Frequency selectivity and dopamine-dependence of plasticity at glutamatergic synapses in the subthalamic nucleus

Neuroscience

Volumn 203, Issue , 2012, Pages 1-11

  Yamawaki, N ^a   Magill, P J ^b   Woodhall, G L ^a   Hall, S D ^a   Stanford, I M ^a  

^a ASTON UNIVERSITY   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

6 hyroxydopamine; Deep brain stimulation; Primary motor cortex; Subthalamic nucleus

Indexed keywords

DOPAMINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN REGION; BRAIN SLICE; CENTRAL NERVOUS SYSTEM DEPRESSION; CONTROLLED STUDY; DOPAMINE BRAIN LEVEL; DOPAMINERGIC SYSTEM; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GLUTAMATERGIC SYNAPSE; HIGH FREQUENCT STIMULATION; LOW FREQUENCT STIMULATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SUBTHALAMIC NUCLEUS; SYNAPSE;

ANIMALS; DOPAMINE; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; MALE; NEURONAL PLASTICITY; NEURONS; ORGAN CULTURE TECHNIQUES; OXIDOPAMINE; PARKINSON DISEASE, SECONDARY; RATS; RATS, WISTAR; SUBTHALAMIC NUCLEUS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84856463419     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.12.027     Document Type: Article

References (70)

1. Ammari R., Bioulac B., Garcia L., Hammond C. The subthalamic nucleus becomes a generator of bursts in the dopamine-depleted state. Its high frequency stimulation dramatically weakens transmission to the globus pallidus. Front Syst Neurosci 2011, 5:43.
2. Bekkers J.M., Stevens C.F. Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 1990, 346:724-729.
3. Benazzouz A., Gross C., Féger J., Boraud T., Bioulac B. Reversal of rigidity and improvement in motor performance by subthalamic high-frequency stimulation in MPTP-treated monkeys. Eur J Neurosci 1993, 5(4):382-389.
4. Benazzouz A., Hallett M. Mechanism of action of deep brain stimulation. Neurology 2000, 55(12 Suppl 6):S13-S16.
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. Bevan M.D., Francis C.M., Bolam J.P. The glutamate-enriched cortical and thalamic input to neurons in the subthalamic nucleus of the rat: convergence with GABA-positive terminals. J Comp Neurol 1995, 361(3):491-511.
7. Bevan M.D., Bolam J.P. Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J Neurosci 1995, 15(11):7105-7120.
8. Bevan M.D., Magill P.J., Hallworth N.E., Bolam J.P., Wilson C.J. Regulation of the timing and pattern of action potential generation in rat subthalamic neurones in vitro by GABA-A IPSPs. J Neurophysiol 2002, 87:1348-1362.
9. Beurrier C., Congar P., Bioulac B., Hammond C. Subthalamic nucleus neurones switch from single-spike activity to burst-firing mode. J Neurosci 1999, 19(2):599-609.
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. Calabresi P., Maj R., Pisani A., Mercuri N.B., Bernardi G. Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 1992, 12(11):4224-4233.
12. Calabresi P., Saiardi A., Pisani A., Baik J.H., Centonze D., Mercuri N.B., Bernardi G., Borrelli E. Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J Neurosci 1997, 17(12):4536-4544.
13. Calabresi P., Centonze D., Gubellini P., Marfia G.A., Pisani A., Sancesario G., Bernardi G. Synaptic transmission in the striatum: from plasticity to neurodegeneration. Prog Neurobiol 2000, 61(3):231-265.
14. Cragg S.J., Baufreton J., Xue Y., Bolam J.P., Bevan M.D. Synaptic release of dopamine in the subthalamic nucleus. Eur J Neurosci 2004, 20(7):1788-1802.
15. Deniau J.M., Degos B., Bosch C., Maurice N. Deep brain stimulation mechanisms: beyond the concept of local functional inhibition. Eur J Neurosci 2010, 32(7):1080-1091.
16. Drouot X., Oshino S., Jarraya B., Besret L., Kishima H., Remy P., Dauguet J., Lefaucheur J.P., Dolle F., Conde F., Bottlaender M., Peschanski M., Keravel Y., Hantraye P., Palfi S. Functional recovery in a primate model of Parkinson's disease following motor cortex stimulation. Neuron 2004, 5:769-778.
17. Eusebio A., Chen C.C., Lu C.S., Lee S.T., Tsai C.H., Limousin P., Hariz M., Brown P. Effects of low-frequency stimulation of the subthalamic nucleus on movement in Parkinson's disease. Exp Neurol 2008, 209(1):125-130.
18. Eusebio A., Thevathasan W., Doyle Gaynor L., Pogosyan A., Bye E., Foltynie T., Zrinzo L., Ashkan K., Aziz T., Brown P. Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. J Neurol Neurosurg Psychiatry 2011, 82(5):569-573.
19. Filion M., Tremblay L. Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 1991, 547:142-151.
20. Fogelson N., Pogosyan A., Kühn A.A., Kupsch A., van Bruggen G., Speelman H., Tijssen M., Quartarone A., Insola A., Mazzone P., Di Lazzaro V., Limousin P., Brown P. Reciprocal interactions between oscillatory activities of different frequencies in the subthalamic region of patients with Parkinson's disease. Eur J Neurosci 2005, 22(1):257-266.
21. Fregni F., Boggio P.S., Santos M.C., Lima M., Vieira A.L., Rigonatti S.P., Silva M.T., Barbosa E.R., Nitsche M.A., Pascual-Leone A. Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson's disease. Mov Disord 2006, 21(10):1693-1702.
22. Fujimoto K., Kita H. Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res 1993, 609(1-2):185-192.
23. Gaynor L.M., Kühn A.A., Dileone M., Litvak V., Eusebio A., Pogosyan A., Androulidakis A.G., Tisch S., Limousin P., Insola A., Mazzone P., Di Lazzaro V., Brown P. Suppression of beta oscillations in the subthalamic nucleus following cortical stimulation in humans. Eur J Neurosci 2008, 28(8):1686-1695.
24. Gradinaru V., Mogri M., Thompson K.R., Henderson J.M., Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science 2009, 324(5925):354-359.
25. Hammond C., Bergman H., Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci 2007, 30:357-364.
26. Hammond C., Ammari R., Bioulac B., Garcia L. Latest view on the mechanism of action of deep brain stimulation. Mov Disord 2008, 23(15):2111-2121.
27. Khedr E.M., Farweez H.M., Islam H. Therapeutic effect of repetitive transcranial magnetic stimulation on motor function in Parkinson's disease patients. Eur J Neurol 2003, 10(5):567-572.
28. Kim J., Alger B.E. Random response fluctuations lead to spurious paired-pulse facilitation. J Neurosci 2001, 21:9608-9619.
29. Kitai S.T., Deniau J.M. Cortical inputs to the subthalamus: intracellular analysis. Brain Res 1981, 214(2):411-415.
30. Krack P., Fraix V., Mendes A., Benabid A.L., Pollak P. Post-operative management of subthalamic nucleus stimulation for Parkinson's disease. Mov Disord 2002, 17(Suppl 3):S188-S197.
31. 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., Pollak P. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 2003, 349(20):1925-1934.
32. Kreitzer A.C., Malenka R.C. Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J Neurosci 2005, 25(45):10537-10545.
33. Kreitzer A.C., Malenka R.C. Striatal plasticity and basal ganglia circuit function. Neuron 2008, 60(4):543-554.
34. Kühn A.A., Kupsch A., Schneider G.H., Brown P. Reduction in subthalamic 8-35 Hz oscillatory activity correlates with clinical improvement in Parkinson's disease. Eur J Neurosci 2006, 23(7):1956-1960.
35. Kühn A.A., Tsui A., Aziz T., Ray N., Brücke 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(2):380-387.
36. Lefaucheur J.P., Drouot X., Von Raison F., Ménard-Lefaucheur I., Cesaro P., Nguyen J.P. Improvement of motor performance and modulation of cortical excitability by repetitive transcranial magnetic stimulation of the motor cortex in Parkinson's disease. Clin Neurophysiol 2004, 115(11):2530-2541.
37. 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(3):1811-1820.
38. Levy R., Hutchison W.D., Lozano A.M., Dostrovsky J.O. High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J Neurosci 2000, 20:7766-7775.
39. Li S., Arbuthnott G.W., Jutras M.J., Goldberg J.A., Jaeger D.J. Resonant antidromic cortical circuit activation as a consequence of high-frequency subthalamic deep-brain stimulation. J Neurophysiol 2007, 98(6):3525-3537.
40. 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.
41. Loucif K.C., Wilson C.L., Baig R., Lacey M.G., Stanford I.M. Functional interconnectivity between the globus pallidus and the subthalamic nucleus in the mouse brain slice. J Physiol 2005, 567:977-987.
42. Loucif A.J., Woodhall G.L., Sehirli U.S., Stanford I.M. Depolarisation and suppression of burst firing in the mouse subthalamic nucleus by dopamine D1/D5 receptor activation of a cyclic nucleotide gated non-specific cation conductance. Neuropharmacology 2008, 55:94-105.
43. Magill P.J., Bolam J.P., Bevan M.D. Relationship of activity in the subthalamic nucleus-globus pallidus network to cortical electroencephalogram. J Neurosci 2000, 20:820-833.
44. Magill P.J., Bolam J.P., Bevan M.D. Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network. Neuroscience 2001, 106:313-330.
45. Magill P.J., Sharott A., Bevan M.D., Brown P., Bolam J.P. Synchronous unit activity and local field potentials evoked in the subthalamic nucleus by cortical stimulation. J Neurophysiol 2004, 92(2):700-714.
46. Mallet N., Pogosyan A., Márton 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.
47. 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.
48. Maurice N., Deniau J.M., Glowinski J., Thierry A.M. Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J Neurosci 1998, 18:9539-9546.
49. 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:e1002124.
50. Moro E., Esselink R.J., Xie J., Hommel M., Benabid A.L., Pollak P. The impact on Parkinson's disease of electrical parameter settings in STN stimulation. Neurology 2002, 59(5):706-713.
51. Nakanishi H., Kita H., Kitai S.T. Electrical membrane properties of rat subthalamic neurones in an in vitro slice preparation. Brain Res 1987, 437:35-44.
52. Nambu A., Tokuno H., Hamada I., Kita H., Imanishi M., Akazawa T., Ikeuchi Y., Hasegawa N. Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J Neurophysiol 2000, 84(1):289-300.
53. Nini A., Feingold A., Slovin H., Bergman H. 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(4):1800-1805.
54. Olsson M., Nikkhah G., Bentlage C., Björklund 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(5):3863-3875.
55. Pagni C.A., Zeme S., Zenga F. Further experience with extradural motor cortex stimulation for the treatment of advanced Parkinson's disease: report of 3 new cases. J Neurosurg Sci 2003, 47:189-193.
56. Pagni C.A., Zeme S., Zenga F., Maina R. Extradural motor cortex stimulation in advanced Parkinson's disease: the Turin experience: technical case report. Neurosurgery 2005, 57(4):E402.
57. Pan H.S., Walters J.R. Unilateral lesion of the nigrostriatal pathway decreases the firing rate and alters the firing pattern of globus pallidus neurons in the rat. Synapse 1988, 2(6):650-656.
58. Plenz D., Kitai S.T. A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 1999, 400:677-682.
59. 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(2):369-379.
60. Schwarting R.K., Huston J.P. Behavioral and neurochemical dynamics of neurotoxic meso-striatal dopamine lesions. Neurotoxicology 1997, 18(3):689-708.
61. 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(5):413-422.
62. Shen K.Z., Johnson S.W. Presynaptic dopamine D2 and muscarine M3 receptors inhibit excitatory and inhibitory transmission to rat subthalamic neurones in vitro. J Physiol 2000, 525(2):331-341.
63. Shen K.Z., Zhu Z.T., Munhall A., Johnson S.W. Synaptic plasticity in rat subthalamic nucleus induced by high-frequency stimulation. Synapse 2003, 50(4):314-319.
64. Shen W., Flajolet M., Greengard P., Surmeier D.J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 2008, 321(5890):848-851.
65. Siebner H.R., Rossmeier C., Mentschel C., Peinemann A., Conrad B. Short-term motor improvement after sub-threshold 5-Hz repetitive transcranial magnetic stimulation of the primary motor hand area in Parkinson's disease. J Neurol Sci 2000, 178(2):91-94.
66. Smith Y., Bevan M.D., Shink E., Bolam J.P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 1998, 86(2):353-387.
67. Temeperli P., Ghika J., Villemure J.G., Burkhard P.R., Bogousslavsky J., Vingerhoets F.J. How do parkinsonian signs return after discontinuation of subthalamic DBS?. Neurology 2003, 60:78-81.
68. Thomson A.M. Molecular frequency filters at central synapses. Prog Neurobiol 2000, 62:159-196.
69. Tseng K.Y., Kargieman L., Gacio S., Riquelme L.A., Murer M.G. Consequences of partial and severe dopaminergic lesion on basal ganglia oscillatory activity and akinesia. Eur J Neurosci 2005, 22:2579-2586.
70. Vila M., Périer C., Féger J., Yelnik J., Faucheux B., Ruberg M., Raisman-Vozari R., Agid Y., Hirsch E.C. 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 2000, 12:337-344.