Therapeutic mechanisms of high-frequency stimulation in parkinson's disease and neural restoration via loop-based reinforcement

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 6, 2015, Pages E586-E595

  Santaniello, Sabato ^a,f   McCarthy, Michelle M ^b   Montgomery, Erwin B ^c   Gale, John T ^d   Kopell, Nancy ^b   Sarma, Sridevi V ^a,e  

^a Johns Hopkins University   (United States)

^b USA   (United States)

^c Greenville Neuromodulation Center   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

^e Johns Hopkins University   (United States)

^f UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Basal ganglia; Deep brain stimulation; Parkinson's disease; Reinforcement; Thalamus

Indexed keywords

ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN DEPTH STIMULATION; CORPUS STRIATUM; CRANIAL NERVE; HIGH FREQUENCY DEEP BRAIN STIMULATION; MODEL; NERVE FUNCTION; PARKINSON DISEASE; PRIORITY JOURNAL; PUTAMEN; SUBTHALAMUS; THALAMUS; BIOLOGICAL MODEL; BRAIN; COMPUTER SIMULATION; HUMAN; NERVE TRACT; PATHOPHYSIOLOGY; PROCEDURES;

ANIMALIA; PARKINSONIA;

BRAIN; COMPUTER SIMULATION; DEEP BRAIN STIMULATION; HUMANS; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; PARKINSON DISEASE;

EID: 84922673016     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1406549111     Document Type: Article

References (102)

1. The Deep-Brain Stimulation for Parkinson' s Disease Study Group (2001) Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. N Engl J Med 345(13):956-963.
2. Durif F, Lemaire JJ, Debilly B, Dordain G (2002) Long-term follow-up of globus pallidus chronic stimulation in advanced Parkinson's disease. Mov Disord 17(4):803-807.
3. Rodriguez-Oroz MC, et al. (2005) Bilateral deep brain stimulation in Parkinson's disease: A multicentre study with 4 years follow-up. Brain 128(Pt 10):2240-2249.
4. Moro E, et al. (2010) Long-term results of a multicenter study on subthalamic and pallidal stimulation in Parkinson's disease. Mov Disord 25(5):578-586.
5. Montgomery EB, Jr, Gale JT (2008) Mechanisms of action of deep brain stimulation (DBS). Neurosci Biobehav Rev 32(3):388-407.
6. McIntyre CC, Hahn PJ (2010) Network perspectives on the mechanisms of deep brain stimulation. Neurobiol Dis 38(3):329-337.
7. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12(10):366-375.
8. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13(7):281-285.
9. Benazzouz A, et 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(2):289-295.
10. Dostrovsky JO, et al. (2000) Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J Neurophysiol 84(1):570-574.
11. Kiss ZH, 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(1):137-143.
12. Magariños-Ascone C, Pazo JH, Macadar O, Bun[[ampi]tild;o W (2002) High-frequency stimulation of the subthalamic nucleus silences subthalamic neurons: A possible cellular mechanism in Parkinson's disease. Neuroscience 115(4):1109-1117.
13. Garcia L, Audin J, D'Alessandro G, Bioulac B, Hammond C (2003) Dual effect of highfrequency stimulation on subthalamic neuron activity. J Neurosci 23(25):8743-8751.
14. Filali M, Hutchison WD, Palter VN, Lozano AM, Dostrovsky JO (2004) Stimulationinduced inhibition of neuronal firing in human subthalamic nucleus. Exp Brain Res 156(3):274-281.
15. Meissner W, et al. (2005) Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 128(Pt 10):2372-2382.
16. 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(2):1150-1160.
17. 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(5): 1916-1923.
18. Montgomery EB, Jr (2006) Effects of GPi stimulation on human thalamic neuronal activity. Clin Neurophysiol 117(12):2691-2702.
19. Vitek JL, Zhang J, Hashimoto T, Russo GS, Baker KB (2012) External pallidal stimulation improves parkinsonian motor signs and modulates neuronal activity throughout the basal ganglia thalamic network. Exp Neurol 233(1):581-586.
20. Benabid AL (2003) Deep brain stimulation for Parkinson's disease. Curr Opin Neurobiol 13(6):696-706.
21. Bar-Gad I, Elias S, Vaadia E, Bergman H (2004) Complex locking rather than complete cessation of neuronal activity in the globus pallidus of a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primate in response to pallidal microstimulation. J Neurosci 24(33):7410-7419.
22. Dorval AD, et al. (2008) Deep brain stimulation reduces neuronal entropy in the MPTP-primate model of Parkinson's disease. J Neurophysiol 100(5):2807-2818.
23. Hahn PJ, et al. (2008) Pallidal burst activity during therapeutic deep brain stimulation. Exp Neurol 211(1):243-251.
24. Johnson MD, Vitek JL, McIntyre CC (2009) Pallidal stimulation that improves parkinsonian motor symptoms also modulates neuronal firing patterns in primary motor cortex in the MPTP-treated monkey. Exp Neurol 219(1):359-362.
25. McCairn KW, Turner RS (2009) Deep brain stimulation of the globus pallidus internus in the parkinsonian primate: Local entrainment and suppression of low-frequency oscillations. J Neurophysiol 101(4):1941-1960.
26. McConnell GC, So RQ, Hilliard JD, Lopomo P, Grill WM (2012) Effective deep brain stimulation suppresses low-frequency network oscillations in the basal ganglia by regularizing neural firing patterns. J Neurosci 32(45):15657-15668.
27. Santaniello S, Gale JT, Montgomery EB, Sarma SV (2010) Modeling the motor striatum under deep brain stimulation in normal and MPTP conditions. Conf Proc IEEE Eng Med Biol Soc 2010:2065-2068.
28. Santaniello S, Montgomery EB, Jr, Gale JT, Sarma SV (2012) Non-stationary discharge patterns in motor cortex under subthalamic nucleus deep brain stimulation. Front Integr Neurosci 6:35.
29. Sarma SV, et al. (2010) Using point process models to compare neural spiking activity in the subthalamic nucleus of Parkinson's patients and a healthy primate. IEEE Trans Biomed Eng 57(6):1297-1305.
30. Saxena S, Santaniello S, Montgomery EB, Jr, Gale JT, Sarma SV (2010) Point process models show temporal dependencies of basal ganglia nuclei under deep brain stimulation. Conf Proc IEEE Eng Med Biol Soc 2010:4152-4155.
31. Xu W, Russo GS, Hashimoto T, Zhang J, Vitek JL (2008) Subthalamic nucleus stimulation modulates thalamic neuronal activity. J Neurosci 28(46):11916-11924.
32. Montgomery EB, Jr, Baker KB (2000) Mechanisms of deep brain stimulation and future technical developments. Neurol Res 22(3):259-266.
33. Grill WM, Snyder AN, Miocinovic S (2004) Deep brain stimulation creates an informational lesion of the stimulated nucleus. Neuroreport 15(7):1137-1140.
34. Rubin JE, Terman D (2004) High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J Comput Neurosci 16(3):211-235.
35. Guo Y, Rubin JE, McIntyre CC, Vitek JL, Terman D (2008) Thalamocortical relay fidelity varies across subthalamic nucleus deep brain stimulation protocols in a datadriven computational model. J Neurophysiol 99(3):1477-1492.
36. Dorval AD, Kuncel AM, Birdno MJ, Turner DA, Grill WM (2010) Deep brain stimulation alleviates parkinsonian bradykinesia by regularizing pallidal activity. J Neurophysiol 104(2):911-921.
37. Agarwal R, Sarma SV (2012) The effects of DBS patterns on basal ganglia activity and thalamic relay: A computational study. J Comput Neurosci 33(1):151-167.
38. Koller WC, Pahwa R, Lyons KE, Albanese A (1999) Surgical treatment of Parkinson's disease. J Neurol Sci 167(1):1-10.
39. Agarwal R, Sarma SV (2012) Performance limitations of relay neurons. PLOS Comput Biol 8(8):e1002626.
40. McIntyre CC, Grill WM (1999) Excitation of central nervous system neurons by nonuniform electric fields. Biophys J 76(2):878-888.
41. McIntyre CC, Grill WM, Sherman DL, Thakor NV (2004) Cellular effects of deep brain stimulation: Model-based analysis of activation and inhibition. J Neurophysiol 91(4): 1457-1469.
42. Haber SN, Calzavara R (2009) The cortico-basal ganglia integrative network: The role of the thalamus. Brain Res Bull 78(2-3):69-74.
43. Canavero S, et al. (2003) Therapeutic extradural cortical stimulation for movement disorders: A review. Neurol Res 25(2):118-122.
44. Koller W, et al. (1997) High-frequency unilateral thalamic stimulation in the treatment of essential and parkinsonian tremor. Ann Neurol 42(3):292-299.
45. Montgomery EB, Jr, Huang H, Walker HC, Guthrie BL, Watts RL (2011) High-frequency deep brain stimulation of the putamen improves bradykinesia in Parkinson's disease. Mov Disord 26(12):2232-2238.
46. Stefani A, et al. (2007) Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. Brain 130(Pt 6):1596-1607.
47. Vitek JL, Hashimoto T, Peoples J, DeLong MR, Bakay RA (2004) Acute stimulation in the external segment of the globus pallidus improves parkinsonian motor signs. Mov Disord 19(8):907-915.
48. Moro E, et al. (2002) The impact on Parkinson's disease of electrical parameter settings in STN stimulation. Neurology 59(5):706-713.
49. Kuncel AM, Cooper SE, Wolgamuth BR, Grill WM (2007) Amplitude- and frequencydependent changes in neuronal regularity parallel changes in tremor with thalamic deep brain stimulation. IEEE Trans Neural Syst Rehabil Eng 15(2):190-197.
50. Kühn AA, et al. (2008) High-frequency stimulation of the subthalamic nucleus suppresses oscillatory beta activity in patients with Parkinson' s disease in parallel with improvement in motor performance. J Neurosci 28(24):6165-6173.
51. Moran A, Stein E, Tischler H, Bar-Gad I (2012) Decoupling neuronal oscillations during subthalamic nucleus stimulation in the parkinsonian primate. Neurobiol Dis 45(1):583-590.
52. Stein E, Bar-Gad I (2013) Betaoscillations in the cortico-basal ganglia loop during parkinsonism. Exp Neurol 245:52-59.
53. Baker KB, Montgomery EB, Jr, Rezai AR, Burgess R, Lüders HO (2002) Subthalamic nucleus deep brain stimulus evoked potentials: Physiological and therapeutic implications. Mov Disord 17(5):969-983.
54. Butson CR, Cooper SE, Henderson JM, Wolgamuth B, McIntyre CC (2011) Probabilistic analysis of activation volumes generated during deep brain stimulation. Neuroimage 54(3):2096-2104.
55. Johnson MD, Zhang J, Ghosh D, McIntyre CC, Vitek JL (2012) Neural targets for relieving parkinsonian rigidity and bradykinesia with pallidal deep brain stimulation. J Neurophysiol 108(2):567-577.
56. Kuriakose R, et al. (2010) The nature and time course of cortical activation following subthalamic stimulation in Parkinson's disease. Cereb Cortex 20(8):1926-1936.
57. Li Q, et al. (2012) Therapeutic deep brain stimulation in parkinsonian rats directly influences motor cortex. Neuron 76(5):1030-1041.
58. Li S, Arbuthnott GW, Jutras MJ, Goldberg JA, Jaeger D (2007) Resonant antidromic cortical circuit activation as a consequence of high-frequency subthalamic deepbrain stimulation. J Neurophysiol 98(6):3525-3537.
59. Miocinovic S, et al. (2006) Computational analysis of subthalamic nucleus and lenticular fasciculus activation during therapeutic deep brain stimulation. J Neurophysiol 96(3):1569-1580.
60. Santaniello S, Gale JT, Montgomery EB, Jr, Sarma SV (2010) Modeling the effects of deep brain stimulation on sensorimotor cortex in normal and MPTP conditions. Conf Proc IEEE Eng Med Biol Soc 2010:2081-2084.
61. Montgomery EB, Jr (2004) Dynamically coupled, high-frequency reentrant, non-linear oscillators embedded in scale-free basal ganglia-thalamic-cortical networks mediating function and deep brain stimulation effects. Nonlinear Studies 11(3): 385-422.
62. Montgomery EB, Jr (2007) Basal ganglia physiology and pathophysiology: A reappraisal. Parkinsonism Relat Disord 13(8):455-465.
63. Sommer MA (2003) The role of the thalamus in motor control. Curr Opin Neurobiol 13(6):663-670.
64. Tachibana Y, Kita H, Chiken S, Takada M, Nambu A (2008) Motor cortical control of internal pallidal activity through glutamatergic and GABAergic inputs in awake monkeys. Eur J Neurosci 27(1):238-253.
65. Nakano K, et al. (1990) Topographical projections from the thalamus, subthalamic nucleus and pedunculopontine tegmental nucleus to the striatum in the Japanese monkey, Macaca fuscata. Brain Res 537(1-2):54-68.
66. Smith Y, Hazrati LN, Parent A (1990) Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method. J Comp Neurol 294(2):306-323.
67. Hedreen JC, DeLong MR (1991) Organization of striatopallidal, striatonigral, and nigrostriatal projections in the macaque. J Comp Neurol 304(4):569-595.
68. Kreitzer AC (2009) Physiology and pharmacology of striatal neurons. Annu Rev Neurosci 32:127-147.
69. Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72(2):507-520.
70. Raz A, Vaadia E, Bergman H (2000) Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of parkinsonism. J Neurosci 20(22): 8559-8571.
71. Soares J, et al. (2004) Role of external pallidal segment in primate parkinsonism: Comparison of the effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonism and lesions of the external pallidal segment. J Neurosci 24(29): 6417-6426.
72. McCarthy MM, et al. (2011) Striatal origin of the pathologic beta oscillations in Parkinson's disease. Proc Natl Acad Sci USA 108(28):11620-11625.
73. Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ (2002) Move to the rhythm: Oscillations in the subthalamic nucleus-external globus pallidus network. TrendsNeurosci 25(10):525-531.
74. Kish LJ, Palmer MR, Gerhardt GA (1999) Multiple single-unit recordings in the striatum of freely moving animals: Effects of apomorphine and D-amphetamine in normal and unilateral 6-hydroxydopamine-lesioned rats. Brain Res 833(1):58-70.
75. Tseng KY, Kasanetz F, Kargieman L, Riquelme LA, Murer MG (2001) Cortical slow oscillatory activity is reflected in the membrane potential and spike trains of striatal neurons in rats with chronic nigrostriatal lesions. J Neurosci 21(16):6430-6439.
76. Pasquereau B, Turner RS (2011) Primary motor cortex of the parkinsonian monkey: Differential effects on the spontaneous activity of pyramidal tract-type neurons. Cereb Cortex 21(6):1362-1378.
77. Guehl D, et al. (2003) Tremor-related activity of neurons in the 'motor' thalamus: Changes in firing rate and pattern in the MPTP vervet model of parkinsonism. Eur J Neurosci 17(11):2388-2400.
78. Pessiglione M, et al. (2005) Thalamic neuronal activity in dopamine-depleted primates: Evidence for a loss of functional segregation within basal ganglia circuits. J Neurosci 25(6):1523-1531.
79. Vitek JL, Ashe J, DeLong MR, Alexander GE (1994) Physiologic properties and somatotopic organization of the primate motor thalamus. J Neurophysiol 71(4): 1498-1513.
80. Shi LH, Luo F, Woodward DJ, Chang JY (2006) Basal ganglia neural responses during behaviorally effective deep brain stimulation of the subthalamic nucleus in rats performing a treadmill locomotion test. Synapse 59(7):445-457.
81. Montgomery EB, Jr (2005) Effect of subthalamic nucleus stimulation patterns on motor performance in Parkinson's disease. Parkinsonism Relat Disord 11(3):167-171.
82. Moran RJ, et al. (2011) Alterations in brain connectivity underlying beta oscillations in Parkinsonism. PLOS Comput Biol 7(8):e1002124.
83. Grill WM, Cantrell MB, Robertson MS (2008) Antidromic propagation of action potentials in branched axons: implications for the mechanisms of action of deep brain stimulation. J Comput Neurosci 24(1):81-93.
84. Chomiak T, Hu B (2007) Axonal and somatic filtering of antidromically evoked cortical excitation by simulated deep brain stimulation in rat brain. J Physiol 579(Pt 2): 403-412.
85. So RQ, Kent AR, Grill WM (2012) Relative contributions of local cell and passing fiber activation and silencing to changes in thalamic fidelity during deep brain stimulation and lesioning: A computational modeling study. J Comput Neurosci 32(3):499-519.
86. Santaniello S, Gale JT, Montgomery EB, Jr, Sarma SV (2012) Reinforcement mechanisms in putamen during high frequency STN DBS: A point process study. Conf Proc IEEE Eng Med Biol Soc 2012:1214-1217.
87. Hahn PJ, McIntyre CC (2010) Modeling shifts in the rate and pattern of subthalamopallidal network activity during deep brain stimulation. J Comput Neurosci 28(3):425-441.
88. Pedoto G, et al. (2012) Point process modeling reveals anatomical non-uniform distribution across the subthalamic nucleus in Parkinson' s disease. Conf Proc IEEE Eng Med Biol Soc 2012:2539-2542.
89. Sarma SV, et al. (2012) The effects of cues on neurons in the basal ganglia in Parkinson's disease. Front Integr Neurosci 6:40.
90. Magnin M, Morel A, Jeanmonod D (2000) Single-unit analysis of the pallidum, thalamus and subthalamic nucleus in parkinsonian patients. Neuroscience 96(3): 549-564.
91. Molnar GF, Pilliar A, Lozano AM, Dostrovsky JO (2005) Differences in neuronal firing rates in pallidal and cerebellar receiving areas of thalamus in patients with Parkinson's disease, essential tremor, and pain. J Neurophysiol 93(6):3094-3101.
92. Nambu A, Llinás R (1994) Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol 72(3):1127-1139.
93. Sato F, Lavallée P, Lévesque M, Parent A (2000) Single-axon tracing study of neurons of the external segment of the globus pallidus in primate. J Comp Neurol 417(1): 17-31.
94. Mallet N, et al. (2012) Dichotomous organization of the external globus pallidus. Neuron 74(6):1075-1086.
95. McCarthy MM, Kopell N (2013) Deep brain stimulation control of beta oscillations through the indirect pathway: A computational study. Conf Proc Neuroscience 2013. Abstract no. 214.16/N17. Available at www.abstractsonline.com/Plan/ViewAbstract. aspx?sKey=44517c24-47c5-4d9a-9a1b-dc63f7bdb640&cKey=bbfcae08-511e-435a-9edcd05cb1e5a471& mKey=8d2a5bec-4825-4cd6-9439-b42bb151d1cf. Accessed January 9, 2015.
96. Destexhe A, Bal T, McCormick DA, Sejnowski TJ (1996) Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. J Neurophysiol 76(3):2049-2070.
97. Destexhe A, Contreras D, Steriade M (1998) Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. J Neurophysiol 79(2):999-1016.
98. Golomb D, et al. (2007) Mechanisms of firing patterns in fast-spiking cortical interneurons. PLOS Comput Biol 3(8):e156.
99. Klaus A, et al. (2011) Striatal fast-spiking interneurons: From firing patterns to postsynaptic impact. Front Syst Neurosci 5:57.
100. McCarthy MM, Brown EN, Kopell N (2008) Potential network mechanisms mediating electroencephalographic beta rhythm changes during propofol-induced paradoxical excitation. J Neurosci 28(50):13488-13504.
101. Koós T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2(5):467-472.
102. Goldberg JA, et al. (2002) Enhanced synchrony among primary motor cortex neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of Parkinson ' s disease. J Neurosci 22(11):4639-4653.