Does suppression of oscillatory synchronisation mediate some of the therapeutic effects of DBS in patients with Parkinson's disease?

Frontiers in Integrative Neuroscience

Volumn , Issue JULY 2012, 2012, Pages

  Eusebio, Alexandre ^a,b   Cagnan, Hayriye ^c   Brown, Peter ^c  

^a TIMONE HOSPITAL   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

Basal ganglia; Deep brain stimulation; Neurophysiology; Oscillations; Parkinson's disease

Indexed keywords

BETA RHYTHM; BRADYKINESIA; BRAIN DEPTH STIMULATION; FEEDBACK SYSTEM; HUMAN; MOTOR DYSFUNCTION; MUSCLE RIGIDITY; NERVOUS SYSTEM PARAMETERS; OSCILLATORY NEURONAL SYNCHRONISATION; PARKINSON DISEASE; REVIEW; SUBTHALAMIC NUCLEUS; SYMPTOM;

EID: 84865079527     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2012.00047     Document Type: Review

References (118)

1. Albin, R. L., Young, A. B., and Penney, J. B. (1989). The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366-375.
2. Alonso-Frech, F., Zamarbide, I., Alegre, M., Rodriguez-Oroz, M. C. Guridi, J., Manrique, M., Valencia, M., Artieda, J., and Obeso, J. A. (2006). Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. Brain 129(Pt 7), 1748-1757.
3. Amirnovin, R., Williams, Z. M., Cosgrove, G. R., and Eskandar, E. N. (2004). Visually guided movements suppress subthalamic oscillations in Parkinson's disease patients. J. Neurosci. 24, 11302-11306.
4. Benabid, A. L., Chabardes, S., Mitrofanis, J., and Pollak, P. (2009). Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease. Lancet Neurol. 8, 67-81.
5. Benabid, A. L., Pollak, P., Gervason, C., Hoffmann, D., Gao, D. M., Hommel, M., Perret, J. E., and de Rougemont, J. (1991). Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337, 403-406.
6. Benabid, A. L., Pollak, P., Gross, C., Hoffmann, D., Benazzouz, A., Gao, D. M., Laurent, A., Gentil, M., and Perret, J. (1994). Acute and long-term effects of subthalamic nucleus stimulation in Parkinson's disease. Stereotact. Funct. Neurosurg. 62, 76-84.
7. Benabid, A. L., Pollak, P., Louveau, A., Henry, S., and de Rougemont, J. (1987). Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl. Neurophysiol. 50, 344-346.
8. Benazzouz, A., Gross, C., Feger, J., Boraud, T., and Bioulac, B. (1993). Reversal of rigidity and improvement in motor performance by subthalamic high-frequency stimulation in MPTP-treated monkeys. Eur. J. Neurosci. 5, 382-389.
9. Bergman, H., Wichmann, T., and DeLong, M. R. (1990). Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249, 1436-1438.
10. Beurrier, C., Bioulac, B., Audin, J., and Hammond, C. (2001). Highfrequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J. Neurophysiol. 85, 1351-1356.
11. Bronte-Stewart, H., Barberini, C., Koop, M. M., Hill, B. C., Henderson, J. M., and Wingeier, B. (2009). The STN beta-band profile in Parkinson's disease is stationary and shows prolonged attenuation after deep brain stimulation. Exp. Neurol. 215, 20-28.
12. Brown, P. (2003). Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson's disease. Mov. Disord. 18, 357-363.
13. Brown, P. (2007). Abnormal oscillatory synchronisation in the motor system leads to impaired movement. Curr. Opin. Neurobiol. 17, 656-664.
14. Brown, P., and Eusebio, A. (2008). Paradoxes of functional neurosurgery: clues from basal ganglia recordings. Mov. Disord. 23, 12-20. quiz: 158.
15. Brown, P., Mazzone, P., Oliviero, A., Altibrandi, M. G., Pilato, F., Tonali, P. A., and Di Lazzaro, V. (2004). Effects of stimulation of the subthalamic area on oscillatory pallidal activity in Parkinson's disease. Exp. Neurol. 188, 480-490.
16. Brown, P., Oliviero, A., Mazzone, P., Insola, A., Tonali, P., and Di Lazzaro, V. (2001). Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J. Neurosci. 21, 1033-1038.
17. Cagnan, H., Meijer, H. G., van Gils, S. A., Krupa, M., Heida, T., Rudolph, M., Wadman, W. J., and Martens, H. C. (2009). Frequency-selectivity of a thalamocortical relay neuron during Parkinson's disease and deep brain stimulation: a computational study. Eur. J. Neurosci. 30, 1306-1317.
18. Carlson, J. D., Cleary, D. R., Cetas, J. S., Heinricher, M. M., and Burchiel, K. J. (2010). Deep brain stimulation does not silence neurons in subthalamic nucleus in Parkinson's patients. J. Neurophysiol. 103, 962-967.
19. Cassidy, M., Mazzone, P., Oliviero, A., Insola, A., Tonali, P., Di Lazzaro, V., and Brown, P. (2002). Movementrelated changes in synchronization in the human basal ganglia. Brain 125(Pt 6), 1235-1246.
20. Chen, C. C., Brucke, C., Kempf, F., Kupsch, A., Lu, C. S., Lee, S. T., Tisch, S., Limousin, P., Hariz, M., and Brown, P. (2006). Deep brain stimulation of the subthalamic nucleus: a two-edged sword. Curr. Biol. 16, R952-R953.
21. Chen, C. C., Hsu, Y. T., Chan, H. L., Chiou, S. M., Tu, P. H., Lee, S. T., Tsai, C. H., Lu, C. S., and Brown, P. (2010). Complexity of subthalamic 13-35 Hz oscillatory activity directly correlates with clinical impairment in patients with Parkinson's disease. Exp. Neurol. 224, 234-240.
22. Chen, C. C., lin, W., Chan, H. L., Hsu, Y. T., Tu, P. H., Lee, S., Chiou, S. M., Tsai, C. H., Lu, C. S., and Brown, P. (2011). Stimulation of the subthalamic region at 20 Hz slows the development of grip force in Parkinson's disease. Exp. Neurol. 231, 91-96.
23. Chen, C. C., Litvak, V., Gilbertson, T., Kuhn, A., Lu, C. S., Lee, S. T., Tsai, C. H., Tisch, S., Limousin, P., Hariz, M., and Brown, P. (2007). Excessive synchronization of basal ganglia neurons at 20 Hz slows movement in Parkinson's disease. Exp. Neurol. 205, 214-221.
24. DeLong, M. R. (1990). Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13, 281-285.
25. de Solages, C., Hill, B. C., Koop, M. M., Henderson, J. M., and Bronte-Stewart, H. (2010). Bilateral symmetry and coherence of subthalamic nuclei beta band activity in Parkinson's disease. Exp. Neurol. 221, 260-266.
26. Deuschl, G., Schade-Brittinger, C., Krack, P., Volkmann, J., Schafer, H., Botzel, K., Daniels, C., Deutschlander, 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., Lorenzl, S., Mehdorn, H. M., Moringlane, J. R., Oertel, W., Pinsker, M. O., Reichmann, H., Reuss, A., Schneider, G. H., Schnitzler, A., Steude, U., Sturm, V., Timmermann, L., Tronnier, V., Trottenberg, T., Wojtecki, L., Wolf, E., Poewe, W., and Voges, J. (2006). A randomized trial of deep-brain stimulation for Parkinson's disease. N. Engl. J. Med. 355, 896-908.
27. Dorval, A. D., Kuncel, A. M., Birdno, M. J., Turner, D. A., and Grill, W. M. (2010). Deep brain stimulation alleviates parkinsonian bradykinesia by regularizing pallidal activity. J. Neurophysiol. 104, 911-921.
28. Dorval, A. D., Russo, G. S., Hashimoto, T., Xu, W., Grill, W. M., and Vitek, J. L. (2008). Deep brain stimulation reduces neuronal entropy in the MPTP-primate model of Parkinson's disease. J. Neurophysiol. 100, 2807-2818.
29. Dostrovsky, J. O., Levy, R., Wu, J. P., Hutchison, W. D., Tasker, R. R., and Lozano, A. M. (2000). Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J. Neurophysiol. 84, 570-574.
30. Eusebio, A., Chen, C. C., Lu, C. S., Lee, S. T., Tsai, C. H., Limousin, P., Hariz, M., and Brown, P. (2008). Effects of low-frequency stimulation of the subthalamic nucleus on movement in Parkinson's disease. Exp. Neurol. 209, 125-130.
31. Eusebio, A., Pogosyan, A., Wang, S., Averbeck, B., Gaynor, L. D., Cantiniaux, S., Witjas, T., Limousin, P., Azulay, J. P., and Brown, P. (2009). Resonance in subthalamocortical circuits in Parkinson's disease. Brain 132(Pt 8), 2139-2150.
32. Eusebio, A., Thevathasan, W., Doyle Gaynor, L., Pogosyan, A., Bye, E., Foltynie, T., Zrinzo, L., Ashkan, K., Aziz, T., and Brown, P. (2011). Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. J. Neurol. Neurosurg. Psychiatry 82, 569-573.
33. Fasano, A., Romito, L. M., Daniele, A., Piano, C., Zinno, M., Bentivoglio, A. R., and Albanese, A. (2010). Motor and cognitive outcome in patients with Parkinson's disease 8 years after subthalamic implants. Brain 133, 2664-2676.
34. Foffani, G., Ardolino, G., Egidi, M., Caputo, E., Bossi, B., and Priori, A. (2006). Subthalamic oscillatory activities at beta or higher frequency do not change after high-frequency DBS in Parkinson's disease. Brain Res. Bull. 69, 123-130.
35. Foffani, G., Ardolino, G., Meda, B., Egidi, M., Rampini, P., Caputo, E., Baselli, G., and Priori, A. (2005). Altered subthalamo-pallidal synchronisation in parkinsonian dyskinesias. J. Neurol. Neurosurg. Psychiatry 76, 426-428.
36. Foffani, G., Priori, A., Egidi, M., Rampini, P., Tamma, F., Caputo, E., Moxon, K. A., Cerutti, S., and Barbieri, S. (2003). 300-Hz subthalamic oscillations in Parkinson's disease. Brain 126(Pt 10), 2153-2163.
37. Fogelson, N., Kuhn, A. A., Silberstein, P., Limousin, P. D., Hariz, M., Trottenberg, T., Kupsch, A., and Brown, P. (2005). Frequency dependent effects of subthalamic nucleus stimulation in Parkinson's disease. Neurosci. Lett. 382, 5-9.
38. Fogelson, N., Williams, D., Tijssen, M., van Bruggen, G., Speelman, H., and Brown, P. (2006). Different functional loops between cerebral cortex and the subthalmic area in Parkinson's disease. Cereb. Cortex 16, 64-75.
39. Follett, K. A., Weaver, F. M., Stern, M., Hur, K., Harris, C. L., Luo, P., Marks, W. J. Jr., Rothlind, J., Sagher, O., Moy, C., Pahwa, R., Burchiel, K., Hogarth, P., Lai, E. C., Duda, J. E., Holloway, K., Samii, A., Horn, S., Bronstein, J. M., Stoner, G., Starr, P. A., Simpson, R., Baltuch, G., De Salles, A., Huang, G. D., and Reda, D. J. (2010). Pallidal versus subthalamic deep-brain stimulation for Parkinson's disease. N. Engl. J. Med. 362, 2077-2091.
40. Frankemolle, A. M., Wu, J., Noecker, A. M., Voelcker-Rehage, C., Ho, J. C., Vitek, J. L., McIntyre, C. C., and Alberts, J. L. (2010). Reversing cognitive-motor impairments in Parkinson's disease patients using a computational modelling approach to deep brain stimulation programming. Brain 133(Pt 3), 746-761.
41. Garcia, L. Audin, J., D'Alessandro, G., Bioulac, B., and Hammond, C. (2003). Dual effect of highfrequency stimulation on subthalamic neuron activity. J. Neurosci. 23, 8743-8751.
42. Garcia, L., D'Alessandro, G., Bioulac, B., and Hammond, C. (2005). High-frequency stimulation in Parkinson's disease: more or less? Trends Neurosci. 28, 209-216.
43. Giannicola, G., Marceglia, S., Rossi, L., Mrakic-Sposta, S., Rampini, P., Tamma, F., Cogiamanian, F., Barbieri, S., and Priori, A. (2010). The effects of levodopa and ongoing deep brain stimulation on subthalamic beta oscillations in Parkinson's disease. Exp. Neurol. 226, 120-127.
44. Gubellini, P., Eusebio, A., Oueslati, A., Melon, C., Kerkerian-Le Goff, L., and Salin, P. (2006). Chronic high-frequency stimulation of the subthalamic nucleus and L-DOPA treatment in experimental parkinsonism: effects on motor behavior and striatal glutamate transmission. Eur. J. Neurosci. 24, 1802-1814.
45. Guo, Y., and Rubin, J. E. (2011). Multi-site stimulation of subthalamic nucleus diminishes thalamocortical relay errors in a biophysical network model. Neural Netw. 24, 602-616.
46. Guo, Y., Rubin, J. E., McIntyre, C. C., Vitek, J. L., and Terman, D. (2008). Thalamocortical relay fidelity varies across subthalamic nucleus deep brain stimulation protocols in a data-driven computational model. J. Neurophysiol. 99, 1477-1492.
47. Gutfreund, Y., yarom, Y., and Segev, I. (1995). Subthreshold oscillations and resonant frequency in guineapig cortical neurons: physiology and modelling. J. Physiol. 483(Pt 3), 621-640.
48. Hahn, P. J., and McIntyre, C. C. (2010). Modeling shifts in the rate and pattern of subthalamopallidal network activity during deep brain stimulation. J. Comput. Neurosci. 28, 425-441.
49. Hammond, C., Ammari, R., Bioulac, B., and Garcia, L. (2008). Latest view on the mechanism of action of deep brain stimulation. Mov. Disord. 23, 2111-2121.
50. Hammond, C., Bergman, H., and Brown, P. (2007). Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci. 30, 357-364.
51. Hariz, M. I., Blomstedt, P., and Zrinzo, L. (2010). Deep brain stimulation between 1947 and 1987, the untold story. Neurosurg. Focus 29, E1.
52. Hashimoto, T., Elder, C. M., Okun, M. S., Patrick, S. K., and Vitek, J. L. (2003). Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J. Neurosci. 23, 1916-1923.
53. Hauptmann, C., and Tass, P. (2010). Restoration of segregated, physiological neuronal connectivity by desynchronizing stimulation. J. Neural Eng. 7, 056008.
54. Hirschmann, J., Ozkurt, T. E., Butz, M., Homburger, M., Elben, S., Hartmann, C. J., Vesper, J., Wojtecki, L., and Schnitzler, A. (2011). Distinct oscillatory STN-cortical loops revealed by simultaneous MEG and local field potential recordings in patients with Parkinson's disease. Neuroimage 55, 1159-1168.
55. Holsheimer, J., Demeulemeester, H., Nuttin, B., and de Sutter, P. (2000). Identification of the target neuronal elements in electrical deep brain stimulation. Eur. J. Neurosci. 12, 4573-4577.
56. Kim, H. J., Paek, S. H., Kim, J. Y., Lee, J. Y., Lim, Y. H., Kim, D. G., and Jeon, B. S. (2009). Two-year followup on the effect of unilateral subthalamic deep brain stimulation in highly asymmetric Parkinson's disease. Mov. Disord. 24, 329-335.
57. Kleiner-Fisman, G., Herzog, J., Fisman, D. N., Tamma, F., Lyons, K. E., Pahwa, R., Lang, A. E., and Deuschl, G. (2006). Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov. Disord. 21(Suppl. 14), S290-S304.
58. Krack, P., Batir, A., Van Blercom, N., Chabardes, S., Fraix, V., Ardouin, C., Koudsie, A., Limousin, P. D., Benazzouz, A., LeBas, J. F., Benabid, A. L., and Pollak, P. (2003). Fiveyear follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N. Engl. J. Med. 349, 1925-1934.
59. Kuhn, A. A., Kempf, F., Brucke, C., Gaynor Doyle, L., Martinez-Torres, I., Pogosyan, A., Trottenberg, T., Kupsch, A., Schneider, G. H., Hariz, M. I., Vandenberghe, W., Nuttin, B., and Brown, P. (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, 6165-6173.
60. Kuhn, A. A., Kupsch, A., Schneider, G. H., and Brown, P. (2006). Reduction in subthalamic 8-35 Hz oscillatory activity correlates with clinical improvement in Parkinson's disease. Eur. J. Neurosci. 23, 1956-1960.
61. Kuhn, A. A., Trottenberg, T., Kivi, A., Kupsch, A., Schneider, G. H., and Brown, P. (2005). The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson's disease. Exp. Neurol. 194, 212-220.
62. Kuhn, A. A., Tsui, A., Aziz, T., Ray, N., Brucke, C., Kupsch, A., Schneider, G. H., and Brown, P. (2009). Pathological synchronisation in the subthalamic nucleus of patients with Parkinson's disease relates to both bradykinesia and rigidity. Exp. Neurol. 215, 380-387.
63. Kuhn, A. A., Williams, D., Kupsch, A., Limousin, P., Hariz, M., Schneider, G. H., Yarrow, K., and Brown, P. (2004). Event-related beta desynchronization in human subthalamic nucleus correlates with motor performance. Brain 127(Pt 4), 735-746.
64. Lalo, E., Thobois, S., Sharott, A., Polo, G., Mertens, P., Pogosyan, A., and Brown, P. (2008). Patterns of bidirectional communication between cortex and basal ganglia during movement in patients with Parkinson disease. J. Neurosci. 28, 3008-3016.
65. Levy, R., Ashby, P., Hutchison, W. D., Lang, A. E., Lozano, A. M., and Dostrovsky, J. O. (2002a). Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. Brain 125(Pt 6), 1196-1209.
66. Levy, R., Hutchison, W. D., Lozano, A. M., and Dostrovsky, J. O. (2002b). Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity. J. Neurosci. 22, 2855-2861.
67. Levy, R., Hutchison, W. D., Lozano, A. M., and Dostrovsky, J. O. (2000). High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J. Neurosci. 20, 7766-7775.
68. Limousin, P., Pollak, P., Benazzouz, A., Hoffmann, D., Le Bas, J. F., Broussolle, E., Perret, J. E., and Benabid, A. L. (1995). Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345, 91-95.
69. Litvak, V., Jha, A., Eusebio, A., Oostenveld, R., Foltynie, T., Limousin, P., Zrinzo, L., Hariz, M. I., Friston, K., and Brown, P. (2011). Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson's disease. Brain 134(Pt 2), 359-374.
70. Lopez-Azcarate, J., Tainta, M., Rodriguez-Oroz, M. C., Valencia, M., Gonzalez, R., Guridi, J., Iriarte, J., Obeso, J. A., Artieda, J., and Alegre, M. (2010). Coupling between beta and high-frequency activity in the human subthalamic nucleus may be a pathophysiological mechanism in Parkinson's disease. J. Neurosci. 30, 6667-6677.
71. Marceglia, S., Foffani, G., Bianchi, A. M., Baselli, G., Tamma, F., Egidi, M., and Priori, A. (2006). Dopamine-dependent non-linear correlation between subthalamic rhythms in Parkinson's disease. J. Physiol. 571(Pt 3), 579-591.
72. Marceglia, S., Rossi, L., Foffani, G., Bianchi, A., Cerutti, S., and Priori, A. (2007). Basal ganglia local field potentials: applications in the development of new deep brain stimulation devices for movement disorders. Expert Rev. Med. Devices 4, 605-614.
73. Marsden, C. D., and Obeso, J. A. (1994). The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. Brain 117(Pt 4), 877-897.
74. Marsden, J. F., Limousin-Dowsey, P., Ashby, P., Pollak, P., and Brown, P. (2001). Subthalamic nucleus, sensorimotor cortex and muscle interrelationships in Parkinson's disease. Brain 124(Pt 2), 378-388.
75. Maurice, N., Thierry, A. M., Glowinski, J., and Deniau, J. M. (2003). Spontaneous and evoked activity of substantia nigra pars reticulata neurons during high-frequency stimulation of the subthalamic nucleus. J. Neurosci. 23, 9929-9936.
76. McIntyre, C. C., Savasta, M., Walter, B. L., and Vitek, J. L. (2004). How does deep brain stimulation work? Present understanding and future questions. J. Clin. Neurophysiol. 21, 40-50.
77. Meissner, W., Leblois, A., Benazzouz, A., and Boraud, T. (2006). Subthalamic high-frequency stimulation drives subthalamic oscillatory activity at stimulation frequency while firing rate is reduced. Brain 129, E60 (letter).
78. Meissner, W., Leblois, A., Hansel, D., Bioulac, B., Gross, C. E., Benazzouz, A., and Boraud, T. (2005). Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 128(Pt 10), 2372-2382.
79. Montgomery, E. B. Jr., and Gale, J. T. (2008). Mechanisms of action of deep brain stimulation. Neurosci. Biobehav. Rev. 32, 388-407.
80. Moro, E., Poon, Y. Y., Lozano, A. M., Saint-Cyr, J. A., and Lang, A. E. (2006). Subthalamic nucleus stimulation: improvements in outcome with reprogramming. Arch. Neurol. 63, 1266-1272.
81. Nicola, S. M., Surmeier, J., and Malenka, R. C. (2000). Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu. Rev. Neurosci. 23, 185-215.
82. Ozkurt, T. E., Butz, M., Homburger, M., Elben, S., Vesper, J., Wojtecki, L., and Schnitzler, A. (2011). High frequency oscillations in the subthalamic nucleus: a neurophysiological marker of the motor state in Parkinson's disease. Exp. Neurol. 229, 324-331.
83. Pfurtscheller, G., Woertz, M., Supp, G., and F. H. Lopes da Silva. (2003). Early onset of post-movement beta electroencephalogram synchronization in the supplementary motor area during self-paced finger movement in man. Neurosci. Lett. 339, 111-114.
84. Pirini, M., Rocchi, L., Sensi, M., and Chiari, L. (2009). A computational modelling approach to investigate different targets in deep brain stimulation for Parkinson's disease. J. Comput. Neurosci. 26, 91-107.
85. Pogosyan, A., Yoshida, F., Chen, C. C., Martinez-Torres, I., Foltynie, T., Limousin, P., Zrinzo, L., Hariz, M., and Brown, P. (2010). Parkinsonian impairment correlates with spatially extensive subthalamic oscillatory synchronization. Neuroscience 171, 245-257.
86. Priori, A., Foffani, G., Pesenti, A., Bianchi, A., Chiesa, V., Baselli, G., Caputo, E., Tamma, F., Rampini, P., Egidi, M., Locatelli, M., Barbieri, S., and Scarlato, G. (2002). Movementrelated modulation of neural activity in human basal ganglia and its L-DOPA dependency: recordings from deep brain stimulation electrodes in patients with Parkinson's disease. Neurol. Sci. 23(Suppl. 2), S101-S102.
87. Priori, A., Foffani, G., Pesenti, A., Tamma, F., Bianchi, A. M., Pellegrini, M., Locatelli, M., Moxon, K. A., and Villani, R. M. (2004). Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease. Exp. Neurol. 189, 369-379.
88. Ray, N. J., Jenkinson, N., Wang, S., Holland, P., Brittain, J. S., Joint, C., Stein, J. F., and Aziz, T. (2008). Local field potential beta activity in the subthalamic nucleus of patients with Parkinson's disease is associated with improvements in bradykinesia after dopamine and deep brain stimulation. Exp. Neurol. 213, 108-113.
89. Ray, N., Jenkinson, N., Brittain, J. S., Holland, P., Joint, C., Nandi, D., Bain, P. G., Yousif, N., Green, A. J., Stein, J., and Aziz, T. (2009). The role of the subthalamic nucleus in response inhibition: evidence from deep brain stimulation for Parkinson's disease. Neuropsychologia 47, 2828-2834.
90. Raz, A., Vaadia, E., and Bergman, H. (2000). Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl1, 2, 3, 6-tetrahydropyridine vervet model of parkinsonism. J. Neurosci. 20, 8559-8571.
91. Rivlin-Etzion, M., Marmor, O., Heimer, G., Raz, A., Nini, A., and Bergman, H. (2006). Basal ganglia oscillations and pathophysiology of movement disorders. Curr. Opin. Neurobiol. 16, 629-637.
92. Rodriguez-Oroz, M. C., Obeso, J. A., Lang, A. E., Houeto, J. L., Pollak, P., Rehncrona, S., Kulisevsky, J., Albanese, A., Volkmann, J., Hariz, M. I., Quinn, N. P., Speelman, J. D., Guridi, J., Zamarbide, I., Gironell, A., Molet, J., Pascual-Sedano, B., Pidoux, B., Bonnet, A. M., Agid, Y., Xie, J., Benabid, A. L., Lozano, A. M., Saint-Cyr, J., Romito, L., Contarino, M. F., Scerrati, M., Fraix, V., and Van Blercom, N. (2005). Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. Brain 128(Pt 10), 2240-2249.
93. Rosin, B., Slovik, M., Mitelman, R., Rivlin-Etzion, M., Haber, S. N., Israel, Z., Vaadia, E., and Bergman, H. (2011). Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron 72, 370-384.
94. Rossi, L., Foffani, G., Marceglia, S., Bracchi, F., Barbieri, S., and Priori, A. (2007). An electronic device for artefact suppression in human local field potential recordings during deep brain stimulation. J. Neural Eng. 4, 96-106.
95. Rossi, L., Marceglia, S., Foffani, G., Cogiamanian, F., Tamma, F., Rampini, P., Barbieri, S., Bracchi, F., and Priori, A. (2008). Subthalamic local field potential oscillations during ongoing deep brain stimulation in Parkinson's disease. Brain Res. Bull. 76, 512-521.
96. Rubin, J. E., and Terman, D. (2004). High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J. Comput. Neurosci. 16, 211-235.
97. Salin, P., Manrique, C., Forni, C., and Kerkerian-Le Goff, L. (2002). Highfrequency 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.
98. Shin, D. S., and Carlen, P. L. (2008). Enhanced Ih depresses rat entopeduncular nucleus neuronal activity from high-frequency stimulation or raised Ke+. J. Neurophysiol. 99, 2203-2219.
99. Silberstein, P., Kuhn, A. A., Kupsch, A., Trottenberg, T., Krauss, J. K., Wohrle, J. C., Mazzone, P., Insola, A., Di Lazzaro, V., Oliviero, A., Aziz, T., and Brown, P. (2003). Patterning of globus pallidus local field potentials differs between Parkinson's disease and dystonia. Brain 126(Pt 12), 2597-2608.
100. Silberstein, P., Pogosyan, A., Kuhn, A. A., Hotton, G., Tisch, S., Kupsch, A., Dowsey-Limousin, P., Hariz, M. I., and Brown, P. (2005). Cortico-cortical coupling in Parkinson's disease and its modulation by therapy. Brain 128(Pt 6), 1277-1291.
101. Sochurkova, D., and Rektor, I. (2003). Event-related desynchronization/synchronization in the putamen. An SEEG case study. Exp. Brain Res. 149, 401-404.
102. Stanslaski, S., Cong, P., Carlson, D., Santa, W., Jensen, R., Molnar, G., Marks, W. J. Jr., Shafquat, A., and Denison, T. (2009). An implantable bi-directional brain-machine interface system for chronic neuroprosthesis research. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 5494-5497.
103. Tabbal, S. D., Ushe, M., Mink, J. W., Revilla, F. J., Wernle, A. R., Hong, M., Karimi, M., and Perlmutter, J. S. (2008). Unilateral subthalamic nucleus stimulation has a measurable ipsilateral effect on rigidity and bradykinesia in Parkinson disease. Exp. Neurol. 211, 234-242.
104. 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. The deep-brain stimulation for Parkinson's disease study group. N. Engl. J. Med. 345, 956-963.
105. Timmermann, L., Wojtecki, L., Gross, J., Lehrke, R., Voges, J., Maarouf, M., Treuer, H., Sturm, V., and Schnitzler, A. (2004). Ten-Hertz stimulation of subthalamic nucleus deteriorates motor symptoms in Parkinson's disease. Mov. Disord. 19, 1328-1333.
106. Tukhlina, N., Rosenblum, M., Pikovsky, A., and Kurths, J. (2007). Feedback suppression of neural synchrony by vanishing stimulation. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 75(1 Pt 1), 011918.
107. Volkmann, J., Albanese, A., Kulisevsky, J., Tornqvist, A. L., Houeto, J. L., Pidoux, B., Bonnet, A. M., Mendes, A., Benabid, A. L., Fraix, V., Van Blercom, N., Xie, J., Obeso, J., Rodriguez-Oroz, M. C., Guridi, J., Schnitzler, A., Timmermann, L., Gironell, A. A., Molet, J., Pascual-Sedano, B., Rehncrona, S., Moro, E., Lang, A. C., Lozano, A. M., Bentivoglio, A. R., Scerrati, M., Contarino, M. F., Romito, L., Janssens, M., and Agid, Y. (2009). Long-term effects of pallidal or subthalamic deep brain stimulation on quality of life in Parkinson's disease. Mov. Disord. 24, 1154-1161.
108. Walker, H. C., Watts, R. L., Guthrie, S., Wang, D., and Guthrie, B. L. (2009). Bilateral effects of unilateral subthalamic deep brain stimulation on Parkinson's disease at 1 year. Neurosurgery 65, 302-309. discussion: 309-310.
109. Weinberger, M., Hutchison, W. D., Lozano, A. M., Hodaie, M., and Dostrovsky, J. O. (2009). Increased gamma oscillatory activity in the subthalamic nucleus during tremor in Parkinson's disease patients. J. Neurophysiol. 101, 789-802.
110. Weinberger, M., Mahant, N., Hutchison, W. D., Lozano, A. M., Moro, E., Hodaie, M., Lang, A. E., and Dostrovsky, J. O. (2006). Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson's disease. J. Neurophysiol. 96, 3248-3256.
111. Welter, M. L., Houeto, J. L., Bonnet, A. M., Bejjani, P. B., Mesnage, V., Dormont, D., Navarro, S., Cornu, P., Agid, Y., and Pidoux, B. (2004). Effects of high-frequency stimulation on subthalamic neuronal activity in parkinsonian patients. Arch. Neurol. 61, 89-96.
112. Williams, D., Kuhn, A., Kupsch, A., Tijssen, M., van Bruggen, G., Speelman, H., Hotton, G., Loukas, C., and Brown, P. (2005). The relationship between oscillatory activity and motor reaction time in the parkinsonian subthalamic nucleus. Eur. J. Neurosci. 21, 249-258.
113. Williams, D., Kuhn, A., Kupsch, A., Tijssen, M., van Bruggen, G., Speelman, H., Hotton, G., Yarrow, K., and Brown, P. (2003). Behavioural cues are associated with modulations of synchronous oscillations in the human subthalamic nucleus. Brain 126(Pt 9), 1975-1985.
114. Williams, D., Tijssen, M., Van Bruggen, G., Bosch, A., Insola, A., Di Lazzaro, V., Mazzone, P., Oliviero, A., Quartarone, A., Speelman, H., and Brown, P. (2002). Dopaminedependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 125(Pt 7), 1558-1569.
115. Wingeier, B., Tcheng, T., Koop, M. M., Hill, B. C., Heit, G., and Bronte-Stewart, H. M. (2006). Intra-operative STN DBS attenuates the prominent beta rhythm in the STN in Parkinson's disease. Exp. Neurol. 197, 244-251.
116. Witjas, T., Kaphan, E., Regis, J., Jouve, E., Cherif, A. A., Peragut, J. C., and Azulay, J. P. (2007). Effects of chronic subthalamic stimulation on nonmotor fluctuations in Parkinson's disease. Mov. Disord. 22, 1729-1734.
117. Yoshida, F., Martinez-Torres, I., Pogosyan, A., Holl, E., Petersen, E., Chen, C. C., Foltynie, T., Limousin, P., Zrinzo, L. U., Hariz, M. I., and Brown, P. (2010). Value of subthalamic nucleus local field potentials recordings in prediciting stimulation parameters for deep brain stimulation in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 81, 885-889.
118. Zaidel, A., Spivak, A., Grieb, B., Bergman, H., and Israel, Z. (2010). Subthalamic span of beta oscillations predicts deep brain stimulation efficacy for patients with Parkinson's disease. Brain 133(Pt 7), 2007-2021.