Deep brain stimulation alleviates parkinsonian bradykinesia by regularizing pallidal activity

Journal of Neurophysiology

Volumn 104, Issue 2, 2010, Pages 911-921

  Dorval, Alan D ^a,c   Kuncel, Alexis M ^a   Birdno, Merrill J ^a   Turner, Dennis A ^b   Grill, Warren M ^a,b  

^a Duke University   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c Department of Electrical and Computer Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBIDOPA; LEVODOPA;

ADULT; AGED; ARTICLE; BASAL GANGLION; BRADYKINESIA; BRAIN DEPTH STIMULATION; CELL STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GLOBUS PALLIDUS; HUMAN; MALE; NERVE CELL; PARKINSONISM; PRIORITY JOURNAL; THALAMUS NUCLEUS;

ACTION POTENTIALS; AGED; AGED, 80 AND OVER; ANALYSIS OF VARIANCE; BASAL GANGLIA; COMPUTER SIMULATION; DEEP BRAIN STIMULATION; FEMALE; GLOBUS PALLIDUS; HUMANS; HYPOKINESIA; MALE; MEMBRANE POTENTIALS; MIDDLE AGED; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; NEURONS; PARKINSON DISEASE; THALAMUS;

EID: 77955961457     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00103.2010     Document Type: Article

References (49)

1. 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 89: 1150-1160, 2003. (Pubitemid 36210899)
2. Anderson TR, Hu B, Iremonger K, Kiss ZHT. Selective attenuation of afferent synaptic transmission as a mechanism of thalamic deep brain stimulation-induced tremor arrest. J Neurosci 26: 841-850, 2006.
3. 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 24: 7410-7419, 2004.
4. Bergman H, Wichmann T, Karmon B, DeLong MR. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72: 507-520, 1994. (Pubitemid 24273560)
5. Beurrier C, Bioulac B, Audin J, Hammond C. High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J Neurophysiol 85: 1351-1356, 2001.
6. Birdno MJ, Cooper SE, Rezai AR, Grill WM. Pulse-to-pulse changes in the frequency of deep brain stimulation affect tremor and modeled neuronal activity. J Neurophysiol 98: 1675-1684, 2007.
7. Birdno MJ, Grill WM. Mechanisms of deep brain stimulation in movement disorders as revealed by changes in stimulus frequency. Neurotherapeutics 5: 14-25, 2008.
8. Birdno MJ, Kuncel AM, Dorval AD, Turner DA, Grill WM. Tremor varies as a function of the temporal regularity of deep brain stimulation. Neuroreport 19: 599-602, 2008. (Pubitemid 351501475)
9. 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 215: 17-20, 1996.
10. Brown P, Mazzone P, Oliviero A, Altibrandi MG, Pilato F, Tonali PA, Di Lazzaro V. Effects of stimulation of the subthalamic area on oscillatory pallidal activity in Parkinson's disease. Exp Neurol 188: 480-490, 2004.
11. Degos B, Deniau J, Thierry A, 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 25: 7687-7696, 2005. (Pubitemid 41170625)
12. Dorval AD. Probability distributions of the logarithm of inter-spike intervals yield accurate entropy estimates from small datasets. J Neurosci Methods 173: 129-139, 2008.
13. Dorval AD, Russo GS, Hashimoto T, Xu W, Grill WM, Vitek JL. Deep brain stimulation reduces neuronal entropy in the MPTP-primate model of Parkinson's disease. J Neurophysiol 100: 2807-2818, 2008.
14. Feng X, Shea-Brown E, Greenwald B, Kosut R, Rabitz H. Optimal deep brain stimulation of the subthalamic nucleus-a computational study. J Comput Neurosci 23: 265-282, 2007.
15. Filali M, Hutchison WD, Palter VN, Lozano AM, Dostrovsky JO. Stimulation-induced inhibition of neuronal firing in human subthalamic nucleus. Exp Brain Res 156: 274-281, 2004.
16. Garcia L, D'Alessandro G, Bioulac B, Hammond C. High-frequency stimulation in Parkinson's disease: more or less? Trends Neurosci 28: 209-216, 2005. (Pubitemid 40445528)
17. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science 324: 354-359, 2009.
18. Grill WM, McIntyre CC. Extracellular excitation of central neurons: implications for the mechanisms of deep brain stimulation. Thalamus Relat Syst 1: 269-277, 2001.
19. Grill WM, Snyder AN, Miocinovic S. Deep brain stimulation creates an informational lesion of the stimulated nucleus. Neuroreport 15: 1137-1140, 2004.
20. Guo Y, Rubin JE, McIntyre CC, Vitek JL, Terman D. Thalamocortical relay fidelity varies across subthalamic nucleus deep brain stimulation protocols in a data-driven computational model. J Neurophysiol 99: 1477-1492, 2008.
21. Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci 23: 1916-1923, 2003.
22. Hauptmann C, Popovych O, Tass PA. Effectively desynchronizing deep brain stimulation based on a coordinated delayed feedback stimulation via several sites: a computational study. Biol Cybern 93: 463-470, 2005.
23. Hershey T, Revilla FJ, Wernle AR, McGee-Minnich L, Antenor JV, Videen TO, Dowling JL, Mink JW, Perlmutter JS. Cortical and subcortical blood flow effects of subthalamic nucleus stimulation in PD. Neurology 61: 816-821, 2003.
24. Kuncel AM, Cooper SE, Wolgamuth BR, Grill WM. Amplitude- and frequency-dependent changes in neuronal regularity parallel changes in tremor with thalamic deep brain stimulation. IEEE Trans Neural Syst Rehabil Eng 15: 190-197, 2007. (Pubitemid 46957036)
25. Legéndy CR, Salcman M. Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons. J Neurophysiol 53: 926-939, 1985.
26. 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 117: 531-543, 1994.
27. 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 98: 3525-3537, 2007.
28. Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA 96: 15222-15227, 1999.
29. Lopiano L, Torre E, Benedetti F, Bergamasco B, Perozzo P, Pollo A, Rizzone M, Tavella A, Lanotte M. Temporal changes in movement time during the switch of the stimulators in Parkinson's disease patients treated by subthalamic nucleus stimulation. Eur Neurol 50: 94-99, 2003. (Pubitemid 37116970)
30. Magnin M, Morel A, Jeanmonod D. Single-unit analysis of the pallidum, thalamus and subthalamic nucleus in parkinsonian patients. Neuroscience 96: 549-564, 2000.
31. McIntyre CC, Grill WM, Sherman DL, Thakor NV. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J Neurophysiol 91: 1457-1469, 2004.
32. Meissner W, Leblois A, Hansel D, Bioulac B, Gross CE, Benazzouz A, Boraud T. Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 128: 2372-2382, 2005. (Pubitemid 41407976)
33. Montgomery EB. Effect of subthalamic nucleus stimulation patterns on motor performance in Parkinson's disease. Parkinsonism Relat. Disord 11: 167-171, 2005.
34. Okun MS, Vitek JL. Lesion therapy for Parkinson's disease and other movement disorders: update and controversies. Mov Disord 19: 375-389, 2004.
35. Phillips MD, Baker KB, Lowe MJ, Tkach JA, Cooper SE, Kopell BH, Rezai AR. Parkinson disease: pattern of functional MR imaging activation during deep brain stimulation of subthalamic nucleus-initial experience. Radiology 239: 209-216, 2006.
36. Rubin JE, Terman D. High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J Comput Neurosci 16: 211-235, 2004.
37. Shi L, Luo F, Woodward DJ, Chang J. Basal ganglia neural responses during behaviorally effective deep brain stimulation of the subthalamic nucleus in rats performing a treadmill locomotion test. Synapse 59: 445-457, 2006.
38. Soares J, Kliem MA, Betarbet R, Greenamyre JT, Yamamoto B, Wichmann T. 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: 6417-6426, 2004.
39. Stefani A, Fedele E, Galati S, Pepicelli O, Frasca S, Pierantozzi M, Peppe A, Brusa L, Orlacchio A, Hainsworth AH, Gattoni G, Stanzione P, Bernardi G, Raiteri M, Mazzone P. Subthalamic stimulation activates internal pallidus: evidence from cGMP microdialysis in PD patients. Ann Neurol 57: 448-452, 2005.
40. Tang JKH, Moro E, Lozano AM, Lang AE, Hutchison WD, Mahant N, Dostrovsky JO. Firing rates of pallidal neurons are similar in Huntington's and Parkinson's disease patients. Exp Brain Res 166: 230-236, 2005. (Pubitemid 41406814)
41. Tass PA. A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations. Biol Cybern 89: 81-88, 2003.
42. Tass PA, Silchenko AN, Hauptmann C, Barnikol UB, Speckmann E. Long-lasting desynchronization in rat hippocampal slice induced by coordinated reset stimulation. Phys Rev E Stat Nonlin Soft Matter Phys 80: 011902, 2009.
43. Tavares ALT, Jefferis GSXE, Koop M, Hill BC, Hastie T, Heit G, Bronte-Stewart HM. Quantitative measurements of alternating finger tapping in Parkinson's disease correlate with UPDRS motor disability and reveal the improvement in fine motor control from medication and deep brain stimulation. Mov Disord 20: 1286-1298, 2005.
44. Temperli P, Ghika J, Villemure J, Burkhard PR, Bogousslavsky J, Vingerhoets FJG. How do parkinsonian signs return after discontinuation of subthalamic DBS? Neurology 60: 78-81, 2003.
45. Terman D, Rubin JE, Yew AC, Wilson CJ. Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J Neurosci 22: 2963-2976, 2002. (Pubitemid 37465845)
46. Vitek JL. Mechanisms of deep brain stimulation: excitation or inhibition. Mov Disord 17 Suppl 3: S69-72, 2002.
47. Wichmann T, DeLong MR. Pathophysiology of Parkinson's disease: the MPTP primate model of the human disorder. Ann NY Acad Sci 991: 199-213, 2003.
48. Wichmann T, Soares J. Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in parkinsonism. J Neurophysiol 95: 2120-2133, 2006.
49. Windels F, Bruet N, Poupard A, Feuerstein C, Bertrand A, Savasta M. 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, 2003.