Changes to interneuron-driven striatal microcircuits in a rat model of Parkinson's disease

Neurobiology of Disease

Volumn 34, Issue 3, 2009, Pages 545-552

  Salin, Pascal ^a   López, Iciar P ^b   Kachidian, Philippe ^a   Barroso Chinea, Pedro ^b   Rico, Alberto J ^b   Gómez Bautista, Virginia ^b   Coulon, Patrice ^c   Kerkerian Le Goff, Lydia ^a   Lanciego, José L ^b  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b UNIVERSITY OF NAVARRA   (Spain)

^c AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Basal ganglia; Caudate putamen; ChAT; Dopamine; Rabies virus

Indexed keywords

DOPAMINE 2 RECEPTOR; OXIDOPAMINE; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CELL POPULATION; CHOLINERGIC NERVE; CONTROLLED STUDY; GLOBUS PALLIDUS; INTERNEURON; MALE; NERVE CELL NETWORK; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RABIES VIRUS; RAT; STRIATE CORTEX; SUBSTANTIA NIGRA; SYNAPTIC MEMBRANE; TISSUE DISTRIBUTION;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL COUNT; CHOLINE O-ACETYLTRANSFERASE; DENSITOMETRY; DISEASE MODELS, ANIMAL; GLOBUS PALLIDUS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; NITRIC OXIDE SYNTHASE TYPE I; OXIDOPAMINE; PARKINSON DISEASE; PARVALBUMINS; RABIES VIRUS; RATS; RATS, WISTAR; SUBSTANTIA NIGRA;

EID: 67349142082     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.03.006     Document Type: Article

References (46)

1. Aoki C., and Pickel V.M. Neuropeptide Y-containing neurons in the rat striatum: ultrastructure and cellular relations with tyrosine hydroxylase-containing terminals and with astrocytes. Brain Res. 459 (1988) 205-225
2. Bennet B.D., and Bolam J.P. Synaptic input and output of parvalbumin-immunoreactive neurons in the neostriatum of the rat. Neuroscience 62 (1994) 707-719
3. Calabresi P., Centonze D., Gubellini P., Pisani A., and Bernardi G. Acetylcholine-mediated modulation of striatal function. Trends Neurosci. 23 (2000) 120-126
4. Calabresi P., Picconi B., Parnetti L., and Di Filippo M. A convergent model for cognitive dysfunctions in Parkinson's disease: the critical dopamine-acetylcholine synaptic balance. Lancet Neurol. 5 (2006) 974-983
5. Cowan R.L., Wilson C.J., Emson P.C., and Heizmann C.W. Parvalbumin-containing GABAergic interneurons in the rat neostriatum. J. Comp. Neurol. 302 (1990) 197-205
6. 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., and Surmeier D.J. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat. Neurosci. 9 (2006) 251-259
7. Deniau J.M., Menetrey A., and Charpier S. The lamellar organization of the rat substantia nigra pars reticulata: segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections. Neuroscience 73 (1996) 761-781
8. Di Chiara G., Morelli M., and Consolo S. Modulatory functions of neurotransmitters in the striatum: ACh/dopamine/NMDA interactions. Trends Neurosci. 17 (1994) 228-233
9. Duvosin R.C. Cholinergic-anticholinergic antagonism in parkinsonism. Arch. Neurol. 17 (1967) 124-136
10. DiFiglia M., and Aronin N. Ultrastructural features of immunoreactive somatostatin neurons in the rat caudate nucleus. J. Neurosci. 9 (1982) 1267-1274
11. DiFiglia M., and Aronin N. Quantitative electron microscopic study of immunoreactive somatostatin axons in the rat neostriatum. Neurosci. Lett. 50 (1984) 325-331
12. Ferrario J.E., Rojas-Mayorquín A.E., Saldaña-Ortega M., Salum C., Gomes M.Z., Hunot S., and Raisman-Vozari R. Pleiotrophin receptor RPTP-zeta/beta expression is upregulated by L-DOPA in striatal medium spiny neurons of parkinsonian rats. J. Neurochem. 107 (2008) 443-452
13. Fukuda T. Network architecture of gap junction-coupled neuronal linkage in the striatum. J. Neurosci. 29 (2009) 1235-1243
14. Groves P.M.A. A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movements. Brain Res. 286 (1983) 109-132
15. Hornykiewicz O., and Kish S.J. Biochemical pathophysiology of Parkinson's disease. Adv. Neurol. 45 (1987) 19-34
16. Ingham C.A., Hodd S.H., Taggart P., and Arbuthnott G.W. Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway. J. Neurosci. 18 (1998) 4732-4743
17. Jaeger D., Kita H., and Wilson C.J. Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. J. Neurophysiol. 72 (1994) 2555-2558
18. Kawaguchi Y., Wilson C.J., Augood S.J., and Emson P.C. Striatal interneurons: chemical, physiological and morphological characterization. Trends Neurosci. 18 (1995) 527-535
19. Kelly R.M., and Strick P.L. Rabies as a transneuronal tracer of circuits in the central nervous system. J. Neurosci. Meth. 103 (2000) 63-71
20. Koos T., and Tepper J.M. Dual cholinergic control of fast-spiking interneurons in the rat neostriatum. J. Neurosci. 22 (2002) 529-535
21. Kubota Y., and Kawaguchi Y. Dependence of GABAergic synaptic areas on the interneuron type and target size. J. Neurosci. 20 (2000) 375-386
22. Lang A.E., and Lees A. Anticholinergic therapies in the treatment of Parkinson's disease. Mov. Disord. 17 (2002) S7-S12
23. Mallet N., Le Moine C., Charpier S., and Gonon F. Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J. Neurosci. 25 (2005) 3857-3869
24. Mallet N., Ballion B., Le Moine C., and Gonon F. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J. Neurosci. 26 (2006) 3875-3884
25. Morello M., Reiner A., Sancesario G., Karle E.J., and Bernardi G. Ultrastructural study of nitric oxide synthase-containing striatal neurons and their relationship with parvalbumin-containing neurons in rats. Brain Res. 776 (1997) 30-39
26. Muramatsu Y., Kurosaki R., Watanabe H., Michimata M., Matsubara M., Imai Y., and Araki T. Cerebral alterations in a MPTP-mouse model of Parkinson's disease - an immunocytochemical study. J. Neural. Transm. 110 (2003) 1129-1144
27. Pakhotin P., and Bracci E. Cholinergic interneurons control the excitatory input to the striatum. J. Neurosci. 27 (2007) 391-400
28. Pisani A., Bonsi P., Centonze D., Gubellini P., Bernardi G., and Calabresi P. Targeting striatal cholinergic interneurons in Parkinson's disease: focus on metabotropic glutamate receptors. Neuropharmacology 45 (2003) 45-56
29. Pisani A., Bernardi G., Ding J., and Surmeier D.J. Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci. 30 (2007) 545-553
30. Plenz D., and 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. 18 (1998) 266-283
31. Pollack A.E., and Wooten G.F. D2 dopaminergic regulation of striatal preproenkephalin mRNA levels is mediated at least in part through cholinergic interneurons. Mol. Brain Res. 13 (1992) 35-41
32. Raux H., Iseni F., Lafay F., and Blondel D. Mapping of monoclonal antibody epitopes of the rabies virus P protein. J. Gen. Virol. 78 (1997) 119-124
33. Salin P., Castle M., Kachidian P., Barroso-Chinea P., López I.P., Rico A.J., Kerkerian-Le Goff L., Coulon P., and Lanciego J.L. High-resolution neuronanatomical tract-tracing for the analysis of striatal microcircuits. Brain Res. 1221 (2008) 49-58
34. Shen W., Tian X., Day M., Ulrich S., Tkatch T., Nathanson N.M., and Surmeier D.J. Cholinergic modulation of Kir2 channels selectively elevates dendritic excitability in striatopallidal neurons. Nat. Neurosci. 10 (2007) 1458-1466
35. Taravini I.R.E., Ferrario J.E., Delbe J., Ginestet L., Debeir T., Courty J., Murer M.G., Gershanik O.S., and Raisman-Vozari R. Immunodetection of heparin-binding growth associated molecule (pleiotrophin) in striatal interneurons. Brain Res. 1066 (2005) 196-200
36. Tepper J.M., and Bolam J.P. Functional diversity and specificity of neostriatal interneurons. Curr. Opin. Neurobiol. 14 (2004) 685-692
37. Tepper J.M., Kóos T., and Wilson C.J. GABAergic microcircuits in the neostriatum. Trends Neurosci. 27 (2004) 662-669
38. Tepper J.M., Wilson C.J., and Koos T. Feedforward and feedback inhibition in neostriatal GABAergic spiny neurons. Brain Res. Rev. 58 (2008) 272-281
39. Ubol S., Hiriote W., Anuntagool N., and Utaisincharoen P. A radical form of nitric oxide suppresses RNA synthesis of rabies virus. Virus Res. 81 (2001) 125-132
40. Ugolini G. Use of rabies virus as a transneuronal tracer of neuronal connections: implications for the understanding of rabies pathogenesis. Dev. Biol. (Basel) 131 (2008) 493-506
41. Vuillet J., Kerkerian L., Salin P., and Nieoullon A. Ultrastructural features of NPY-containing neurons in the rat striatum. Brain Res. 477 (1989) 241-251
42. Vuillet J., Dimova R., Nieoullon A., and Kerkerian-Le Goff L. Ultrastructural relationships between choline acetyltransferase- and neuropeptide Y-containing neurons in the rat striatum. Neuroscience 46 (1992) 351-360
43. Wang Z., Kai L., Day M., Ronesi J., Yin H.H., Ding J., Tkatch T., Lovinger D.M., and Surmeier D.J. Dopaminergic control of corticostriatal long-term depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50 (2006) 443-452
44. Wilson C.J. Striatal D2 receptors and LTD: yes, but not where you thought they were. Neuron 50 (2006) 347-348
45. Wilson C.J. GABAergic inhibition in the neostriatum. Prog. Brain Res. 160 (2007) 91-110
46. Wilson C.J., and Phelan K.D. Dual topographic representation of neostriatum in the globus pallidus of rats. Brain Res. 243 (1982) 354-359