stimulation of the nucleus accumbens region suppresses neuronal activity and selectively modulates afferent drive in rat orbitofrontal cortex in vivo. J Neurosci 2007;27:12601-12610.
25. Bolam JP, Hanley JJ, Booth PA, Bevan MD. Synaptic organisation of the basal ganglia. J Anat 2000;196 (Part 4):527-542.
26. Luscher C, Nicoll RA, Malenka RC, Muller D. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 2000;3:545-550.
27. Rizzone M, Lanotte M, Bergamasco B, et al. 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.
28. Kuncel AM, Grill WM. Selection of stimulus parameters for deep brain stimulation. Clin Neurophysiol 2004;115:2431-2441.
29. Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 1975; 98:417-440.
30. Holsheimer J, Dijkstra EA, Demeulemeester H, Nuttin B. Chronaxie calculated from current-duration and voltage-duration data. J Neurosci Methods 2000;97:45-50.
31. Wallace BA, Ashkan K, Heise CE, et al. Survival of midbrain dopaminergic cells after lesion or deep brain stimulation of the subthalamic nucleus in MPTP-treated monkeys. Brain 2007;130 (Part 8):2129-2145.
32. Haberler C, Alesch F, Mazal PR, et al. No tissue damage by chronic deep brain stimulation in Parkinson's disease. Ann Neurol 2000;48:372-376.
33. Tai CH, Boraud T, Bezard E, Bioulac B, Gross C, Benazzouz A. 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 2003;17:1820-1830.
34. Meissner W, Leblois A, Hansel D, et al. Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 2005;128 (Part 10):2372-2382.
35. Filali M, Hutchison WD, Palter VN, Lozano AM, Dostrovsky JO. Stimulation-induced inhibition of neuronal firing in human subthalamic nucleus. Exp Brain Res 2004;156:274-281.
36. Welter ML, Houeto JL, Bonnet AM, et al. Effects of high-frequency stimulation on subthalamic neuronal activity in Parkinsonian patients. Arch Neurol 2004;61:89-96.
37. Li S, Arbuthnott GW, Jutras MJ, Goldberg JA, Jaeger D. Resonant antidromic cortical circuit activation as a consequence of high-frequency subthalamic deep-brain stimulation. J Neurophysiol 2007;98:3525-3537.
38. Maurice N, Thierry AM, Glowinski J, Deniau JM. Spontaneous and evoked activity of substantia nigra pars reticulata neurons during high-frequency stimulation of the subthalamic nucleus. J Neurosci 2003;23:9929-9936.
39. Montgomery EB, Jr. Effects of GPi stimulation on human thalamic neuronal activity. Clin Neurophysiol 2006;117:2691-2702.
40. Garcia L, D'Alessandro G, Fernagut PO, Bioulac B, Hammond C. The impact of high frequency stimulation parameters on the pattern of discharge of subthalamic neurons. J Neurophysiol 2005; 94:3662-3669.
41. 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.
42. McIntyre CC, Grill WM, Sherman DL, Thakor NV. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J Neurophysiol 2004;91:1457-1469.
43. Chomiak T, Hu B. Axonal and somatic filtering of antidromically evoked cortical excitation by simulated deep brain stimulation in rat brain. J Physiol 2007;579 (Part 2):403-412.
44. Canteras NS, Shammah-Lagnado SJ, Silva BA, Ricardo JA. Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res 1990;513:43-59.
45. Baker KB, Montgomery EB, Jr, Rezai AR, Burgess R, Luders HO. Subthalamic nucleus deep brain stimulus evoked potentials: physiological and therapeutic implications. Mov Disord 2002;17: 969-983.
46. Cowan RL, Wilson CJ. Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 1994;71:17-32.
47. Grill WM, Cantrell MB, Robertson MS. Antidromic propagation of action potentials in branched axons: implications for the mechanisms of action of deep brain stimulation. J Comput Neurosci 2008;24:81-93.
48. Sadek AR, Magill PJ, Bolam JP. A single-cell analysis of intrinsic connectivity in the rat globus pallidus. J Neurosci 2007;27: 6352-6362.
49. Mailly P, Charpier S, Menetrey A, Deniau JM. Three-dimensional organization of the recurrent axon collateral network of the substantia nigra pars reticulata neurons in the rat. J Neurosci 2003;23:5247-5257.
50. Hammond C, Rouzaire-Dubois B, Féger J, Jackson A, Crossman AR. Anatomical and electrophysiological studies on the reciprocal projections between the subthalamic nucleus and nucleus tegmenti pedunculopontinus in the rat. Neuroscience 1983;9:41-52.
51. Florio T, Scarnati E, Confalone G, et al. High-frequency stimulation of the subthalamic nucleus modulates the activity of pedunculopontine neurons through direct activation of excitatory fibres as well as through indirect activation of inhibitory pallidal fibres in the rat. Eur J Neurosci 2007;25:1174-1186.
52. Kita H, Tachibana Y, Nambu A, Chiken S. Balance of monosynaptic excitatory and disynaptic inhibitory responses of the globus pallidus induced after stimulation of the subthalamic nucleus in the monkey. J Neurosci 2005;25:8611-8619.
53. Galati S, Mazzone P, Fedele E, et al. Biochemical and electrophysiological changes of substantia nigra pars reticulata driven by subthalamic stimulation in patients with Parkinson's disease. Eur J Neurosci 2006;23:2923-2928.
54. Maltete D, Jodoin N, Karachi C, et al. Subthalamic stimulation and neuronal activity in the substantia nigra in Parkinson's disease. J Neurophysiol 2007;97:4017-4022.
55. Temel Y, Visser-Vandewalle V, Kaplan S, et al. Protection of nigral cell death by bilateral subthalamic nucleus stimulation. Brain Res 2006;1120:100-105.
56. Welter ML, Houeto JL, Tezenas du MS, et al. Clinical predictive factors of subthalamic stimulation in Parkinson's disease. Brain 2002;125 (Part 3):575-583.
57. Moro E, Scerrati M, Romito LM, Roselli R, Tonali P, Albanese A. Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson's disease. Neurology 1999;53:85-90.
58. Lacombe E, Carcenac C, Boulet S, et al. High-frequency stimulation of the subthalamic nucleus prolongs the increase in striatal dopamine induced by acute l-3,4-dihydroxyphenylalanine in dopaminergic denervated rats. Eur J Neurosci 2007;26:1670-1680.
59. Meissner W, Harnack D, Reese R, et al. High-frequency stimulation of the subthalamic nucleus enhances striatal dopamine release and metabolism in rats. J Neurochem 2003;85:601-609.
60. Lee KH, Chang SY, Roberts DW, Kim U. Neurotransmitter release from high-frequency stimulation of the subthalamic nucleus. J Neurosurg 2004;101:511-517.
61. Stefani A, Lozano AM, Peppe A, et al. Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. Brain 2007;130 (Part 6):1596-1607.
62. Bar-Gad I, Elias S, Vaadia E, Bergman H. 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 2004; 24:7410-7419.
63. Degos B, Deniau JM, Thierry AM, Glowinski J, Pezard L, Maurice N. Neuroleptic-induced catalepsy: electrophysiological mechanisms of functional recovery induced by high-frequency stimulation of the subthalamic nucleus. J Neurosci 2005;25:7687-7696.
64. Hariz MI, Krack P, Alesch F, et al. Multicentre European study of thalamic stimulation for Parkinsonian tremor, a 6-year follow-up. J Neurol Neurosurg Psychiatry (in press).
65. Deuschl G, Bergman H. Pathophysiology of nonparkinsonian tremors. Mov Disord 2002;17 (Suppl 3):S41-S48.
66. Anderson T, Hu B, Pittman Q, Kiss ZH. Mechanisms of deep brain stimulation: an intracellular study in rat thalamus. J Physiol 2004;559 (Part 1):301-313.
67. Anderson TR, Hu B, Iremonger K, Kiss ZH. Selective attenuation of afferent synaptic transmission as a mechanism of thalamic deep brain stimulation-induced tremor arrest. J Neurosci 2006; 26:841-850.
68. Bekar L, Libionka W, Tian GF, et al. Adenosine is crucial for deep brain stimulation-mediated attenuation of tremor. Nat Med 2008;14:75-80.
69. Lozano AM, Kumar R, Gross RE, et al. Globus pallidus internus pallidotomy for generalized dystonia. Mov Disord 1997;12:865-870.
70. Wichmann T, Bergman H, Starr PA, Subramanian T, Watts RL, DeLong MR. Comparison of MPTP-induced changes in spontaneous neuronal discharge in the internal pallidal segment and in the substantia nigra pars reticulata in primates. Exp Brain Res 1999;125:397-409.
71. Zhuang P, Li Y, Hallett M. Neuronal activity in the basal ganglia and thalamus in patients with dystonia. Clin Neurophysiol 2004; 115:2542-2557.
72. Tang JK, Moro E, Mahant N, et al. Neuronal firing rates and patterns in the globus pallidus internus of patients with cervical dystonia differ from those with Parkinson's disease. J Neurophysiol 2007;98:720-729.
73. Kupsch A, Benecke R, Muller J, et al. Pallidal deep-brain stimulation in primary generalized or segmental dystonia. N Engl J Med 2006;355:1978-1990.
74. Vidailhet M, Vercueil L, Houeto JL, et al. Bilateral, pallidal, deep-brain stimulation in primary generalised dystonia: a prospective 3 year follow-up study. Lancet Neurol 2007;6:223-229.
75. Anderson ME, Postupna N, Ruffo M. Effects of high-frequency stimulation in the internal globus pallidus on the activity of thalamic neurons in the awake monkey. J Neurophysiol 2003;89: 1150-1160.
76. Baxter LR, Jr, Phelps ME, Mazziotta JC, Guze BH, Schwartz JM, Selin CE. Local cerebral glucose metabolic rates in obsessive-compulsive disorder. A comparison with rates in unipolar depression and in normal controls. Arch Gen Psychiatry 1987;44: 211-218.
77. Swedo SE, Schapiro MB, Grady CL, et al. Cerebral glucose metabolism in childhood-onset obsessive-compulsive disorder. Arch Gen Psychiatry 1989;46:518-523.
78. Saxena S, Brody AL, Schwartz JM, Baxter LR. Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder. Br J Psychiatry Suppl 1998;35:26-37.
79. Guehl D, Benazzouz A, Aouizerate B, et al. Neuronal correlates of obsessions in the caudate nucleus. Biol Psychiatry 2008;63: 557-562.
80. 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.
81. Mallet L, Schupbach M, N'Diaye K, et al. Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior. Proc Natl Acad Sci USA 2007;104:10661-10666.
82. Montgomery EB, Jr, Gale JT. Mechanisms of action of deep brain stimulation (DBS). Neurosci Biobehav Rev 2008;32:388-407.
83. 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.
84. Windels F, Bruet N, Poupard A, Feuerstein C, Bertrand A, Savasta M. Influence of the frequency parameter on extracellular glutamate and γ-aminobutyric acid in substantia nigra and globus pallidus during electrical stimulation of subthalamic nucleus in rats. J Neurosci Res 2003;72:259-267.
85. Windels F, Carcenac C, Poupard A, Savasta M. Pallidal origin of GABA release within the substantia nigra pars reticulata during high-frequency stimulation of the subthalamic nucleus. J Neurosci 2005;25:5079-5086.
86. Lee KH, Kristic K, van HR, et al. 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 2007;1162:121-129.
87. Meissner W, Guigoni C, Cirilli L, et al. 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 2007;25:1492-1500.
88. Oueslati A, Sgambato-Faure V, Melon C, et al. High-frequency stimulation of the subthalamic nucleus potentiates L-dopa-induced neurochemical changes in the striatum in a rat model of Parkinson's disease. J Neurosci 2007;27:2377-2386.