What basal ganglia changes underlie the parkinsonian state? The significance of neuronal oscillatory activity

Neurobiology of Disease

Volumn 58, Issue , 2013, Pages 242-248

  Quiroga Varela, A ^b,c   Walters, J R ^d   Brazhnik, E ^d   Marin, C ^c,e   Obeso, J A ^a,b,c  

^a UNIVERSITY CLINIC OF NAVARRA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

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

^e INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

Basal ganglia; Beta oscillations; Oscillatory activity; Parkinson's disease

Indexed keywords

DOPAMINE;

BASAL GANGLION; BETA RHYTHM; BRAIN FUNCTION; DOPAMINERGIC ACTIVITY; GLOBUS PALLIDUS; HUMAN; INTERNEURON; NEUROPHYSIOLOGY; NONHUMAN; OSCILLATION; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SUBSTANTIA NIGRA PARS RETICULATA; SUBTHALAMIC NUCLEUS; SUBTHALAMUS; TASK PERFORMANCE;

BASAL GANGLIA; BETA OSCILLATIONS; OSCILLATORY ACTIVITY; PARKINSON'S DISEASE;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; BASAL GANGLIA; BIOLOGICAL CLOCKS; DISEASE MODELS, ANIMAL; HUMANS; NEURONS; OXIDOPAMINE; PARKINSON DISEASE; RATS;

EID: 84880150978     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.05.010     Document Type: Review

References (91)

1. Alegre M., et al. The subthalamic nucleus is involved in successful inhibition in the stop-signal task: a local field potential study in Parkinson's disease. Exp. Neurol. 2013, 239:1-12.
2. Alonso-Frech F., et al. Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. Brain 2006, 129:1748-1757.
3. Anzak A., et al. Subthalamic nucleus gamma oscillations mediate a switch from automatic to controlled processing: a study of random number generation in Parkinson's disease. NeuroImage 2013, 64:284-289.
4. Avila I., et al. Beta frequency synchronization in basal ganglia output during rest and walk in a hemiparkinsonian rat. Exp. Neurol. 2010, 221:307-319.
5. Bar-Gad I., Bergman H. Stepping out of the box: information processing in the neural networks of the basal ganglia. Curr. Opin. Neurobiol. 2001, 11:689-695.
6. Bateup H.S., et al. Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14845-14850.
7. Bergman H., et al. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 1994, 72:507-520.
8. Bergman H., et al. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. 1998, 21:32-38.
9. Berke J.D. Fast oscillations in cortical-striatal networks switch frequency following rewarding events and stimulant drugs. Eur. J. Neurosci. 2009, 30:848-859.
10. Berke J.D., et al. Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 2004, 43:883-896.
11. Blesa J., et al. The nigrostriatal system in the presymptomatic and symptomatic stages in the MPTP monkey model: a PET, histological and biochemical study. Neurobiol. Dis. 2012, 48:79-91.
12. Brazhnik E., et al. Early Developing Motor Cortex-Basal Ganglia Synchrony in High Beta Frequency Range in the Rodent Model of Parkinson's Disease 2010, Society for Neuroscience, San Diego, CA, US.
13. Brazhnik E., et al. State-dependent spike and local field synchronization between motor cortex and substantia nigra in hemiparkinsonian rats. J. Neurosci. 2012, 32:7869-7880.
14. Brown P., et al. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J. Neurosci. 2001, 21:1033-1038.
15. Brown P., et al. Oscillatory local field potentials recorded from the subthalamic nucleus of the alert rat. Exp. Neurol. 2002, 177:581-585.
16. Cassidy M., et al. Movement-related changes in synchronization in the human basal ganglia. Brain 2002, 125:1235-1246.
17. Chevalier G., Deniau J.M. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 1990, 13:277-280.
18. Courtemanche R., et al. Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. J. Neurosci. 2003, 23:11741-11752.
19. Crossman A.R. A hypothesis on the pathophysiological mechanisms that underlie levodopa- or dopamine agonist-induced dyskinesia in Parkinson's disease: implications for future strategies in treatment. Mov. Disord. 1990, 5:100-108.
20. Cruz A.V., et al. Effects of dopamine depletion on information flow between the subthalamic nucleus and external globus pallidus. J. Neurophysiol. 2011, 106:2012-2023.
21. Damier P., et al. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 1999, 122(Pt 8):1437-1448.
22. Danish S.F., et al. High-frequency oscillations (>200Hz) in the human non-parkinsonian subthalamic nucleus. Brain Res. Bull. 2007, 74:84-90.
23. DeCoteau W.E., et al. Oscillations of local field potentials in the rat dorsal striatum during spontaneous and instructed behaviors. J. Neurophysiol. 2007, 97:3800-3805.
24. Degos B., et al. 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, 19:1616-1630.
25. Dejean C., et al. Evolution of the dynamic properties of the cortex-basal ganglia network after dopaminergic depletion in rats. Neurobiol. Dis. 2012, 46:402-413.
26. DeLong M.R. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990, 13:281-285.
27. Djaldetti R., et al. Residual striatal dopaminergic nerve terminals in very long-standing Parkinson's disease: a single photon emission computed tomography imaging study. Mov. Disord. 2011, 26:327-330.
28. Fearnley J.M., Lees A.J. Striatonigral degeneration. A clinicopathological study. Brain 1990, 113(Pt 6):1823-1842.
29. Fearnley J.M., Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991, 114(Pt 5):2283-2301.
30. Foffani G., et al. 300-Hz subthalamic oscillations in Parkinson's disease. Brain 2003, 126:2153-2163.
31. Gradinaru V., et al. Optical deconstruction of parkinsonian neural circuitry. Science 2009, 324:354-359.
32. Haber S.N., et al. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J. Neurosci. 2000, 20:2369-2382.
33. Halliday G.M., et al. Neuropathology of immunohistochemically identified brainstem neurons in Parkinson's disease. Ann. Neurol. 1990, 27:373-385.
34. Hariz M. Twenty-five years of deep brain stimulation: celebrations and apprehensions. Mov. Disord. 2012, 27:930-933.
35. Hashimoto T., et al. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J. Neurosci. 2003, 23:1916-1923.
36. Heimer G., et al. 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.
37. Hornykiewicz O. Chemical neuroanatomy of the basal ganglia-normal and in Parkinson's disease. J. Chem. Neuroanat. 2001, 22:3-12.
38. Israel Z., Bergman H. Pathophysiology of the basal ganglia and movement disorders: from animal models to human clinical applications. Neurosci. Biobehav. Rev. 2008, 32:367-377.
39. Jenkinson N., Brown P. New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci. 2011, 34:611-618.
40. Jenkinson N., Kühn A.A., Brown P. Gamma oscillations in the human basal ganglia. Exp. Neurol. 2012, 245:72-76.
41. Krack P., et al. Deep brain stimulation: from neurology to psychiatry?. Trends Neurosci. 2010, 33:474-484.
42. Kravitz A.V., et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010, 466:622-626.
43. Kuhn A.A., et al. Event-related beta desynchronization in human subthalamic nucleus correlates with motor performance. Brain 2004, 127:735-746.
44. Kuhn A.A., et al. 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.
45. Kuhn A.A., et al. Pathological synchronisation in the subthalamic nucleus of patients with Parkinson's disease relates to both bradykinesia and rigidity. Exp. Neurol. 2009, 215:380-387.
46. Leblois A., et al. Temporal and spatial alterations in GPi neuronal encoding might contribute to slow down movement in Parkinsonian monkeys. Eur. J. Neurosci. 2006, 24:1201-1208.
47. Leblois A., et al. Late emergence of synchronized oscillatory activity in the pallidum during progressive Parkinsonism. Eur. J. Neurosci. 2007, 26:1701-1713.
48. Lehericy S., et al. Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12566-12571.
49. Leventhal D.K., et al. Basal ganglia beta oscillations accompany cue utilization. Neuron 2012, 73:523-536.
50. Levy R., et al. High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J. Neurosci. 2000, 20:7766-7775.
51. Levy R., et al. Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. Brain 2002, 125:1196-1209.
52. Lopez-Azcarate J., et al. Coupling between beta and high-frequency activity in the human subthalamic nucleus may be a pathophysiological mechanism in Parkinson's disease. J. Neurosci. 2010, 30:6667-6677.
53. Magill P.J., et al. Relationship of activity in the subthalamic nucleus-globus pallidus network to cortical electroencephalogram. J. Neurosci. 2000, 20:820-833.
54. Magill P.J., et al. Delayed synchronization of activity in cortex and subthalamic nucleus following cortical stimulation in the rat. J. Physiol. 2006, 574:929-946.
55. Mallet N., et al. Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J. Neurosci. 2008, 28:14245-14258.
56. Mallet N., et al. Dichotomous organization of the external globus pallidus. Neuron 2012, 74:1075-1086.
57. Marsden C.D., Obeso J.A. The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. Brain 1994, 117(Pt 4):877-897.
58. Mazzoni P., et al. Why don't we move faster? Parkinson's disease, movement vigor, and implicit motivation. J. Neurosci. 2007, 27:7105-7116.
59. McHaffie J.G., et al. Subcortical loops through the basal ganglia. Trends Neurosci. 2005, 28:401-407.
60. Montgomery E.B. Basal ganglia physiology and pathophysiology: a reappraisal. Parkinsonism Relat. Disord. 2007, 13:455-465.
61. Moran R.J., et al. Alterations in brain connectivity underlying beta oscillations in Parkinsonism. PLoS Comput. Biol. 2011, 7:e1002124.
62. Nambu A. A new dynamic model of the cortico-basal ganglia loop. Prog. Brain Res. 2004, 143:461-466.
63. Nandhagopal R., et al. Longitudinal evolution of compensatory changes in striatal dopamine processing in Parkinson's disease. Brain 2011, 134:3290-3298.
64. Nini A., et al. Neurons in the globus pallidus do not show correlated activity in the normal monkey, but phase-locked oscillations appear in the MPTP model of parkinsonism. J. Neurophysiol. 1995, 74:1800-1805.
65. Novikov N., et al. Lack of Correlation Between Progressive Emergence of Motor Cortex-Basal Ganglia Synchrony in the High Beta/Low Gamma Frequency Range and Motor Deficits in Rodent Models of Parkinson's Disease 2012, Society for Neuroscience, New Orleans (US).
66. Obeso J.A., et al. Pathophysiology of levodopa-induced dyskinesias in Parkinson's disease: problems with the current model. Ann. Neurol. 2000, 47:S22-S32. (discussion S32-4).
67. Obeso J.A., et al. Pathophysiology of the basal ganglia in Parkinson's disease. Trends Neurosci. 2000, 23:S8-S19.
68. Penney J.B., Young A.B. Striatal inhomogeneities and basal ganglia function. Mov. Disord. 1986, 1:3-15.
69. Priori A., et al. 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(Suppl. 2):S101-S102.
70. Raz A., et al. Activity of pallidal and striatal tonically active neurons is correlated in MPTP-treated monkeys but not in normal monkeys. J. Neurosci. 2001, 21:RC128.
71. Redgrave P., et al. Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease. Nat. Rev. Neurosci. 2010, 11:760-772.
72. Rodriguez M., et al. Dopamine cell degeneration induced by intraventricular administration of 6-hydroxydopamine in the rat: similarities with cell loss in Parkinson's disease. Exp. Neurol. 2001, 169:163-181.
73. Rodriguez M., et al. Firing regulation in dopaminergic cells: effect of the partial degeneration of nigrostriatal system in surviving neurons. Eur. J. Neurosci. 2003, 18:53-60.
74. Rodriguez-Oroz M.C., et al. Involvement of the subthalamic nucleus in impulse control disorders associated with Parkinson's disease. Brain 2011, 134:36-49.
75. Ruskin D.N., et al. Nigrostriatal lesion and dopamine agonists affect firing patterns of rodent entopeduncular nucleus neurons. J. Neurophysiol. 2002, 88:487-496.
76. Sato F., et al. Axonal branching pattern of neurons of the subthalamic nucleus in primates. J. Comp. Neurol. 2000, 424:142-152.
77. Sharott A., et al. Directional analysis of coherent oscillatory field potentials in the cerebral cortex and basal ganglia of the rat. J. Physiol. 2005, 562:951-963.
78. Sharott A., et al. 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.
79. Shink E., et al. The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey. Neuroscience 1996, 73:335-357.
80. Stein E., Bar-Gad I. Beta oscillations in the cortico-basal ganglia loop during parkinsonism. Exp. Neurol. 2012, 245:52-59.
81. Tachibana Y., et al. Subthalamo-pallidal interactions underlying parkinsonian neuronal oscillations in the primate basal ganglia. Eur. J. Neurosci. 2011, 34:1470-1484.
82. Tseng K.Y., et al. Consequences of partial and severe dopaminergic lesion on basal ganglia oscillatory activity and akinesia. Eur. J. Neurosci. 2005, 22:2579-2586.
83. Urbain N., et al. Unrelated course of subthalamic nucleus and globus pallidus neuronal activities across vigilance states in the rat. Eur. J. Neurosci. 2000, 12:3361-3374.
84. Vitek J.L., et al. Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus. Ann. Neurol. 1999, 46:22-35.
85. Weinberger M., et al. Pedunculopontine nucleus microelectrode recordings in movement disorder patients. Exp. Brain Res. 2008, 188:165-174.
86. Weinberger M., et al. Oscillatory activity in the globus pallidus internus: comparison between Parkinson's disease and dystonia. Clin. Neurophysiol. 2012, 123:358-368.
87. Wichmann T., DeLong M.R. Pathophysiology of Parkinson's disease: the MPTP primate model of the human disorder. Ann. N. Y. Acad. Sci. 2003, 991:199-213.
88. Wichmann T., et al. The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J. Neurophysiol. 1994, 72:521-530.
89. Wichmann T., et al. Milestones in research on the pathophysiology of Parkinson's disease. Mov. Disord. 2011, 26:1032-1041.
90. Williams D., et al. Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 2002, 125:1558-1569.
91. Zaidel A., et al. Subthalamic span of beta oscillations predicts deep brain stimulation efficacy for patients with Parkinson's disease. Brain 2010, 133:2007-2021.