Striatal gating through up states and oscillations in the basal ganglia: Implications for Parkinson's disease

Journal of Physiology Paris

Volumn 106, Issue 1-2, 2012, Pages 40-46

  Zold, Camila L ^a,b   Kasanetz, Fernando ^a,c   Pomata, Pablo E ^a,d   Belluscio, Mariano A ^a,e   Escande, Mariela V ^a   Galinanes, Gregorio L ^a   Riquelme, Luis A ^a   Murer, Mario Gustavo ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^e RUTGERS UNIVERSITY   (United States)

Author keywords

Basal ganglia; Globus pallidus; Medium spiny neuron; Oscillations; Parkinson's disease

Indexed keywords

DOPAMINE 2 RECEPTOR; DOPAMINE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN FUNCTION; CORPUS STRIATUM; CORTICAL SYNCHRONIZATION; DISEASE COURSE; ELECTROENCEPHALOGRAM; ENZYME REGULATION; GLOBUS PALLIDUS; MEDIUM SPINY PROJECTION NEURON; NERVE CELL; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NERVE CONDUCTION; NERVE PROJECTION; NEUROIMAGING; NEUROPATHOLOGY; NONHUMAN; OSCILLATION; PARKINSON DISEASE; SIGNAL TRANSDUCTION; STRIATAL GATING; THALAMOCORTICAL TRACT; UPREGULATION;

ANIMALS; BASAL GANGLIA; BIOLOGICAL CLOCKS; CORPUS STRIATUM; EXCITATORY AMINO ACID AGENTS; HUMANS; ION CHANNEL GATING; NEURONS; PARKINSON DISEASE; RECEPTORS, DOPAMINE D2; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84861200180     PISSN: 09284257     EISSN: 17697115     Source Type: Journal    
DOI: 10.1016/j.jphysparis.2011.06.002     Document Type: Article

References (71)

1. Aizman O., Brismar H., Uhlén P., Zettergren E., Levey A.I., Forssberg H., Greengard P., Aperia A. Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons. Nat. Neurosci. 2000, 3:226-230.
2. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
3. Ballion B., Mallet N., Bézard E., Lanciego J.L., Gonon F. Intratelencephalic corticostriatal neurons equally excite striatonigral and striatopallidal neurons and their discharge activity is selectively reduced in experimental parkinsonism. Eur. J. Neurosci. 2008, 27:2313-2321.
4. Ballion B., Frenois F., Zold C.L., Chetrit J., Murer M.G., Gonon F. D2 receptor stimulation, but not D1, restores striatal equilibrium in a rat model of Parkinsonism. Neurobiol. Dis. 2009, 35:376-384.
5. Bamford N.S., Zhang H., Schmitz Y., Wu N.P., Cepeda C., Levine M.S., Schmauss C., Zakharenko S.S., Zablow L., Sulzer D. Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 2004, 42:653-663.
6. Belluscio M.A., Kasanetz F., Riquelme L.A., Murer M.G. Spreading of slow cortical rhythms to the basal ganglia output nuclei in rats with nigrostriatal lesions. Eur. J. Neurosci. 2003, 17:1046-1052.
7. Belluscio M.A., Riquelme L.A., Murer M.G. Striatal dysfunction increases basal ganglia output during motor cortex activation in parkinsonian rats. Eur. J. Neurosci. 2007, 25:2791-2804.
8. Bergman H., Wichmann T., DeLong M.R. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990, 249:1436-1438.
9. Bergman H., Feingold A., Nini A., Raz A., Slovin H., Abeles M., Vaadia E. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. 1998, 21:32-38.
10. Bevan M.D., Magill P.J., Terman D., Bolam J.P., Wilson C.J. Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci. 2002, 25:525-531.
11. Bolam J.P., Hanley J.J., Booth P.A., Bevan M.D. Synaptic organisation of the basal ganglia. J. Anat. 2000, 196:527-542.
12. Brown P., Marsden C.D. What do the basal ganglia do?. Lancet 1998, 351:1801-1804.
13. Cenci M.A., Whishaw I.Q., Schallert T. Animal models of neurological deficits: how relevant is the rat?. Nat. Rev. Neurosci. 2002, 3:574-579.
14. Chan C.S., Glajch K.E., Gertler T.S., Guzman J.N., Mercer J.N., Lewis A.S., Goldberg A.B., Tkatch T., Shigemoto R., Fleming S.M., Chetkovich D.M., Osten P., Kita H., Surmeier D.J. HCN channelopathy in external globus pallidus neurons in models of Parkinson's disease. Nat. Neurosci. 2011, 14:85-92.
15. Chesselet M.F., Delfs J.M. Basal ganglia and movement disorders: an update. Trends Neurosci. 1996, 19:417-422.
16. Day M., Wang Z., Ding J., An X., Ingham C.A., Shering A.F., Wokosin D., Ilijic E., Sun Z., Sampson A.R., Mugnaini E., Deutch A.Y., Sesack S.R., Arbuthnott G.W., Surmeier D.J. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat. Neurosci. 2006, 9:251-259.
17. Day M., Wokosin D., Plotkin J.L., Tian X., Surmeier D.J. Differential excitability and modulation of striatal medium spiny neuron dendrites. J. Neurosci. 2008, 28:11603-11614.
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, 19:1616-1630.
19. Destexhe A., Hughes S.W., Rudolph M., Crunelli V. Are corticothalamic 'up' states fragments of wakefulness?. Trends Neurosci. 2007, 30:334-342.
20. Escande M.V., Zold C.L., Riquelme L.A., Belforte J.E., Murer M.G. Mechanisms underlying pathological oscillations in the rat 6-hydroxydopamine model of Parkinson's disease. Poster 477. 14th International Congress of Parkinson's Disease and Movement Disorders. Mov. Disord. 2010, 25(Suppl. 2):S339.
21. Ferezou I., Haiss F., Gentet L.J., Aronoff R., Weber B., Petersen C.C. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 2007, 56:907-923.
22. Gerdeman G.L., Ronesi J., Lovinger D.M. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 2002, 5:446-451.
23. Gerfen C.R., Surmeier D.J. Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci. 2011, 34:441-466.
24. Goto Y., O'Donnell P. Synchronous activity in the hippocampus and nucleus accumbens in vivo. J. Neurosci. 2001, 21:RC131.
25. Gradinaru V., Mogri M., Thompson K.R., Henderson J.M., Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science 2009, 324:354-359.
26. Hammond C., Bergman H., Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci. 2007, 30:357-364.
27. Hernandez-Lopez S., Bargas J., Surmeier D.J., Reyes A., Galarraga E. D1 receptor activation enhances evoked discharge in neostriatal medium spiny neurons by modulating an L-type Ca2+ conductance. J. Neurosci. 1997, 17:3334-3342.
28. Hernandez-Lopez S., Tkatch T., Perez-Garci E., Galarraga E., Bargas J., Hamm H., Surmeier D.J. D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability via a novel PLC[beta]1-IP3-calcineurin-signaling cascade. J. Neurosci. 2000, 20:8987-8995.
29. Higley M.J., Sabatini B.L. Competitive regulation of synaptic Ca2+ influx by D2 dopamine and A2A adenosine receptors. Nat. Neurosci. 2010, 13:958-966.
30. Hutchison W.D., Dostrovsky J.O., Walters J.R., Courtemanche R., Boraud T., Goldberg J., Brown P. Neuronal oscillations in the basal ganglia and movement disorders: evidence from whole animal and human recordings. J. Neurosci. 2004, 24:9240-9343.
31. 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.
32. Kasanetz F., Riquelme L.A., Murer M.G. Disruption of the two-state membrane potential of striatal neurones during cortical desynchronisation in anaesthetized rats. J. Physiol. (London) 2002, 543:577-589.
33. Kasanetz F., Riquelme L.A., O'Donnell P., Murer M.G. Turning off cortical ensembles stops striatal up states and elicits phase perturbations in cortical and striatal slow oscillations in rat in vivo. J. Physiol. (London) 2006, 577:97-113.
34. Kasanetz F., Riquelme L.A., Della-Maggiore V., O'Donnell P., Murer M.G. Functional integration across a gradient of corticostriatal channels controls UP state transitions in the dorsal striatum. Proc. Natl. Acad. Sci. USA 2008, 105:8124-8129.
35. Kitai S.T., Surmeier D.J. Cholinergic and dopaminergic modulation of potassium conductances in neostriatal neurons. Adv. Neurol. 1993, 60:40-52.
36. Kravitz A.V., Freeze B.S., Parker P.R., Kay K., Thwin M.T., Deisseroth K., Kreitzer A.C. Regulation of parkinsonian motor behaviours by optogenetic control of basalganglia circuitry. Nature 2010, 466:622-626.
37. Kreitzer A.C., Malenka R.C. Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J. Neurosci. 2005, 25. 10537-10345.
38. Kreitzer A.C., Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 2007, 445:643-647.
39. 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.
40. 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.
41. Levy R., Hazrati L.N., Herrero M.T., Vila M., Hassani O.K., Mouroux M., Ruberg M., Asensi H., Agid Y., Féger J., Obeso J.A., Parent A., Hirsch E.C. Re-evaluation of the functional anatomy of the basal ganglia in normal and parkinsonian states. Neuroscience 1997, 76:335-343.
42. Liu X.Y., Chu X.P., Mao L.M., Wang M., Lan H.X., Li M.H., Zhang G.C., Parelkar N.K., Fibuch E.E., Haines M., Neve K.A., Liu F., Xiong Z.G., Wang J.Q. Modulation of D2R-NR2B interactions in response to cocaine. Neuron 2006, 52:897-909.
43. Mahon S., Deniau J.M., Charpier S. Relationship between EEG potentials and intracellular activity of striatal and cortico-striatal neurons: an in vivo study under different anesthetics. Cereb. Cortex. 2001, 11:360-373.
44. Mahon S., Vautrelle N., Pezard L., Slaght S.J., Deniau J.M., Chouvet G., Charpier S. Distinct patterns of striatal medium spiny neuron activity during the natural sleep-wake cycle. J. Neurosci. 2006, 26:12587-12595.
45. Mallet N., Ballion B., Le Moine C., Gonon F. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J. Neurosci. 2006, 26:3875-3884.
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. Mink J.W. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 1996, 50:381-425.
49. 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. Erratum in: Cell Mol. Neurobiol. 2003 Jun;23 (3), 449.
50. Nambu A. A new dynamic model of the cortico-basal ganglia loop. Prog. Brain Res. 2004, 143:461-466.
51. O'Donnell P., Grace A.A. Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J. Neurosci. 1995, 15:3622-3639.
52. Plenz D., Kitai S.T. Up and down states in striatal medium spiny neurons simultaneously recorded with spontaneous activity in fast-spiking interneurons studied in cortex-striatum-substantia nigra organotypic cultures. J. Neurosci. 1998, 18:266-283.
53. Pomata P.E., Belluscio M.A., Riquelme L.A., Murer M.G. NMDA receptor gating of information flow through the striatum in vivo. J. Neurosci. 2008, 28:13384-13389.
54. Ponce F.A., Lozano A.M. Deep brain stimulation state of the art and novel stimulation targets. Prog. Brain Res. 2010, 184:311-324.
55. Schwarting R.K., Huston J.P. The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments. Prog. Neurobiol. 1996, 50:275-331.
56. Shen W., Flajolet M., Greengard P., Surmeier D.J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 2008, 321:848-851.
57. Soares J., Kliem M.A., Betarbet R., Greenamyre J.T., Yamamoto B., Wichmann T. Role of external pallidal segment in primate parkinsonism: comparison of the effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonism and lesions of the external pallidal segment. J. Neurosci. 2004, 24:6417-6426.
58. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262:679-685.
59. Steriade M., Timofeev I., Grenier F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 2001, 85:1969-1985.
60. Surmeier D.J., Song W.J., Yan Z. Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J. Neurosci. 1996, 16:6579-6591.
61. 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.
62. Vergara R., Rick C., Hernandez-Lopez S., Laville J.A., Guzman J.N., Galarraga E., Surmeier D.J., Bargas J. Spontaneous voltage oscillations in striatal projection neurons in a rat corticostriatal slice. J. Physiol. (London) 2003, 553:169-182.
63. Vyazovskiy V.V., Olcese U., Hanlon E.C., Nir Y., Cirelli C., Tononi G. Local sleep in awake rats. Nature 2011, 472:443-447.
64. 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.
65. Wang Z., Kai L., Day M., Ronesi J., Yin H.H., Ding J., Tkatch T., Lovinger D.M., Surmeier D.J. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 2006, 50:443-452.
66. Wilson C.J. The generation of natural firing patterns in neostriatal neurons. Prog. Brain Res. 1993, 99:277-297.
67. Wilson C.J., Groves P.M. Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Res. 1981, 220:67-80.
68. Wolf J.A., Moyer J.T., Lazarewicz M.T., Contreras D., Benoit-Marand M., O'Donnell P., Finkel L.H. NMDA/AMPA ratio impacts state transitions and entrainment to oscillations in a computational model of the nucleus accumbens medium spiny projection neuron. J. Neurosci. 2005, 25:9080-9095.
69. Zold, C., Riquelme, L., Murer, M.G., 2005. Switch from Excitatory to Inhibitory Cortical Control of GP Neurons Activity in 6-OHDA Rats. Program No. 330.6. Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington, DC (Online).
70. Zold C.L., Ballion B., Riquelme L.A., Gonon F., Murer M.G. Nigrostriatal lesion induces D2-modulated phase-locked activity in the basal ganglia of rats. Eur. J. Neurosci. 2007, 25:2131-2144.
71. Zold C.L., Larramendy C., Riquelme L.A., Murer M.G. Distinct changes in evoked and resting globus pallidus activity in early and late Parkinson's disease experimental models. Eur. J. Neurosci. 2007, 26:1267-1279.