The highs and lows of beta activity in cortico-basal ganglia loops

European Journal of Neuroscience

Volumn 39, Issue 11, 2014, Pages 1951-1959

  Brittain, John Stuart ^a   Sharott, Andrew ^b   Brown, Peter ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Basal ganglia; Beta activity; Cortical; Information transfer; Parkinson's disease; Synchronization

Indexed keywords

ARTICLE; BASAL GANGLION; BETA RHYTHM; BRAIN DEPTH STIMULATION; COGNITION; CORTICOBASAL GANGLIA; DISEASE ASSOCIATION; EVOKED RESPONSE; GLOBUS PALLIDUS; HUMAN; MENTAL TASK; NERVE CELL NETWORK; NERVE CONDUCTION; NERVE STIMULATION; NERVOUS SYSTEM; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SENSORY GATING; TASK PERFORMANCE; BRAIN CORTEX; CORTICAL SYNCHRONIZATION; PATHOPHYSIOLOGY; PHYSIOLOGY;

BASAL GANGLIA; BETA RHYTHM; CEREBRAL CORTEX; CORTICAL SYNCHRONIZATION; DEEP BRAIN STIMULATION; HUMANS; PARKINSON DISEASE;

EID: 84901690796     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12574     Document Type: Article

References (100)

1. Alegre, M., Lopez-Azcarate, J., Obeso, I., Wilkinson, L., Rodriguez-Oroz, M.C., Valencia, M., Garcia-Garcia, D., Guridi, J., Artieda, J., Jahanshahi, M. & Obeso, J.A. (2013) The subthalamic nucleus is involved in successful inhibition in the stop-signal task: a local field potential study in Parkinson's disease. Exp. Neurol., 239, 1-12.
2. Ali, M.M., Sellers, K.K. & Fröhlich, F. (2013) Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J. Neurosci., 33, 11262-11275.
3. Androulidakis, A.G., Doyle, L.M., Gilbertson, T.P. & Brown, P. (2006) Corrective movements in response to displacements in visual feedback are more effective during periods of 13-35 Hz oscillatory synchrony in the human corticospinal system. Eur. J. Neurosci., 24, 3299-3304.
4. Androulidakis, A.G., Doyle, L.M., Yarrow, K., Litvak, V., Gilbertson, T.P. & Brown, P. (2007) Anticipatory changes in beta synchrony in the human corticospinal system and associated improvements in task performance. Eur. J. Neurosci., 25, 3758-3765.
5. Baker, S.N., Olivier, E. & Lemon, R.N. (1997) Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J. Physiol., 501, 225-241.
6. Baker, S.N., Pinches, E.M. & Lemon, R.N. (2003) Synchronization in monkey motor cortex during a precision grip task. II. Effect of oscillatory activity on corticospinal output. J. Neurophysiol., 89, 1941-1953.
7. Bar-Gad, I., Havazelet-Heimer, G., Goldberg, J.A., Ruppin, E. & Bergman, H. (2000) Reinforcement-driven dimensionality reduction - a model for information processing in the basal ganglia. J. Basic Clin. Physiol. Pharmacol., 11, 305-320.
8. Bar-Gad, I., Heimer, G., Ritov, Y. & Bergman, H. (2003) Functional correlations beteen neighboring neurons in the primate globus pallidus are weak or non-existent. J. Neurosci., 23, 4012-4016.
9. Baufreton, J.I., Atherton, J.F., Surmeier, D.J. & Bevan, M.D. (2005) Enhancement of excitatory synaptic integration by GABAergic inhibition in the subthalamic nucleus. J. Neurosci., 25, 8505-8517.
10. Belitski, A., Panzeri, S., Magri, C., Logothetis, N.K. & Kayser, C. (2010) Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands. J. Comput. Neurosci., 29, 533-545.
11. Berman, B.D., Starr, P.A., Marks, W.J. Jr. & Ostrem, J.L. (2009) Induction of bradykinesia with pallidal deep brain stimulation in patients with cranial-cervical dystonia. Stereot. Funct. Neuros., 87, 37-44.
12. Bertschinger, N. & Natschläger, T. (2004) Real-time computation at the edge of chaos in recurrent neural networks. Neural Comput., 16, 1413-1436.
13. Bevan, M.D., Booth, P.A., Eaton, S.A. & Bolam, J.P. (1998) Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J. Neurosci., 18, 9438-9452.
14. Brittain, J.S. & Brown, P. (2014) Oscillations and the basal ganglia: motor control and beyond. NeuroImage, 85, 637-647.
15. Brittain, J.S., Watkins, K.E., Joundi, R.A., Ray, N.J., Holland, P., Green, A.L., Aziz, T.Z. & Jenkinson, N. (2012) A role for the subthalamic nucleus in response inhibition during conflict. J. Neurosci., 32, 13396-13401.
16. 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.
17. Brown, P., Chen, C.C., Wang, S., Kühn, A.A., Doyle, L., Yarrow, K., Nuttin, B., Stein, J. & Aziz, T. (2006) Involvement of human basal ganglia in off-line feed-back control of voluntary movement. Curr. Biol., 16, 2129-2134.
18. Buzsaki, G., Anastassiou, C.A. & Koch, C. (2012) The origin of extracellular fields and currents - EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci., 13, 407-420.
19. Cagnan, H., Meijer, H.G., van Gils, S.A., Krupa, M., Heida, T., Rudolph, M., Wadman, W.J. & 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.
20. Chen, C.C., Brucke, C., Kempf, F., Kupsch, A., Lu, C.S., Tseng Lee, S., Tisch, S., Limousin, P., Hariz, M. & Brown, P. (2006) Deep brain stimulation of the subthalamic nucleus: a two-edged sword. Curr. Biol., 16, R952-R953.
21. Chen, C.C., Litvak, V., Gilbertson, T., Kühn, A., Lu, C.S., Lee, S.T., Tsai, C.H., Tisch, S., Limousin, P., Hariz, M. & Brown, P. (2007) Excessive synchronization of basal ganglia neurons at 20 Hz slows movement in Parkinson's disease. Exp. Neurol., 205, 214-221.
22. Chen, C.C., Lin, W.Y., Chan, H.L., Hsu, Y.T., Tu, P.H., Lee, S.T., Chiou, S.M., Tsai, C.H., Lu, C.S. & 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. Corcos, D.M., Chen, C.M., Quinn, N.P., McAuley, J. & Rothwell, J.C. (1996) Strength in Parkinson's disease: relationship to rate of force generation and clinical status. Ann. Neurol., 39, 79-88.
24. Courtemanche, R., Fujii, N. & Graybiel, A.M. (2003) Synchronous, focally modulated β-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. J. Neurosci., 23, 11741-11752.
25. Cruz, A.V., Mallet, N., Magill, P.J., Brown, P. & Averbeck, B.B. (2009) The effects of dopamine depletion on network entropy in the external globus pallidus. J. Neurophysiol., 102, 1092-1102.
26. Devos, D., Labyt, E., Derambure, P., Bourriez, J.L., Cassim, F., Reyns, N., Blond, S., Guieu, J.D., Destée, A. & Defebvre, L. (2004) Subthalamic nucleus stimulation modulates motor cortex oscillatory activity in Parkinson's disease. Brain, 127, 408-419.
27. Devos, D., Szurhaj, W., Reyns, N., Labyt, E., Houdayer, E., Bourriez, J.L., Cassim, F., Krystkowiak, P., Blond, S., Destée, A., Derambure, P. & Defebvre, L. (2006) Predominance of the contralateral movement-related activity in the subthalamo-cortical loop. Clin. Neurophysiol., 117, 2315-2327.
28. Doyle, L.M.F., Yarrow, K. & Brown, P. (2005a) Lateralization of event-related beta desynchronization in the EEG during pre-cued reaction time tasks. Clin. Neurophysiol., 116, 1879-1888.
29. Doyle, L.M., Kühn, A.A., Hariz, M., Kupsch, A., Schneider, G.H. & Brown, P. (2005b) Levodopa-induced modulation of subthalamic beta oscillations during self-paced movements in patients with Parkinson's disease. Eur. J. Neurosci., 21, 1403-1412.
30. Engel, A.K. & Fries, P. (2010) Beta-band oscillations - signalling the status quo? Curr. Opin. Neurobiol., 20, 156-165.
31. Eusebio, A., Thevathasan, W., Doyle Gaynor, L., Pogosyan, A., Bye, E., Foltynie, T., Zrinzo, L., Ashkan, K., Aziz, T. & Brown, P. (2011) Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. J. Neurol. Neurosur. Ps., 82, 569-573.
32. Falls, W.M., Park, M.R. & Kitai, S.T. (1983) An intracellular HRP study of the rat globus pallidus. II. Fine structural characteristics and synaptic connections of medially located large GP neurons. J. Comp. Neurol., 221, 229-245.
33. Feurra, M., Pasqualetti, P., Bianco, G., Santarnecchi, E., Rossi, A. & Rossi, S. (2013) State-dependent effects of transcranial oscillatory currents on the motor system: what you think matters. J. Neurosci., 33, 17483-17489.
34. Frank, M.J., Samanta, J., Moustafa, A.A. & Sherman, S.J. (2007) Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science, 318, 1309-1312.
35. Gilbertson, T., Lalo, E., Doyle, L., Di Lazzaro, V., Cioni, B. & Brown, P. (2005) Existing motor state is favored at the expense of new movement during 13-35 hz oscillatory synchrony in the human corticospinal system. J. Neurosci., 25, 7771-7779.
36. Goldberg, J.A. & Bergman, H. (2011) Computational physiology of the neural networks of the primate globus pallidus: function and dysfunction. Neuroscience, 198, 171-192.
37. Gould, I.C., Rushworth, M. & Nobre, A.C. (2011) Indexing the graded allocation of visuospatial attention using anticipatory alpha oscillations. J. Neurophysiol., 105, 1318-1326.
38. Gould, I.C., Nobre, A.C., Wyart, V. & Rushworth, M.F. (2012) Effects of decision variables and intraparietal stimulation on sensorimotor oscillatory activity in the human brain. J. Neurosci., 32, 13805-13818.
39. Gradinaru, V., Mogri, M., Thompson, K.R., Henderson, J.M. & Deisseroth, K. (2009) Optical deconstruction of Parkinsonian neural circuitry. Science, 324, 354-359.
40. Guo, Y., Rubin, J.E., McIntyre, C.C., Vitek, J.L. & 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.
41. Hammond, C., Bergman, H. & Brown, P. (2007) Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci., 30, 357-364.
42. Hanslmayr, S., Staudigl, T. & Fellner, M.-C. (2012) Oscillatory power decreases and long-term memory: the information via desynchronization hypothesis. Front. Hum. Neurosci., 6, 74.
43. Heimer, G., Rivlin-Etzion, M., Bar-Gad, I., Goldberg, J.A., Haber, S.N. & Bergman, H. (2006) Dopamine replacement therapy does not restore the full spectrum of normal pallidal activity in the 1-methyl-4-phenyl-1, 2, 3, 6-tetra-hydropyridine primate model of Parkinsonism. J. Neurosci., 26, 8101-8114.
44. Hirschmann, J., Özkurt, T.E., Butz, M., Homburger, M., Elben, S., Hartmann, C.J., Vesper, J., Wojtecki, L. & 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.
45. Jenkinson, N. & Brown, P. (2011) New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci., 34, 611-618.
46. Joundi, R.A., Jenkinson, N., Brittain, J.-S., Aziz, T.Z. & Brown, P. (2012) Driving oscillatory activity in the human cortex enhances motor performance. Curr. Biol., 22, 403-407.
47. Kilner, J., Bott, L. & Posada, A. (2005) Modulations in the degree of synchronization during ongoing oscillatory activity in the human brain. Eur. J. Neurosci., 21, 2547-2554.
48. Kühn, A.A., Williams, D., Kupsch, A., Dowsey-Limousin, P., Hariz, M., Schneider, G.H., Yarrow, K. & Brown, P. (2004) Event related beta desynchronization in human subthalamic nucleus correlates with motor performance. Brain, 127, 735-746.
49. Kühn, A.A., Kupsch, A., Schneider, G.-H. & 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.
50. Kühn, A.A., Kempf, F., Brücke, C., Doyle, L.G., Martinez-Torres, I., Pogosyan, A., Trottenberg, T., Kupsch, A., Schneider, G.-H., Hariz, M.I., Vandenberghe, W., Nuttin, B. & Brown, P. (2008) High-frequency stimulation of the subthalamic nucleus suppresses oscillatory β activity in patients with Parkinson's disease in parallel with improvement in motor performance. J. Neurosci., 28, 6165-6173.
51. Kühn, A.A., Tsui, A., Aziz, T., Ray, N., Brücke, C., Kupsch, A., Schneider, G.-H. & 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.
52. Little, S., Pogosyan, A., Kuhn, A.A. & Brown, P. (2012) Beta band stability over time correlates with Parkinsonian rigidity and bradykinesia. Exp. Neurol., 236, 383-388.
53. Little, S., Pogosyan, A., Neal, S., Zavala, B., Zrinzo, L., Hariz, M., Foltynie, T., Limousin, P., Ashkan, K., FitzGerald, J., Green, A.L., Aziz, T.Z. & Brown, P. (2013) Adaptive deep brain stimulation in advanced Parkinson's disease. Ann. Neurol., 74, 449-457.
54. Litvak, V., Jha, A., Eusebio, A., Oostenveld, R., Foltynie, T., Limousin, P., Zrinzo, L., Hariz, M., Friston, K. & Brown, P. (2011) Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson's disease. Brain, 134, 359-374.
55. Magill, P.J., Bolam, J.P. & Bevan, M.D. (2001) Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network. Neuroscience, 106, 313-330.
56. Mallet, N., Pogosyan, A., Sharott, A., Csicsvari, J., Bolam, J.P., Brown, P. & Magill, P.J. (2008) Disrupted dopamine transmission and the emergence of pathological beta oscillations in the subthalamic nucleus and cortex. J. Neurosci., 28, 4795-4806.
57. McIntyre, C.C., Grill, W.M., Sherman, D.L. & Thakor, N.V. (2004) Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J. Neurophysiol., 91, 1457-1469.
58. 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.
59. Moshel, S., Shamir, R.R., Raz, A., de Noriega, F.R., Eitan, R., Bergman, H. & Israel, Z. (2013) Subthalamic nucleus long-range synchronization-an independent hallmark of human Parkinson's disease. Front. Syst. Neurosci., 7, 79.
60. Murthy, V.N. & Fetz, E.E. (1996) Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J. Neurophysiol., 76, 3968-3982.
61. Ostrem, J.L., Marks, W.J. Jr., Volz, M.M., Heath, S.L. & Starr, P.A. (2007) Pallidal deep brain stimulation in patients with cranial-cervical dystonia (Meige syndrome). Movement Disord., 22, 1885-1891.
62. Oswal, A., Litvak, V., Sauleau, P. & Brown, P. (2012) Beta reactivity, prospective facilitation of executive processing, and its dependence on dopaminergic therapy in Parkinson's Disease. J. Neurosci., 32, 9909-9916.
63. Ozen, S., Sirota, A., Belluscio, M.A., Anastassiou, C.A., Stark, E., Koch, C. & Buzsaki, G. (2010) Transcranial electric stimulation entrains cortical neuronal populations in rats. J. Neurosci., 30, 11476-11485.
64. Pastötter, B., Hanslmayr, S. & Bäuml, K.H. (2008) Inhibition of return arises from inhibition of response processes: an analysis of oscillatory beta activity. J. Cognitive Neurosci., 20, 65-75.
65. Pfurtscheller, G. (1981) Central beta rhythm during sensorimotor activities in man. Electroen. Clin. Neuro., 51, 253-264.
66. Plenz, D. (2012) Neuronal avalanches and coherence potentials. Eur. Phys. J.- Spec. Top., 205, 259-301.
67. Pogosyan, A., Doyle Gaynor, L., Eusebio, A. & Brown, P. (2009) Boosting cortical activity at beta band frequencies slows movement in humans. Curr. Biol., 19, 1637-1641.
68. Pogosyan, A., Yoshida, F., Chen, C.C., Martinez-Torres, I., Foltynie, T., Limousin, P., Zrinzo, L., Hariz, M.I. & Brown, P. (2010) Parkinsonian impairment correlates with spatially extensive subthalamic oscillatory synchronization. Neuroscience, 171, 245-257.
69. Pollok, B., Krause, V., Martsch, W., Wach, C., Schnitzler, A. & Südmeyer, M. (2012) Motor-cortical oscillations in early stages of Parkinson's disease. J. Physiol., 590, 3203-3212.
70. Ponzi, A. & Wickens, J.R. (2013) Optimal balance of the striatal medium spiny neuron network. PLoS Comput. Biol., 9, e1002954.
71. Ray, N.J., Jenkinson, N., Wang, S., Holland, P., Brittain, J.S., Joint, C., Stein, J.F. & 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., 13, 108-113.
72. Ray, N.J., Jenkinson, N., Brittain, J., Holland, P., Joint, C., Nandi, D., Bain, P.G., Yousif, N., Green, A., Stein, J.S. & Aziz, T.Z. (2009) The role of the subthalamic nucleus in response inhibition: evidence from deep brain stimulation for Parkinson's disease. Neuropsychologia, 47, 2828-2834.
73. Ray, N.J., Brittain, J.S., Holland, P., Joundi, R.A., Stein, J.F., Aziz, T.Z. & Jenkinson, N. (2012) The role of the subthalamic nucleus in response inhibition: evidence from local field potential recordings in the human subthalamic nucleus. NeuroImage, 60, 271-278.
74. Rosa, M., Giannicola, G., Servello, D., Marceglia, S., Pacchetti, C., Porta, M., Sassi, M., Scelzo, E., Barbieri, S. & Priori, A. (2011) Subthalamic local field beta oscillations during ongoing deep brain stimulation in Parkinson's disease in hyperacute and chronic phases. Neurosignals, 19, 151-162.
75. Rosin, B., Slovik, M., Mitelman, R., Rivlin-Etzion, M., Haber, S.N., Israel, Z., Vaadia, E. & Bergman, H. (2011) Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron, 72, 370-384.
76. Rubin, J.E. & Terman, D. (2004) High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J. Comput. Neurosci., 16, 211-235.
77. Sadek, A.R., Magill, P.J. & Bolam, J.P. (2007) A single-cell analysis of intrinsic connectivity in the rat globus pallidus. J. Neurosci., 27, 6352-6362.
78. Schneidman, E., Puchalla, J.L., Segev, R., Harris, R.A., Bialek, W. & Berry, M.J. (2011) Synergy from silence in a combinatorial neural code. J. Neurosci., 31, 15732-15741.
79. Schrader, C., Capelle, H.H., Kinfe, T.M., Blahak, C., Bäzner, H., Lütjens, G., Dressler, D. & Krauss, J.K. (2011) GPi-DBS may induce a hypokinetic gait disorder with freezing of gait in patients with dystonia. Neurology, 77, 483-488.
80. Spinks, R.L., Kraskov, A., Brochier, T., Umilta, M.A. & Lemon, R.N. (2008) Selectivity for grasp in local field potential and single neuron activity recorded simultaneously from M1 and F5 in the awake macaque monkey. J. Neurosci., 28, 10961-10971.
81. Surmeier, D.J., Mercer, J.N. & Chan, C.S. (2005) Autonomous pacemakers in the basal ganglia: who needs excitatory synapses anyway? Curr. Opin. Neurobiol., 15, 312-318.
82. Swann, N., Tandon, N., Canolty, R., Ellmore, T.M., McEvoy, L.K., Dreyer, S., DiSano, M. & Aron, A.R. (2009) Intracranial EEG reveals a time- and frequency-specific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. J. Neurosci., 29, 12675-12685.
83. Tan, H., Pogosyan, A., Anzak, A., Ashkan, K., Bogdanovic, M., Green, A.L., Aziz, T., Foltynie, T., Limousin, P., Zrinzo, L. & Brown, P. (2013) Complementary roles of different oscillatory activities in the subthalamic nucleus in coding motor effort in Parkinsonism. Exp. Neurol., 248, 187-195.
84. Tass, P.A. & Majtanik, M. (2006) Long-term anti-kindling effects of desynchronizing brain stimulation: a theoretical study. Biol. Cybern., 94, 58-66.
85. Tripoliti, E., Zrinzo, L., Martinez-Torres, I., Pinto, S., Foltynie, T., Holl, E., Petersen, E., Roughton, M., Hariz, M.I. & Limousin, P. (2011) Effects of subthalamic nucleus deep brain stimulation on speech of consecutive patients with Parkinson's disease. Neurology, 76, 80-86.
86. Tzagarakis, C., Ince, N.F., Leuthold, A.C. & Pellizzer, G. (2010) Beta-band activity during motor planning reflects response uncertainty. J. Neurosci., 30, 11270-11277.
87. Vaillancourt, D.E., Schonfeld, D., Kwak, Y., Bohnen, N.I. & Seidler, R. (2013) Dopamine overdose hypothesis: evidence and clinical implications. Movement Disord., 28, 1920-1929.
88. Wach, C., Krause, V., Moliadze, V., Paulus, W., Schnitzler, A. & Pollok, B. (2013) Effects of 10 Hz and 20 Hz transcranial alternating current stimulation (tACS) on motor functions and motor cortical excitability. Behav. Brain Res., 241, 1-6.
89. Weinberger, M., Mahant, N., Hutchison, W.D., Lozano, A.M., Moro, E., Hodaie, M., Lang, A.E. & 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.
90. Weinberger, M., Hutchison, W.D., Alavi, M., Hodaie, M., Lozano, A.M., Moro, E. & Dostrovsky, J.O. (2012) Oscillatory activity in the globus pallidus internus: comparison between Parkinson's disease and dystonia. Clin. Neurophysiol., 123, 358-368.
91. Whitmer, D., de Solages, C., Hill, B., Yu, H., Henderson, J.M. & Bronte-Stewart, H. (2012) High frequency deep brain stimulation attenuates subthalamic and cortical rhythms in Parkinson's disease. Front. Hum. Neurosci., 6, 155.
92. van Wijk, B.C., Daffertshofer, A., Roach, N. & Praamstra, P. (2009) A role of beta oscillatory synchrony in biasing response competition? Cereb. Cortex, 19, 1294-1302.
93. Williams, D., Kühn, A., Kupsch, A., Tijssen, M., van Bruggen, G., Speelman, H., Hotton, G., Yarrow, K. & Brown, P. (2003) Behavioural cues are associated with modulations of synchronous oscillations in the human subthalamic nucleus. Brain, 126, 1975-1985.
94. Williams, D., Kühn, A., Kupsch, A., Tijssen, M., van Bruggen, G., Speelman, H., Hotton, G., Loukas, C. & Brown, P. (2005) The relationship between oscillatory activity and motor reaction time in the parkinsonian subthalamic nucleus. Eur. J. Neurosci., 21, 249-258.
95. Wilson, C.J. (2013) Active decorrelation in the basal ganglia. Neuroscience, 250, 467-482.
96. Wilson, C.J. & Kawaguchi, Y. (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J. Neurosci., 16, 2397-2410.
97. Wilson, C.J., Beverlin, B. & Netoff, T. (2011) Chaotic desynchronization as the therapeutic mechanism of deep brain stimulation. Front. Syst. Neurosci., 5, 50.
98. Wyart, V., de Gardelle, V., Scholl, J. & Summerfield, C. (2012) Rhythmic fluctuations in evidence accumulation during decision making in the human brain. Neuron, 76, 847-858.
99. Zaidel, A., Spivak, A., Grieb, B., Bergman, H. & Israel, Z. (2010) Subthalamic span of beta oscillations predicts deep brain stimulation efficacy for patients with Parkinson's disease. Brain, 133, 2007-2021.
100. Zhang, Y., Chen, Y., Bressler, S.L. & Ding, M. (2008) Response preparation and inhibition: the role of the cortical sensorimotor beta rhythm. Neuroscience, 156, 238-246.