Functional correlates of exaggerated oscillatory activity in basal ganglia output in hemiparkinsonian rats

Experimental Neurology

Volumn 261, Issue , 2014, Pages 563-577

  Brazhnik, Elena ^a   Novikov, Nikolay ^a   McCoy, Alex J ^a   Cruz, Ana V ^a   Walters, Judith R ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

6 Hydroxydopamine; Basal ganglia; Beta frequency; Dopamine; Gait; Local field potentials; Motor cortex; Oscillations; Parkinson's disease; Serotonin; Substantia nigra pars reticulata

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; DOPAMINE; LEVODOPA; URETHAN; BENSERAZIDE; ADRENERGIC RECEPTOR STIMULATING AGENT; ANTIPARKINSON AGENT; DOPAMINE RECEPTOR BLOCKING AGENT; ETICLOPRIDE; N-(2-(4-(2-METHOXYPHENYL)-1-PIPERAZINYL)ETHYL)-N-(2-PYRIDINYL)CYCLOHEXANECARBOXAMIDE; OXIDOPAMINE; PIPERAZINE DERIVATIVE; PYRIDINE DERIVATIVE; SALICYLAMIDE DERIVATIVE; SEROTONIN ANTAGONIST;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BETA RHYTHM; BRAIN DAMAGE; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; GAMMA RHYTHM; GROOMING; LOCAL FIELD POTENTIAL; MALE; MOTOR ACTIVITY; MOTOR DYSFUNCTION; NERVE CELL LESION; NERVOUS SYSTEM PARAMETERS; NONHUMAN; OSCILLATION; PARKINSON DISEASE; PARKINSONISM; PRIORITY JOURNAL; RAT; SENSORY STIMULATION; SPIKE WAVE; SUBSTANTIA NIGRA PARS RETICULATA; TREADMILL EXERCISE; UNSTEADY GAIT; WALKING; ANIMAL CELL; BRAIN ELECTROPHYSIOLOGY; DOPAMINERGIC NERVE CELL; ELECTRIC POTENTIAL; EXPLORATORY RESEARCH; FUNCTIONAL DISEASE; GAIT; HEMISPHERE; NEUROMODULATION; OSCILLATORY POTENTIAL; REM SLEEP; TREADMILL TEST; WALKING DIFFICULTY; WALKING SPEED; ACTION POTENTIAL; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ELECTROENCEPHALOGRAM; HEMISPHERIC DOMINANCE; INJURIES; LONG EVANS RAT; NERVE TRACT; PARKINSONIAN DISORDERS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SUBSTANTIA NIGRA;

ACTION POTENTIALS; ADRENERGIC AGENTS; ANIMALS; ANTIPARKINSON AGENTS; BASAL GANGLIA; BRAIN WAVES; DISEASE MODELS, ANIMAL; DOPAMINE ANTAGONISTS; FUNCTIONAL LATERALITY; LEVODOPA; MALE; NEURAL PATHWAYS; OXIDOPAMINE; PARKINSONIAN DISORDERS; PIPERAZINES; PYRIDINES; RATS; RATS, LONG-EVANS; SALICYLAMIDES; SEROTONIN ANTAGONISTS; SUBSTANTIA NIGRA;

EID: 84906729488     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.07.010     Document Type: Article

References (91)

1. Aghajanian G.K., Sprouse J.S., Sheldon P., Rasmussen K. Electrophysiology of the central serotonin system: receptor subtypes and transducer mechanisms. Ann. N. Y. Acad. Sci. 1990, 600:93-103.
2. Alonso-Frech F., Zamarbide I., Alegre M., Rodriguez-Oroz M.C., Guridi J., Manrique M., Valencia M., Artieda J., Obeso J.A. Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. Brain 2006, 129:1748-1757.
3. Avila I., Parr-Brownlie L.C., Brazhnik E., Castaneda E., Bergstrom D.A., Walters J.R. Beta frequency synchronization in basal ganglia output during rest and walk in a hemiparkinsonian rat. Exp. Neurol. 2010, 221:307-319.
4. Belluscio M.A., Escande M.V., Keifman E., Riquelme L.A., Murer M.G., Zold C.L. Oscillations in the basal ganglia in Parkinson's disease. Role of the Striatum 2013, Basal Ganglia in press.
5. Bergman H., Wichmann T., Karmon B., Delong M.R. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 1994, 72:507-520.
6. Brazhnik E., Cruz A.V., Avila I., Wahba M.I., Novikov N., Ilieva N.M., McCoy A.J., Gerber C., Walters J.R. State-dependent spike and local field synchronization between motor cortex and substantia nigra in hemiparkinsonian rats. J. Neurosci. 2012, 32:7869-7880.
7. Brittain J.S., Brown P. Oscillations and the basal ganglia: motor control and beyond. Neuroimage 2014, 85(Pt 2):637-647.
8. Brown P. Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson's disease. Mov. Disord. 2003, 18:357-363.
9. Brown P., Williams D. Basal ganglia local field potential activity: character and functional significance in the human. Clin. Neurophysiol. 2005, 116:2510-2519.
10. Brown P., Oliviero A., Mazzone P., Insola A., Tonali P., Di Lazzaro V. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J. Neurosci. 2001, 21:1033-1038.
11. Carta M., Carlsson T., Kirik D., Bjorklund A. Dopamine released from 5-HT terminals is the cause of l-DOPA-induced dyskinesia in parkinsonian rats. Brain 2007, 130:1819-1833.
12. Carta M., Carlsson T., Munoz A., Kirik D., Bjorklund A. Involvement of the serotonin system in l-dopa-induced dyskinesias. Parkinsonism Relat. Disord. 2008, 14(Suppl. 2):S154-S158.
13. Carta M., Carlsson T., Munoz A., Kirik D., Bjorklund A. Serotonin-dopamine interaction in the induction and maintenance of l-DOPA-induced dyskinesias. Prog. Brain Res. 2008, 172:465-478.
14. Cassidy M., Mazzone P., Oliviero A., Insola A., Tonali P., Di Lazzaro V., Brown P. Movement-related changes in synchronization in the human basal ganglia. Brain 2002, 125:1235-1246.
15. Chen C.C., Hsu Y.T., Chan H.L., Chiou S.M., Tu P.H., Lee S.T., Tsai C.H., Lu C.S., Brown P. Complexity of subthalamic 13-35Hz oscillatory activity directly correlates with clinical impairment in patients with Parkinson's disease. Exp. Neurol. 2010, 224:234-240.
16. Cruz A.V., Mallet N., Magill P.J., Brown P., Averbeck B.B. Effects of Dopamine Depletion on Network Entropy in the External Globus Pallidus. J. Neurophysiol. 2009, 102:1092-1102.
17. de Solages C., Hill B.C., Koop M.M., Henderson J.M., Bronte-Stewart H. Bilateral symmetry and coherence of subthalamic nuclei beta band activity in Parkinson's disease. Exp. Neurol. 2010, 221:260-266.
18. Degos B., Deniau J.-M., Chavez M., Maurice N. Chronic but not acute dopaminergic transmission interruption promotes a progressive increase in cortical beta frequency synchronization: relationships to vigilance state and akinesia. Cereb. Cortex 2009, 1616-1630.
19. Dejean C., Nadjar A., Le M.C., Bioulac B., Gross C.E., Boraud T. Evolution of the dynamic properties of the cortex-basal ganglia network after dopaminergic depletion in rats. Neurobiol. Dis. 2012, 46:402-413.
20. Delaville C., Cruz A.V., McCoy A.J., Brazhnik E., Avila I., Novikov N., Walters J.R. Oscillatory activity in basal ganglia and motor cortex in an awake behaving rodent model of Parkinson's disease. Basal Ganglia 2014, 3:221-227.
21. Delval A., Tard C., Defebvre L. Why we should study gait initiation in Parkinson's disease. Neurophysiol. Clin. 2014, 44:69-76.
22. Doyle L.M.F., Kuhn A.A., Hariz M. Levodopa-induced modulation of subthalamic beta oscillations during self-paced movements in patients with Parkinson's disease. Eur. J. Neurosci. 2005, 21:1403-1412.
23. Ellens D.J., Leventhal D.K. Review: electrophysiology of basal ganglia and cortex in models of Parkinson disease. J. Park. Dis. 2013, 3:241-254.
24. Eusebio A., Pogosyan A., Wang S., Averbeck B., Gaynor L.D., Cantiniaux S., Witjas T., Limousin P., Azulay J.P., Brown P. Resonance in subthalamo-cortical circuits in Parkinson's disease. Brain 2009, 132:2139-2150.
25. Fan K.Y., Baufreton J., Surmeier D.J., Chan C.S., Bevan M.D. Proliferation of external globus pallidus-subthalamic nucleus synapses following degeneration of midbrain dopamine neurons. J. Neurosci. 2012, 32:13718-13728.
26. Florin E., Dafsari H.S., Reck C., Barbe M.T., Pauls K.A., Maarouf M., Sturm V., Fink G.R., Timmermann L. Modulation of local field potential power of the subthalamic nucleus during isometric force generation in patients with Parkinson's disease. Neuroscience 2013, 240:106-116.
27. Foffani G., Bianchi A.M., Baselli G., Priori A. Movement-related frequency modulation of beta oscillatory activity in the human subthalamic nucleus. J. Physiol. 2005, 568:699-711.
28. Foffani G., Priori A., Ardolino, Bossi, Carrabba, Egidi, Locatelli, Caputo M., Tamma Baselli, Bianchi A., Cerutti S. Multiple independent subthalamic rhythms in patients with Parkinson's disease. Mov. Disord. 2005, 20:S86.
29. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
30. Gatev P., Darbin O., Wichmann T. Oscillations in the basal ganglia under normal conditions and in movement disorders. Mov. Disord. 2006, 21:1566-1577.
31. Goldberg J.A., Boraud T., Maraton S., Haber S.N., Vaadia E., Bergman H. 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. 2002, 22:4639-4653.
32. Heimer G., Rivlin-Etzion M., Bar-Gad I., Goldberg J.A., Haber S.N., Bergman H. 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. 2006, 26:8101-8114.
33. Hirschmann J., Ozkurt T.E., Butz M., Homburger M., Elben S., Hartmann C.J., Vesper J., Wojtecki L., Schnitzler A. Differential modulation of STN-cortical and cortico-muscular coherence by movement and levodopa in Parkinson's disease. Neuroimage 2013, 68:203-213.
34. Jenkinson N., Brown P. New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci. 2011, 34:611-618.
35. Joundi R.A., Brittain J.S., Green A.L., Aziz T.Z., Brown P., Jenkinson N. Persistent suppression of subthalamic beta-band activity during rhythmic finger tapping in Parkinson's disease. Clin. Neurophysiol. 2013, 124:565-573.
36. Kannari K., Yamato H., Shen H., Tomiyama M., Suda T., Matsunaga M. Activation of 5-HT(1A) but not 5-HT(1B) receptors attenuates an increase in extracellular dopamine derived from exogenously administered l-DOPA in the striatum with nigrostriatal denervation. J. Neurochem. 2001, 76:1346-1353.
37. Kempf F., Kuhn A.A., Kupsch A., Brucke C., Weise L., Schneider G.H., Brown P. Premovement activities in the subthalamic area of patients with Parkinson's disease and their dependence on task. Eur. J. Neurosci. 2007, 25:3137-3145.
38. Kerr C.C., Van Albada S.J., Neymotin S.A., Chadderdon G.L., Robinson P.A., Lytton W.W. Cortical information flow in Parkinson's disease: a composite network/field model. Front. Comput. Neurosci. 2013, 7:39.
39. Kita H., Kita T. Cortical stimulation evokes abnormal responses in the dopamine-depleted rat basal ganglia. J. Neurosci. 2011, 31:10311-10322.
40. Kita H., Kita T. Role of striatum in the pause and burst generation in the globus pallidus of 6-OHDA-treated rats. Front. Syst. Neurosci. 2011, 5:42.
41. Kuhn A.A., Williams D., Kupsch A., Limousin P., Hariz M., Schneider G.H., Yarrow K., Brown P. Event-related beta desynchronization in human subthalamic nucleus correlates with motor performance. Brain 2004, 127:735-746.
42. Kuhn A.A., Trottenberg T., Kivi A., Kupsch A., Schneider G.H., Brown P. The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson's disease. Exp. Neurol. 2005, 194:212-220.
43. Kuhn A.A., Kupsch A., Schneider G.H., Brown P. Reduction in subthalamic 8-35Hz oscillatory activity correlates with clinical improvement in Parkinson's disease. Eur. J. Neurosci. 2006, 23:1956-1960.
44. Kuhn A.A., Tsui A., Aziz T., Ray N., Brucke C., Kupsch A., Schneider G.H., Brown P. Pathological synchronisation in the subthalamic nucleus of patients with Parkinson's disease relates to both bradykinesia and rigidity. Exp. Neurol. 2009, 215:380-387.
45. Leblois A., Boraud T., Meissner W., Bergman H., Hansel D. Competition between feedback loops underlies normal and pathological dynamics in the basal ganglia. J. Neurosci. 2006, 26:3567-3583.
46. Leblois A., Meissner W., Bioulac B., Gross C.E., Hansel D., Boraud T. Late emergence of synchronized oscillatory activity in the pallidum during progressive Parkinsonism. Eur. J. Neurosci. 2007, 26:1701-1713.
47. Lehmkuhle M.J., Bhangoo S.S., Kipke D.R. The electrocorticogram signal can be modulated with deep brain stimulation of the subthalamic nucleus in the hemiparkinsonian rat. J. Neurophysiol. 2009, 102:1811-1820.
48. Leventhal D.K., Gage G.J., Schmidt R., Pettibone J.R., Case A.C., Berke J.D. Basal ganglia beta oscillations accompany cue utilization. Neuron 2012, 73:523-536.
49. Levy R., Hutchison W.D., Lozano A.M., Dostrovsky J.O. Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity. J. Neurosci. 2002, 22:2855-2861.
50. Li S., Arbuthnott G.W., Jutras M.J., Goldberg J.A., Jaeger D. Resonant antidromic cortical circuit activation as a consequence of high-frequency subthalamic deep-brain stimulation. J. Neurophysiol. 2007, 98:3525-3537.
51. Lindgren H.S., Andersson D.R., Lagerkvist S., Nissbrandt H., Cenci M.A. l-DOPA-induced dopamine efflux in the striatum and the substantia nigra in a rat model of Parkinson's disease: temporal and quantitative relationship to the expression of dyskinesia. J. Neurochem. 2010, 112:1465-1476.
52. Litvak V., Jha A., Eusebio A., Oostenveld R., Foltynie T., Limousin P., Zrinzo L., Hariz M.I., Friston K., Brown P. Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson's disease. Brain 2011, 134:359-374.
53. Maeda T., Nagata K., Yoshida Y., Kannari K. Serotonergic hyperinnervation into the dopaminergic denervated striatum compensates for dopamine conversion from exogenously administered l-DOPA. Brain Res. 2005, 1046:230-233.
54. Mallet N., Pogosyan A., Marton L.F., Bolam J.P., Brown P., Magill P.J. Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J. Neurosci. 2008, 28:14245-14258.
55. Mallet N., Pogosyan A., Sharott A., Csicsvari J., Bolam J.P., Brown P., Magill P.J. Disrupted dopamine transmission and the emergence of exaggerated beta oscillations in subthalamic nucleus and cerebral cortex. J. Neurosci. 2008, 28:4795-4806.
56. Marreiros A.C., Cagnan H., Moran R.J., Friston K.J., Brown P. Basal ganglia-cortical interactions in Parkinsonian patients. Neuroimage 2012, 66C:301-310.
57. Martin L.P., Jackson D.M., Wallsten C., Waszczak B.L. Electrophysiological comparison of 5-Hydroxytryptamine 1A receptor antagonists on dorsal raphe cell firing. J. Pharmacol. Exp. Ther. 1999, 288:820-826.
58. McCarthy M.M., Moore-Kochlacs C., Gu X., Boyden E.S., Han X., Kopell N. Striatal origin of the pathologic beta oscillations in Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:11620-11625.
59. Montgomery E.B. Basal ganglia pathophysiology in Parkinson's disease. Ann. Neurol. 2009, 65:618.
60. Moran R.J., Mallet N., Litvak V., Dolan R.J., Magill P.J., Friston K.J., Brown P. Alterations in brain connectivity underlying beta oscillations in parkinsonism. PLoS Comput. Biol. 2011, 7.
61. Munoz A., Li Q., Gardoni F., Marcello E., Qin C., Carlsson T., Kirik D., Di L.M., Bjorklund A., Bezard E., Carta M. Combined 5-HT1A and 5-HT1B receptor agonists for the treatment of l-DOPA-induced dyskinesia. Brain 2008, 131:3380-3394.
62. Murer M.G., Tseng K.Y., Kasanetz F., Belluscio M., Riquelme L.A. Brain oscillations, medium spiny neurons, and dopamine. Cell. Mol. Neurobiol. 2002, 22:611-632.
63. Navailles S., Bioulac B., Gross C., De D.P. Serotonergic neurons mediate ectopic release of dopamine induced by l-DOPA in a rat model of Parkinson's disease. Neurobiol. Dis. 2010, 38:136-143.
64. Nevado-Holgado A.J., Mallet N., Magill P.J., Bogacz R. Effective connectivity of the subthalamic nucleus-globus pallidus network during Parkinsonian oscillations. J. Physiol. 2014, 592:1429-1455.
65. Olsson M., Nikkhah G., Bentlage C., Bjorklund A. Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J. Neurosci. 1995, 15:3863-3875.
66. Pavlides A., Hogan S.J., Bogacz R. Improved conditions for the generation of beta oscillations in the subthalamic nucleus-globus pallidus network. Eur. J. Neurosci. 2012, 36:2229-2239.
67. Politis M., Wu K., Loane C., Brooks D.J., Kiferle L., Turkheimer F.E., Bain P., Molloy S., Piccini P. Serotonergic mechanisms responsible for levodopa-induced dyskinesias in Parkinson's disease patients. J. Clin. Invest. 2014, 124:1340-1349.
68. Priori A., Foffani G., Pesenti A., Bianchi A., Chiesa V., Baselli G., Caputo E., Tamma F., Rampini P., Egidi M., Locatelli M., Barbieri S., Scarlato G. Movement-related 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. 2002, 23:S101-S102.
69. Priori A., Foffani G., Pesenti A., Tamma F., Bianchi A.M., Pellegrini M., Locatelli M., Moxon K.A., Villani R.M. Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease. Exp. Neurol. 2004, 189:369-379.
70. Quiroga-Varela A., Walters J.R., Brazhnik E., Marin C., Obeso J.A. What basal ganglia changes underlie the parkinsonian state? The significance of neuronal oscillatory activity. Neurobiol. Dis. 2013, 58:242-248.
71. Ray N.J., Jenkinson N., Wang S., Holland P., Brittain J.S., Joint C., Stein J.F., Aziz T. 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. 2008, 213:108-113.
72. Raz A., Vaadia E., Bergman H. 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. 2000, 20:8559-8571.
73. Raz A., Frechter-Mazar V., Feingold A., Abeles M., Vaadia E., Bergman H. Activity of pallidal and striatal tonically active neurons is correlated in mptp-treated monkeys but not in normal monkeys. J. Neurosci. 2001, 21:RC128.
74. Rubin J.E., McIntyre C.C., Turner R.S., Wichmann T. Basal ganglia activity patterns in parkinsonism and computational modeling of their downstream effects. Eur. J. Neurosci. 2012, 36:2213-2228.
75. Schallert T., Tillerson J. Intervention strategies for degeneration of dopamine neurons in parkinsonism: optimizing behavioral assessment of outcome. Central Nervous System Diseases Humana Press Inc 1999, 131-151. Totowa, NJ. D. Emerich, R. Dean, P. Sanberg (Eds.).
76. Sharott A., Magill P.J., Harnack D., Kupsch A., Meissner W., Brown P. Dopamine depletion increases the power and coherence of beta-oscillations in the cerebral cortex and subthalamic nucleus of the awake rat. Eur. J. Neurosci. 2005, 21:1413-1422.
77. Stein E., Bar-Gad I. Beta oscillations in the cortico-basal ganglia loop during parkinsonism. Exp. Neurol. 2013, 245:52-59.
78. Tachibana Y., Iwamuro H., Kita H., Takada M., Nambu A. Subthalamo-pallidal interactions underlying parkinsonian neuronal oscillations in the primate basal ganglia. Eur. J. Neurosci. 2011, 34:1470-1484.
79. Tronci E., Carta M. 5-HT1 receptor agonists for the treatment of l-DOPA-induced dyskinesia: from animal models to clinical investigation. Basal Ganglia 2013, 3:9-13.
80. Tseng K.Y., Kasanetz F., Kargieman L., Riquelme L.A., Murer M.G. Cortical slow oscillatory activity is reflected in the membrane potential and spike trains of striatal neurons in rats with chronic nigrostriatal lesions. J. Neurosci. 2001, 21:6430-6439.
81. Urrestarazu E., Iriarte J., Alegre M., Clavero P., Rodriguez-Oroz M.C., Guridi J., Obeso J.A., Artieda J. Beta activity in the subthalamic nucleus during sleep in patients with Parkinson's disease. Mov. Disord. 2009, 24:254-260.
82. Van Albada S.J., Gray R.T., Drysdale P.M., Robinson P.A. Mean-field modeling of the basal ganglia-thalamocortical system. II. Dynamics of parkinsonian oscillations. J. Theor. Biol. 2009, 257:664-688.
83. Walters J.R., Hu D., Itoga C.A., Parr-Brownlie L.C., Bergstrom D.A. Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine. Neuroscience 2007, 144:762-776.
84. Waterhouse B.D., Devilbiss D., Seiple S., Markowitz R. Sensorimotor-related discharge of simultaneously recorded, single neurons in the dorsal raphe nucleus of the awake, unrestrained rat. Brain Res. 2004, 1000:183-191.
85. Weinberger M., Dostrovsky J.O. A basis for the pathological oscillations in basal ganglia: the crucial role of dopamine. Neuroreport 2011, 22:151-156.
86. Weinberger M., Mahant N., Hutchison W.D., Lozano A.M., Moro E., Hodaie M., Lang A.E., Dostrovsky J.O. Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson's disease. J. Neurophysiol. 2006, 96:3248-3256.
87. Wichmann T., Smith Y. Extrastriatal plasticity in parkinsonism. Basal Ganglia 2013, 3:5-8.
88. Wilson C.J., Bevan M.D. Intrinsic dynamics and synaptic inputs control the activity patterns of subthalamic nucleus neurons in health and in Parkinson's disease. Neuroscience 2011, 198:54-68.
89. Wingeier B., Tcheng T., Koop M.M., Hill B.C., Heit G., Bronte-Stewart H.M. Intra-operative STN DBS attenuates the prominent beta rhythm in the STN in Parkinson's disease. Exp. Neurol. 2006, 197:244-251.
90. Yamawaki N., Magill P.J., Woodhall G.L., Hall S.D., Stanford I.M. Frequency selectivity and dopamine-dependence of plasticity at glutamatergic synapses in the subthalamic nucleus. Neuroscience 2012, 203:1-11.
91. Zold C.L., Escande M.V., Pomata P.E., Riquelme L.A., Murer M.G. Striatal NMDA receptors gate cortico-pallidal synchronization in a rat model of Parkinson's disease. Neurobiol. Dis. 2012, 47:38-48.