Effective deep brain stimulation suppresses low-frequency network oscillations in the basal ganglia by regularizing neural firing patterns

Journal of Neuroscience

Volumn 32, Issue 45, 2012, Pages 15657-15668

  McConnell, George C ^a   So, Rosa Q ^a   Hilliard, Justin D ^a   Lopomo, Paola ^a   Grill, Warren M ^a,b  

^a Duke University   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HALOPERIDOL; METHAMPHETAMINE; OXIDOPAMINE;

AKINESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; BASAL GANGLION; BRAIN DEPTH STIMULATION; CELL LOSS; CIRCLING BEHAVIOR; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ELECTROENCEPHALOGRAPHY; FEMALE; GLOBUS PALLIDUS; HIGH FREQUENCY OSCILLATION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SINGLE UNIT ACTIVITY; SPIKE WAVE; SUBSTANTIA NIGRA PARS RETICULATA; SUBTHALAMIC NUCLEUS;

ACTION POTENTIALS; ANIMALS; BASAL GANGLIA; BEHAVIOR, ANIMAL; DEEP BRAIN STIMULATION; FEMALE; MOTOR ACTIVITY; NERVE NET; NEURONS; OXIDOPAMINE; PARKINSON DISEASE, SECONDARY; RATS; RATS, LONG-EVANS;

EID: 84868601717     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2824-12.2012     Document Type: Article

References (42)

1. Benazzouz A, Piallat B, Pollak P, Benabid AL (1995) Responsesofsubstantia nigra pars reticulata and globus pallidus complex to high frequency stim-ulationof the subthalamic nucleus in rats: electrophysiological data. Neu-rosci Lett 189:77-80.
2. Benazzouz A, Gao DM, Ni ZG, Piallat B, Bouali-Benazzouz R, Benabid AL (2000) Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ven-trolateral nucleus of the thalamus in the rat. Neuroscience 99:289-295.
3. Birdno MJ, Grill WM (2008) Mechanisms of deep brain stimulation in movement disorders as revealed by changes in stimulus frequency. Neu-rotherapeutics 5:14-25.
4. Bokil H, Purpura K, Schoffelen J-M, Thomson D, Mitra P (2007) Comparing spectra and coherences for groups of unequal size. J Neurosci Methods 159: 337-345.
5. Bosch C, Degos B, Deniau JM, Venance L (2011) Subthalamic nucleus high frequency stimulation generates a concomitant synaptic excitation-inhibition in substantia nigra pars reticulata. J Physiol 589:4189-4207.
6. Breese GR, Traylor TD (1971) Depletion of brain noradrenaline and dopa-mine by 6-hydroxydopamine. Br J Pharmacol 42:88-99.
7. Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V (2001) Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J Neurosci 21:1033-1038.
8. Buonamici M, Maj R, Pagani F, Rossi AC, Khazan N (1986) Tremor at rest episodes in unilaterally 6-OHDA-induced substantia nigra lesioned rats: EEG-EMG and behavior. Neuropharmacology 25:323-325.
9. Burbaud P, Gross C, Bioulac B (1994) Effect of subthalamic high frequency stimulation on substantia nigra pars reticulata and globus pallidus neurons in normal rats. J Physiol Paris 88:359-361.
10. Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schäfer H, Bötzel K, Daniels C, Deutschländer A, Dillmann U, Eisner W, Gruber D, Hamel W, Herzog J, Hilker R, Klebe S, Kloss M, Koy J, Krause M, Kupsch A, Lorenz D, et al. (2006) Arandomized trial ofdeep-brain stimulation for Parkinson's disease. N Engl J Med 355:896-908.
11. Dorval AD, Russo GS, Hashimoto T, Xu W, Grill WM, Vitek JL (2008) Deep brain stimulation reduces neuronal entropy in the MPTP-primate model of Parkinson's disease. J Neurophysiol 100:2807-2818.
12. Eusebio A, Chen CC, Lu CS, Lee ST, Tsai CH, Limousin P, Hariz M, Brown P (2008) Effects of low-frequency stimulation of the subthalamic nucleus on movement in Parkinson's disease. Exp Neurol 209:125-130.
13. Fogelson N, Kühn AA, Silberstein P, Limousin PD, Hariz M, Trottenberg T, Kupsch A, Brown P (2005) Frequency dependent effects of subthalamic nucleus stimulation in Parkinson's disease. Neurosci Lett 382:5-9.
14. Garcia L, D'Alessandro G, Fernagut PO, Bioulac B, Hammond C (2005) Impact of high-frequency stimulation parameters on the pattern of discharge of subthalamic neurons. J Neurophysiol 94:3662-3669.
15. Goldberg JM, Brown PB (1969) Responses of binaural neurons of dog superior olivary complex to dichotic tonal stimulation: some physiological mechanisms of sound localization. J Neurophysiol 32:940-958.
16. Gradinaru V, Mogri M, Thompson KR, Henderson MJ, Deisseroth K (2009) Optical deconstruction of parkinsonian neural circuitry. Science 324: 354-359.
17. Grill WM, Snyder AN, Miocinovic S (2004) Deep brain stimulation creates an informational lesion of the stimulated nucleus. Neuroreport 15:1137-1140.
18. 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 23:1916-1923.
19. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO (2000) High-frequency synchronization of neuronal activity in the subthalamic nucleus of par-kinsonian patients with limb tremor. J Neurosci 20:7766-7775.
20. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO (2002a) Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity. J Neurosci 22:2855-2861.
21. Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO (2002b) Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. Brain 125:1196-1209.
22. McIntyre CC, Hahn PJ (2010) Network perspectives on the mechanisms of deep brain stimulation. Neurobiol Dis 38:329-337.
23. Meissner W, Harnack D, Paul G, Reum T, Sohr R, Morgenstern R, Kupsch A (2002) Deep brain stimulation of subthalamic neurons increases striatal dopamine metabolism and induces contralateral circling infreely moving 6-hydroxydopamine-lesioned rats. Neurosci Lett 328:105-108.
24. Mitra PP, Pesaran B (1999) Analysis of dynamic brain imaging data. Biophysical journal 76:691-708.
25. Moran A, Stein E, Tischler H, Belelovsky K, Bar-Gad I (2011) Dynamic stereotypic responses of basal ganglia neurons to subthalamic nucleus high-frequency stimulation in the parkinsonian primate. Front Syst Neu-rosci 5:21.
26. Moran A, Stein E, Tischler H, Bar-Gad I (2012) Decoupling neuronal oscillations during subthalamic nucleus stimulation in the parkinsonian primate. Neurobiol Dis 45:583-590.
27. Moro E, Esselink RJ, Xie J, Hommel M, Benabid AL, Pollak P (2002) The impact on Parkinson's disease of electrical parameter settings in STN stimulation. Neurology 59:706-713.
28. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, Ed 6. San Diego: Academic.
29. Reese R, Leblois A, Steigerwald F, Pötter-Nerger M, Herzog J, Mehdorn HM, Deuschl G, Meissner WG, Volkmann J (2011) Subthalamic deep brain stimulation increases pallidal firing rate and regularity. Experimental neurology 229:517-521.
30. Richards JB, Sabol KE, Freed CR (1990) Unilateral dopamine depletion causes bilateral deficits in conditioned rotation in rats. Pharmacol Biochem Behav 36:217-223.
31. Rosin B, Slovik M, Mitelman R, Rivlin-Etzion M, Haber SN, Israel Z, Vaadia E, Bergman H (2011) Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron 72:370-384.
32. Rubin JE, Terman D (2004) High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J Comput Neurosci 16:211-235.
33. Sanberg PR, Bunsey MD, Giordano M, Norman AB (1988) The catalepsy test: its ups and downs. Behav Neurosci 102:748-759.
34. Schwarting RK, Huston JP (1996) The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments. Prog Neurobiol 50:275-331.
35. Shi LH, Luo F, Woodward DJ, Chang JY (2006) Basal ganglia neural responses during behaviorally effective deep brain stimulation of the sub-thalamic nucleus in rats performing a treadmill locomotion test. Synapse 59:445-457.
36. So RQ, McConnell GC, August AT, Grill WM (2012a) Characterizing effects of subthalamic nucleus deep brain stimulation on methamphet-amine-induced circling behavior in hemiparkinsonian rats. IEEE Trans Neural Syst Rehabil Eng 20:626-635.
37. So RQ, Kent AR, Grill WM (2012b) 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 32:499-519.
38. Terman D, Rubin JE, Yew AC, Wilson CJ (2002) Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J Neurosci 22:2963-2976.
39. Timmermann L, Wojtecki L, Gross J, Lehrke R, Voges J, Maarouf M, Treuer H, Sturm V, Schnitzler A (2004) Ten-hertz stimulation of subthalamic nucleus deteriorates motor symptoms in Parkinson's disease. Mov Disord 19:1328-1333.
40. Windels F, Bruet N, Poupard A, Urbain N, Chouvet G, Feuerstein C, Savasta M (2000) Effects of high frequency stimulation of subthalamic nucleus on extracellular glutamate and GABA in substantia nigra and globus pal-lidus in the normal rat. Eur J Neurosci 12:4141-4146.
41. Windels F, Bruet N, Poupard A, Feuerstein C, Bertrand A, Savasta M (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.
42. Windels F, Carcenac C, Poupard A, Savasta M (2005) Pallidal origin of GABA release within the substantia nigra pars reticulata during high-frequency stimulation of the subthalamic nucleus. J Neurosci 25:5079-5086.