Striatal NMDA receptors gate cortico-pallidal synchronization in a rat model of Parkinson's disease

Neurobiology of Disease

Volumn 47, Issue 1, 2012, Pages 38-48

  Zold, Camila L ^a   Escande, Mariela V ^a   Pomata, Pablo E ^a,b   Riquelme, Luis A ^a   Murer, M Gustavo ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

Globus pallidus; Neuronal phase locking; Neuronal synchronization; NMDA receptor; Parkinson's disease; Striatum

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; CORTICAL SYNCHRONIZATION; GLOBUS PALLIDUS; HIGH FREQUENCY OSCILLATION; MALE; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; RECEPTOR UPREGULATION;

ANIMALS; BRAIN WAVES; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; GLOBUS PALLIDUS; MALE; NEOSTRIATUM; PARKINSON DISEASE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84861229307     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.03.022     Document Type: Article

References (61)

1. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. Chan C.S., Shigemoto R., Mercer J.N., Surmeier D.J. HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J. Neurosci. 2004, 24:9921-9932.
8. 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.
9. Costa R.M., Lin S.C., Sotnikova T.D., Cyr M., Gainetdinov R.R., Caron M.G., Nicolelis M.A. Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction. Neuron 2006, 52:359-369.
10. 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.
11. Dejean C., Gross C.E., Bioulac B., Boraud T. Dynamic changes in the cortex-basal ganglia network after dopamine depletion in the rat. J. Neurophysiol. 2008, 100:385-396.
12. Destexhe A., Hughes S.W., Rudolph M., Crunelli V. Are corticothalamic 'up' states fragments of wakefulness?. Trends Neurosci. 2007, 30:334-342.
13. Fisher N.I. Statistical Analysis of Circular Data/N.I. Fisher 1993, Cambridge University Press, New York.
14. Galiñanes G.L., Taravini I.R., Murer M.G. Dopamine-dependent periadolescent maturation of corticostriatal functional connectivity in mouse. J. Neurosci. 2009, 29:2496-2509.
15. Gatev P., Wichmann T. Interactions between cortical rhythms and spiking activity of single basal ganglia neurons in the normal and parkinsonian state. Cereb. Cortex 2009, 19:1330-1344.
16. Gittis A.H., Hang G.B., Ladow E.S., Shoenfeld L.R., Atallah B.V., Finkbeiner S., Kreitzer A.C. Rapid target-specific remodeling of fast-spiking inhibitory circuits after loss of dopamine. Neuron 2011, 71:858-868.
17. Goldberg J.A., Rokni U., Boraud T., Vaadia E., Bergman H. Spike synchronization in the cortex/basal-ganglia networks of Parkinsonian primates reflects global dynamics of the local field potentials. J. Neurosci. 2004, 24:6003-6010.
18. Gruber A.J., Hussain R.J., O'Donnell P. The nucleus accumbens: a switchboard for goal-directed behaviors. PLoS One 2009, 4:e5062.
19. Guehl D., Pessiglione M., François C., Yelnik J., Hirsch E.C., Féger J., Tremblay L. Tremor-related activity of neurons in the 'motor' thalamus: changes in firing rate and pattern in the MPTP vervet model of parkinsonism. Eur. J. Neurosci. 2003, 17:2388-2400.
20. Halliday D.M., Rosenberg J.R., Amjad A.M., Breeze P., Conway B.A., Farmer S.F. 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. 1995, 64:237-278.
21. Hammond C., Bergman H., Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci. 2007, 30:357-364.
22. 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.
23. Hutchison W.D., Lozano A.M., Tasker R.R., Lang A.E., Dostrovsky J.O. Identification and characterization of neurons with tremor-frequency activity in human globus pallidus. Exp. Brain Res. 1997, 113:557-563.
24. Hutchison W.D., Allan R.J., Opitz H., Levy R., Dostrovsky J.O., Lang A.E., Lozano A.M. Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson's disease. Ann. Neurol. 1998, 44:622-628.
25. 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. 2002, 543:577-589.
26. 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 basal ganglia circuitry. Nature 2010, 466:622-626.
27. 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.
28. Kühn 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.
29. Kumar A., Cardanobile S., Rotter S., Aertsen A. The role of inhibition in generating and controlling Parkinson's disease oscillations in the Basal Ganglia. Front. Syst. Neurosci. 2011, 5:86.
30. Kwak Y., Peltier S., Bohnen N.I., Müller M.L., Dayalu P., Seidler R.D. Altered resting state cortico-striatal connectivity in mild to moderate stage Parkinson's disease. Front. Syst. Neurosci. 2010, 4:143.
31. 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.
32. Lenz F.A., Tasker R.R., Kwan H.C., Schnider S., Kwong R., Murayama Y., Dostrovsky J.O., Murphy J.T. Single unit analysis of the human ventral thalamic nuclear group: correlation of thalamic "tremor cells" with the 3-6 Hz component of parkinsonian tremor. J. Neurosci. 1988, 8:754-764.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. Moran A., Bergman H., Israel Z., Bar-Gad I. Subthalamic nucleus functional organization revealed by parkinsonian neuronal oscillations and synchrony. Brain 2008, 131:3395-3409.
43. 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.
44. 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.
45. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1997, Academic Press, London. 3rd Edn.
46. 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.
47. Quiroga R.Q., Nadasdy Z., Ben-Shaul Y. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput. 2004, 16:1661-1687.
48. 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.
49. Rodriguez-Oroz M.C., Rodriguez M., Guridi J., Mewes K., Chockkman V., Vitek J., DeLong M.R., Obeso J.A. The subthalamic nucleus in Parkinson's disease: somatotopic organization and physiological characteristics. Brain 2001, 124:1777-1790.
50. Rosin B., Slovik M., Mitelman R., Rivlin-Etzion M., Haber S.N., Israel Z., Vaadia E., Bergman H. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron 2011, 72:370-384.
51. Shen W., Flajolet M., Greengard P., Surmeier D.J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 2008, 321:848-851.
52. Stanford I.M. Independent neuronal oscillators of the rat globus pallidus. J. Neurophysiol. 2003, 89:1713-1717.
53. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262:679-685.
54. Steriade M., Timofeev I., Grenier F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 2001, 85:1969-1985.
55. Stern E.A., Jaeger D., Wilson C.J. Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo. Nature 1998, 394:475-478.
56. Stoffers D., Bosboom J.L., Deijen J.B., Wolters E.C., Berendse H.W., Stam C.J. Slowing of oscillatory brain activity is a stable characteristic of Parkinson's disease without dementia. Brain 2007, 130:1847-1860.
57. Terman D., Rubin J.E., Yew A.C., Wilson C.J. Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J. Neurosci. 2002, 22:2963-2976.
58. 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.
59. 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.
60. 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.
61. 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.