Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity

Journal of Neuroscience

Volumn 28, Issue 52, 2008, Pages 14245-14258

  Mallet, Nicolas ^a,b   Pogosyan, Alek ^b   Márton, László F ^a,c   Bolam, J Paul ^a   Brown, Peter ^b   Magill, Peter J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c SAPIENTIA HUNGARIAN UNIVERSITY OF TRANSYLVANIA   (Romania)

Author keywords

6 hydroxydopamine; Basal ganglia; Dopamine; Globus pallidus; Parkinson's disease; Subthalamic nucleus

Indexed keywords

DOPAMINE; OXIDOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASAL GANGLION; BETA RHYTHM; CELL SYNCHRONIZATION; DOPAMINERGIC NERVE CELL; FEEDBACK SYSTEM; GLOBUS PALLIDUS; HANDWRITING; MALE; NERVE CELL NETWORK; NERVE FIBER; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SLOW BRAIN WAVE; SUBTHALAMIC NUCLEUS;

ACTION POTENTIALS; ANIMALS; BETA RHYTHM; BIOLOGICAL CLOCKS; DISEASE MODELS, ANIMAL; GLOBUS PALLIDUS; MALE; NERVE NET; NEURAL PATHWAYS; NEURONS; OXIDOPAMINE; PARKINSONIAN DISORDERS; RATS; RATS, SPRAGUE-DAWLEY; SUBTHALAMIC NUCLEUS;

EID: 58149387591     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4199-08.2008     Document Type: Article

References (59)

1. Bar-Gad I, Ritov Y, Vaadia E, Bergman H (2001) Failure in identification of overlapping spikes from multiple neuron activity causes artificial correlations. J Neurosci Methods 107:1-13.
2. Bar-Gad I, Heimer G, Ritov Y, Bergman H (2003) Functional correlations between neighboring neurons in the primate globus pallidus are weak or nonexistent. J Neurosci 23:4012-4016.
3. Barthó P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsáki G (2004) Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 92:600-608.
4. Baufreton J, Atherton JF, Surmeier DJ, Bevan MD (2005) Enhancement of excitatory synaptic integration by GABAergic inhibition in the subthalamic nucleus. J Neurosci 25:8505-8517.
5. Belluscio MA, Kasanetz F, Riquelme LA, Murer MG (2003) Spreading of slow cortical rhythms to the basal ganglia output nuclei in rats with nigrostriatal lesions. Eur J Neurosci 17:1046-1052.
6. Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72:507-520.
7. Bergman H, Feingold A, Nini A, Raz A, Slovin H, Abeles M, Vaadia E (1998) Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci 21:32-38.
8. Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ (2002) Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci 25:525-531.
9. Bevan MD, Atherton JF, Baufreton J (2006) Cellular principles underlying normal and pathological activity in the subthalamic nucleus. Curr Opin Neurobiol 16:621-628.
10. Bolam JP, Hanley JJ, Booth PA, Bevan MD (2000) Synaptic organisation of the basal ganglia. J Anat 196:527-542.
11. Boraud T, Brown P, Goldberg JA, Graybiel AM, Magill PJ (2005) Oscillations in the basal ganglia: the good, the bad and the unexpected. In: The basal ganglia VIII (Bolam JP, Ingham CA, Magill PJ, eds), pp 3-24. New York: Springer Science and Business Media.
12. Brown P (2006) Bad oscillations in Parkinson's disease. J Neural Transm Suppl 70:27-30.
13. 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.
14. Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926-1929.
15. Costa RM, Lin SC, Sotnikova TD, Cyr M, Gainetdinov RR, Caron MG, Nicolelis MA (2006) Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction. Neuron 52:359-369.
16. Courtemanche R, Fujii N, Graybiel AM (2003) Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. J Neurosci 23:11741-11752.
17. DeLong MR (1971) Activity of pallidal neurons during movement. J Neurophysiol 34:414-427.
18. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281-285.
19. Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704-716.
20. Gatev P, Darbin O, Wichmann T (2006) Oscillations in the basal ganglia under normal conditions and in movement disorders. Mov Disord 21:1566-1577.
21. Halliday DM, Rosenberg JR, Amjad AM, Breeze P, Conway BA, Farmer SF (1995) A framework for the analysis of mixed time series/point process data-theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Prog Biophys Mol Biol 64:237-278.
22. Hammond C, Bergman H, Brown P (2007) Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci 30:357-364.
23. Johnson DH (1996) Point process models of single-neuron discharges. J Comput Neurosci 3:275-299.
24. Kita H, Kitai ST (1991) Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res 564:296-305.
25. Kita H, Kitai ST (1994) The morphology of globus pallidus projection neurons in the rat: an intracellular staining study. Brain Res 636:308-319.
26. Kühn AA, Trottenberg T, Kivi A, Kupsch A, Schneider GH, 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.
27. Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO (2002) Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. Brain 125:1196-1209.
28. Magill PJ, Bolam JP, Bevan MD (2001) Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network. Neuroscience 106:313-330.
29. Magill PJ, Sharott A, Bevan MD, Brown P, Bolam JP (2004) Synchronous unit activity and local field potentials evoked in the subthalamic nucleus by cortical stimulation. J Neurophysiol 92:700-714.
30. Magill PJ, Pogosyan A, Sharott A, Csicsvari J, Bolam JP, Brown P (2006) Changes in functional connectivity within the rat striatopallidal axis during global brain activation in vivo. J Neurosci 26:6318-6329.
31. Mallet N, Le Moine C, Charpier S, Gonon F (2005) Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J Neurosci 25:3857-3869.
32. Mallet N, Ballion B, Le Moine C, Gonon F (2006) Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci 26:3875-3884.
33. Mallet N, Pogosyan A, Sharott A, Csicsvari J, Bolam JP, Brown P, Magill PJ (2008) Disrupted dopamine transmission and the emergence of exaggerated beta oscillations in subthalamic nucleus and cerebral cortex. J Neurosci 28:4795-4806.
34. Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65:37-100.
35. Nambu A, Llinaś R (1994) Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol 72:1127-1139.
36. Nini A, Feingold A, Slovin H, Bergman H (1995) 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 74:1800-1805.
37. Oorschot DE (1996) Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: a stereological study using the cavalieri and optical disector methods. J Comp Neurol 366:580-599.
38. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, Ed 2. Sydney: Academic.
39. Paz JT, Deniau JM, Charpier S (2005) Rhythmic bursting in the cortico-subthalamo-pallidal network during spontaneous genetically determined spike and wave discharges. J Neurosci 25:2092-2101.
40. Plenz D, Kital ST (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400:677-682.
41. Rubino D, Robbins KA, Hatsopoulos NG (2006) Propagating waves mediate information transfer in the motor cortex. Nat Neurosci 9:1549-1557.
42. Sadek AR, Magill PJ, Bolam JP (2007) A single-cell analysis of intrinsic connectivity in the rat globus pallidus. J Neurosci 27:6352-6362.
43. Schnitzler A, Gross J (2005) Normal and pathological oscillatory communication in the brain. Nat Rev Neurosci 6:285-296.
44. Schwarting RK, Huston JP (1996a) Unilateral 6-hydroxydopamine lesions of meso-striatal dopamine neurons and their physiological sequelae. Prog Neurobiol 49:215-266.
45. Schwarting RK, Huston JP (1996b) The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments. Prog Neurobiol 50:275-331.
46. Sharott A, Magill PJ, Harnack D, Kupsch A, Meissner W, Brown P (2005) Dopamine depletion increases the power and coherence of beta-oscillations in the cerebral cortex and subthalamic nucleus of the awake rat. Eur J Neurosci 21:1413-1422.
47. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24:49-65, 111-125.
48. Smith Y, Bevan MD, Shink E, Bolam JP (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86:353-387.
49. Somogyi P, Klausberger T (2005) Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol 562:9-26.
50. Stanford IM (2003) Independent neuronal oscillators of the rat globus pallidus. J Neurophysiol 89:1713-1717.
51. Steriade M (2000) Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101:243-276.
52. Surmeier DJ, Mercer JN, Chan CS (2005) Autonomous pacemakers in the basal ganglia: who needs excitatory synapses anyway? Curr Opin Neurobiol 15:312-318.
53. 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.
54. Uhlhaas PJ, Singer W (2006) Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52:155-168.
55. Vila M, Périer C, Féger J, Yelnik J, Faucheux B, Ruberg M, Raisman-Vozari R, Agid Y, Hirsch EC (2000) Evolution of changes in neuronal activity in the subthalamic nucleus of rats with unilateral lesion of the substantia nigra assessed by metabolic and electrophysiological measurements. Eur J Neurosci 12:337-344.
56. Walters JR, Hu D, Itoga CA, Parr-Brownlie LC, Bergstrom DA (2007) 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 144:762-776.
57. Williams D, Tijssen M, Van Bruggen G, Bosch A, Insola A, Di Lazzaro V, Mazzone P, Oliviero A, Quartarone A, Speelman H, Brown P (2002) Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 125:1558-1569.
58. 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.
59. Zold CL, Ballion B, Riquelme LA, Gonon F, Murer MG (2007) Nigrostriatal lesion induces D2-modulated phase-locked activity in the basal ganglia of rats. Eur J Neurosci 25:2131-2144.