Striatal GPR88 expression is confined to the whole projection neuron population and is regulated by dopaminergic and glutamatergic afferents

European Journal of Neuroscience

Volumn 30, Issue 3, 2009, Pages 397-414

  Massart, Renaud ^a,b   Guilloux, Jean Philippe ^a   Mignon, Virginie ^a   Sokoloff, Pierre ^b   Diaz, Jorge ^a  

^a INSERM   (France)

^b INSTITUT DE RECHERCHE PIERRE FABRE   (France)

Author keywords

6 hydroxydopamine; Basal ganglia; G protein coupled receptor; Immunoreactivity; L DOPA; Primate; Rat

Indexed keywords

DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 88; LEVODOPA; PREPROTACHYKININ; SUBSTANCE P; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITE; DENDRITIC SPINE; DOPAMINERGIC NERVE CELL; IMMUNOREACTIVITY; MALE; MONKEY; NONHUMAN; PARKINSON DISEASE; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; TISSUE SPECIFICITY;

ANIMALS; CORPUS STRIATUM; DENDRITES; DOPAMINE; DOPAMINE AGENTS; FLUORESCENT ANTIBODY TECHNIQUE; GLUTAMINE; HAPLORHINI; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LEVODOPA; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS, AFFERENT; PARKINSONIAN DISORDERS; RATS; RATS, WISTAR; RECEPTORS, G-PROTEIN-COUPLED;

EID: 68249103429     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06842.x     Document Type: Article

References (94)

1. Arbuthnott, G.W., Ingham, C.A. Wickens, J.R. (2000) Dopamine and synaptic plasticity in the neostriatum. J. Anat., 196, 587 596.
2. Avila-Costa, M.R., Coli'n-Barenque, L., Aley-Medina, P., Valdez, A.L., Librado, J.L., Martinez, E.F. Fortoul, T.I. (2005) Bilateral increase of perforated synapses after unilateral dopamine depletion. Int. J. Neurosci., 115, 79 86.
3. Bamford, N.S., Zhang, H., Schmitz, Y., Wu, N.P., Cepeda, C., Levine, M.S., Schmauss, C., Zakharenko, S.S., Zablow, L. Sulzer, D. (2004) Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron, 42, 653 663.
4. Befort, K., Filliol, D., Ghate, A., Darcq, E., Matifas, A., Muller, J., Lardenois, A., Thibault, C., Dembele, D., Le Merrer, J., Becker, J.A.J., Poch, O. Kieffer, B.L. (2008) Mu-opioid receptor activation induces transcriptional plasticity in the central extended amygdala. Eur. J. Neurosci., 27, 2973 2984.
5. Bernard, V., Décossas, M., Liste, I. Bloch, B. (2006) Intraneuronal trafficking of G-protein-coupled receptors in vivo. Trends Neurosci., 29, 140 147.
6. Bézard, E., Ferry, S., Mach, U., Stark, H., Leriche, L., Boraud, T., Gross, C. Sokoloff, P. (2003) Attenuation of levodopa-induced dyskinesia by normalizing dopamine D3 receptor function. Nat. Med., 9, 762 767.
7. Blandini, F., Fancellu, R., Orzi, F., Conti, G., Greco, R., Tassorelli, C. Nappi, G. (2003) Selective stimulation of striatal dopamine receptors of the D1 or D2-class causes opposite changes of fos expression in the rat cerebral cortex. Eur. J. Neurosci., 17, 763 770.
8. Boehm, C., Newrzella, D., Herberger, S., Schramm, N., Eisenhardt, G., Schenk, V., Sonntag-Buck, V. Sorgenfrei, O. (2006) Effects of antidepressant treatment on gene expression profile in mouse brain: cell type-specific transcription profiling using laser microdissection and microarray analysis. J. Neurochem., 97 (Suppl. 1 44 49.
9. Bolam, J.P., Somogyi, P., Takagi, H., Fodor, I. Smith, A.D. (1983) Localisation of substance P-like immunoreactivity in neurons and nerve terminals in the neostriatum of the rat: a correlated light and electron microscopic study. J. Neurocytol., 12, 325 344.
10. Bolam, J.P., Hanley, J.J., Booth, P.A.C. Bevan, M.D. (2000) Synaptic organisation of the basal ganglia. J. Anat., 196, 527 542.
11. Bordet, R., Ridray, S., Carboni, S., Diaz, J., Sokoloff, P. Schwartz, J.-C. (1997) Induction of dopamine D3 receptor expression as a mechanism of behavioral sensitization to levodopa. Proc. Natl Acad. Sci. USA, 94, 3363 3367.
12. Bouyer, J.J., Park, D.H., Joh, T.H. Pickel, V.M. (1984) Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res., 302, 267 275.
13. Brandish, P.E., Su, M., Holder, D.J., Hodor, P., Szumiloski, J., Kleinhanz, R.R., Forbes, J.E., McWhorter, M.E., Duenwald, S.J., Parrish, M.L., Na, S., Liu, Y., Phillips, R.L., Renger, J.J., Sankaranarayanan, S., Simon, A.J. Scolnick, E.M. (2005) Regulation of gene expression by lithium and depletion of inositol in slices of adult rat cortex. Neuron, 45, 861 872.
14. Calabresi, P., Picconi, B., Tozzi, A. Di Filippo, M. (2007) Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci., 30, 211 219.
15. Carta, A.R., Tronci, E., Pinna, A. Morelli, M. (2005) Different responsiveness of striatonigral and striatopallidal neurons to L-DOPA after a subchronic intermittent L-DOPA treatment. Eur. J. Neurosci., 21, 1196 1204.
16. Cepeda, C., Hurst, R.S., Altemus, K.L., Flores-Hernandez, J., Calvert, C.R., Jokel, E.S., Grandy, D.K., Low, M.J., Rubinstein, M., Ariano, M.A. Levine, M.S. (2001) Facilitated glutamatergic transmission in the striatum of D2 dopamine receptor-deficient mice. J. Neurophysiol, 85, 659 670.
17. Cepeda, C., Starling, A.J., Wu, N., Soda, T., Lobo, M.K., Yang, X.W. Levine, M.S. (2004) Defining electrophysiological properties of subpopulations of striatal neurons using genetic expression of enhanced green fluorescent protein. Soc. Neurosci. Abstr., 30, 307.
18. Chan, J., Aoki, C. Pickel, V.M. (1990) Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J. Neurosci. Methods, 33, 113 127.
19. Ciruela, F., Ferre, S., Casado, V., Cortes, A., Cunha, R.A., Lluis, C. Franco, R. (2006) Heterodimeric adenosine receptors: a device to regulate neurotransmitter release. Cell. Mol. Life Sci., 63, 2427 2431.
20. Conti, B., Maier, R., Barr, A.M., Morale, M.C., Lu, X., Sanna, P.P., Bilbe, G., Hoyer, D. Bartfai, T. (2007) Region-specific transcriptional changes following the three antidepressant treatments electro convulsive therapy, sleep deprivation and fluoxetine. Mol. Psychiatry, 12, 167 189.
21. David, H.N., Ansseau, M. Abraini, J.H. (2005) Dopamine-glutamate reciprocal modulation of release and motor responses in the rat caudate-putamen and nucleus accumbens of "intact" animals. Brain Res. Rev., 50, 336 360.
22. 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. (2006) Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat. Neurosci., 9, 251 259.
23. Day, M., Wokosin, D., Plotkin, J.L., Tian, X. Surmeier, D.J. (2008) Differential excitability and modulation of striatal medium spiny neuron dendrites. J. Neurosci., 28, 11603 11614.
24. Deutch, A.Y. (2006) Striatal plasticity in parkinsonism: dystrophic changes in medium spiny neurons and progression in Parkinson's disease. J. Neural Transm. Suppl., 70, 67 70.
25. Diaz, J., Levesque, D., Lammers, C.H., Griffon, N., Martres, M.-P., Schwartz, J.-C. Sokoloff, P. (1995) Phenotypical characterization of neurons expressing the dopamine D3 receptor in the rat brain. Neuroscience, 65, 731 745.
26. Ferré, S., Fredholm, B.B., Morelli, M., Popoli, P. Fuxe, K. (1997) Adenosine-dopamine receptor-receptor interactions as an integrative mechanism in the basal ganglia. Trends Neurosci., 20, 482 487.
27. Ferré, S., Karcz-Kubicha, M., Hope, B.T., Popoli, P., Burgueno, J., Gutierrez, M.A., Casado, V., Fuxe, K., Goldberg, S.R., Lluis, C., Franco, R. Ciruela, F. (2002) Synergistic interaction between adenosine A2A and glutamate mGlu5 receptors: implications for striatal neuronal function. Proc. Natl Acad. Sci. USA, 99, 11940 11945.
28. Ferré, S., Borycz, J., Goldberg, S.R., Hope, B.T., Morales, M., Lluis, C., Franco, R., Ciruela, F. Cunha, R. (2005) Role of adenosine in the control of homosynaptic plasticity in striatal excitatory synapses. J. Integr. Neurosci., 4, 445 464.
29. Ferré, S., Ciruela, F., Woods, A.S., Lluis, C. Franco, R. (2007) Functional relevance of neurotransmitter receptor heteromers in the central nervous system. Trends Neurosci., 30, 440 446.
30. Flaherty, A.W. Graybiel, A.M. (1994) Input-output organization of the sensorimotor striatum in the squirrel monkey. J. Neurosci., 14, 599 610.
31. Fredholm, B.B., IJzerman, A.P., Jacobson, K.A., Klotz, K.N. Linden, J. (2001) International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev., 53, 527 552.
32. Fremeau, R.T., Kam, K., Qureshi, T., Johnson, J., Copenhagen, D.R., Storm-Mathisen, J., Chaudhry, F.A., Nicoll, R.A. Edwards, R.H. (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science, 304, 1815 1819.
33. Fujiyama, F., Kuramoto, E., Okamoto, K., Hioki, H., Furuta, T., Zhou, L., Nomura, S. Kaneko, T. (2004) Presynaptic localisation of an AMPA-type glutamate receptor in corticostriatal and thalamostriatal axon terminals. Eur. J. Neurosci., 20, 3322 3330.
34. Fujiyama, F., Unzai, T., Nakamura, K., Nomura, S. Kaneko, T. (2006) Difference in organization of corticostriatal and thalamostriatal synapses between patch and matrix compartments of rat neostriatum. Eur. J. Neurosci., 24, 2813 2824.
35. Gerfen, C.R. (2000) Molecular effects of dopamine on striatal-projection pathways. Trends Neurosci., 23, 64 70.
36. Gerfen, C. Wilson, C. (1996) The basal ganglia. In Swanson, L.W., Björklund, A. Hökfelt, T. (Eds Handbook of chemical neuroanatomy. Integrated systems of the CNS, part III. Elsevier, Amsterdam, pp. 371 468.
37. Gerfen, C.R., Engber, T.M., Mahan, L.C., Susel, Z., Chase, T.N., Monsma, F.J. Sibley, D.R. (1990) D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science, 250, 1429 1432.
38. Gerfen, C.R., McGinty, J.F. Young, W.S. (1991) Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridisation histochemical analysis. J. Neurosci., 11, 1016 1031.
39. Ghate, A., Befort, K., Becker, J.A.J., Filliol, D., Bole-Feysot, C., Demebele, D., Jost, B., Koch, M. Kieffer, B.L. (2007) Identification of novel striatal genes by expression profiling in adult mouse brain. Neuroscience, 146, 1182 1192.
40. Graybiel, A.M. (1995) The basal ganglia. Trends Neurosci., 18, 60 62.
41. Guillin, O., Diaz, J., Carroll, P., Griffon, N., Schwartz, J.-C. Sokoloff, P. (2001) BDNF controls dopamine D3 receptor expression and triggers behavioral sensitisation. Nature, 411, 86 89.
42. Hajji, M.D., Salin, P. Kerkerian Le Goff, L. (1996) Chronic di-zocilpine maleate MK-801 treatment suppresses the effects of nigrostriatal dopamine deafferentation on enkephalin but not substance P expression in the rat striatum, Eur. J. Neurosci., 8, 917 926.
43. Heiman, M., Schaefer, A., Gong, S., Peterson, J.D., Day, M., Ramsey, K.E., Suarez-Farinas, M., Schwarz, C., Stephan, D.A., Surmeier, D.J., Greengard, P. Heintz, N. (2008) A translational profiling approach for the molecular characterization of CNS cell types. Cell, 135, 738 748.
44. Herzog, E., Bellenchi, G.C., Gras, C., Bernard, V., Ravassard, P., Bedet, C., Gasnier, B., Giros, B. El Mestikawy, S. (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J. Neurosci., 21, RC181.
45. Hettinger, B.D., Lee, A., Linden, J. Rosin, D.L. (2001) Ultrastructural localization of adenosine A2A receptors suggests multiple cellular sites for modulation of GABAergic neurons in rat striatum. J. Comp. Neurol., 431, 331 346.
46. Huang, Q., Zhou, D., Chase, K., Gusella, J.F., Aronin, N. DiFiglia, M. (1992) Immunohistochemical localisation of the D1 dopamine receptor in rat brain reveals its axonal transport, pre- and postsynaptic localisation, and prevalence in the basal ganglia, limbic system, and thalamic reticular nucleus. Proc. Natl Acad. Sci. USA, 89, 11988 11992.
47. Ingham, C.A., Hood, S.H. Arbuthnott, G.W. (1989) Spine density on neostriatal neurones changes with 6-hydroxydopamine lesions and with age. Brain Res., 503, 334 338.
48. Ingham, C.A., Hood, S.H., van Maldegem, B., Weenink, A. Arbuthnott, G.W. (1993) Morphological changes in the rat neostriatum after unilateral 6-hydroxydopamine injections into the nigrostriatal pathway. Exp. Brain Res., 93, 17 27.
49. Jonkers, N., Sarre, S., Ebinger, G. Michotte, Y. (2002) MK801 suppresses the L-DOPA-induced increase of glutamate in striatum of hemi-Parkinson rats. Brain Res., 926, 149 155.
50. Kaneko, T. Fujiyama, F. (2002) Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci. Res., 42, 243 250.
51. Kerner, J.A., Standaert, D.G., Penney, J.B. Jr., Young, A.B. Landwehrmeyer, G.B. (1997) Expression of group one metabotropic glutamate receptor subunit mRNA in neurochemically identified neurons in the rat neostriatum, neocortex and hippocampus. Mol. Brain Res., 48, 259 269.
52. Ko, F., Seeman, P., Sun, W.S. Kapur, S. (2002) Dopamine D2 receptors internalize in their low-affinity state. Neuroreport, 13, 1017 1020.
53. Le Moine, C. Bloch, B. (1995) D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J. Comp. Neurol., 355, 418 426.
54. Le Moine, C., Normand, E., Guitteny, A.F., Fouque, B., Teoule, R. Bloch, B. (1990) Dopamine receptor gene expression by enkephalin neurons in rat forebrain. Proc. Natl Acad. Sci. USA, 87, 230 234.
55. Lei, W., Jiao, Y., Del Mar, N. Reiner, A. (2004) Evidence for differential cortical input to direct pathway versus indirect pathway striatal projection neurons in rats. J. Neurosci., 24, 8289 8299.
56. Mao, L.M., Zhang, G.C., Liu, X.Y., Fibuch, E.E. Wang, J.Q. (2008) Group I metabotropic glutamate receptor-mediated gene expression in striatal neurons. Neurochem. Res., 33, 1920 1924.
57. Massart, R., Guilloux, J., Mignon, V., Lauressergues, E., Cussac, D., Sokoloff, P. Diaz, J. (2007) Complex regulation of the orphan G protein-coupled receptor GPR88 in the unilaterally 6-OHDA lesioned rat model of Parkinson's disease. Soc. Neurosci. Abstr., 904.2.
58. Massart, R., Guilloux, J., Mignon, V., Lauressergues, E., Cussac, D., Sokoloff, P. Diaz, J. (2008) Striatal synaptic and cortical nuclear GPR88, a promising target for psychiatric and movement disorders. In ECNP Workshop, Nice, France, Poster no. P1.25.
59. Meshul, C.K., Emre, N., Nakamura, C.M., Allen, C., Donohue, M.K. Buckman, J.F. (1999) Time-dependent changes in striatal glutamate synapses following a 6-hydroxydopamine lesion. Neuroscience, 88, 1 16.
60. Mizushima, K., Miyamoto, Y., Tsukahara, F., Hirai, M., Sakaki, Y. Ito, T. (2000) A novel G-protein-coupled receptor gene expressed in striatum. Genomics, 69, 314 321.
61. Napolitano, M., Centonze, D., Calce, A., Picconi, B., Spiezia, S., Gulino, A., Bernardi, G. Calabresi, P. (2002) Experimental Parkinsonism modulates multiple genes involved in the transduction of dopaminergic signals in the striatum. Neurobiol. Dis., 10, 387 395.
62. Neely, M.D., Schmidt, D.E. Deutch, A.Y. (2007) Cortical regulation of dopamine depletion-induced dendritic spine loss in striatal medium spiny neurons. Neuroscience, 149, 457 464.
63. Nishi, A., Liu, F., Matsuyama, S., Hamada, M., Higashi, H., Nairn, A.C. Greengard, P. (2003) Metabotropic mGlu5 receptors regulate adenosine A2A receptor signaling. Proc. Natl Acad. Sci. USA, 100, 1322 1327.
64. Ogden, C.A., Rich, M.E., Schork, N.J., Paulus, M.P., Geyer, M.A., Lohr, J.B., Kuczenski, R. Niculescu, A.B. (2004) Candidate genes, pathways and mechanisms for bipolar (manic-depressive) and related disorders: an expanded convergent functional genomics approach. Mol. Psychiatry, 9, 1007 1029.
65. Okabe, S. (2007) Molecular anatomy of the postsynaptic density. Mol. Cell. Neurosci., 34, 503 518.
66. Pausch, M., Bates, B., Graf, R., Grauer, S., Hughes, Z., Sung, M., Mabrouk, O., Kanki, K., Zhang, L., Taylor, N., Marguis, K. Logue, S. (2006) Gpr88 knockout mice show a schizophrenia-like phenotype: behavioral and neurochemical profile. Soc. Neurosci. Abstr., 763.12.
67. Paxinos, G. Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic, London.
68. Popoli, P., Pezzola, A., Torvinen, M., Reggio, R., Pintor, A., Scarchilli, L., Fuxe, K. Ferré, S. (2001) The selective mGlu(5) receptor agonist CHPG inhibits quinpirole-induced turning in 6-hydroxydopamine-lesioned rats and modulates the binding characteristics of dopamine D(2) receptors in the rat striatum: interactions with adenosine A(2a) receptors. Neuropsychopharmacology, 25, 505 513.
69. Ragsdale, C.W. Graybiel, A.M. (1988) Fibers from the basolateral nucleus of the amygdala selectively innervate striosomes in the caudate nucleus of the cat. J. Comp. Neurol., 269, 506 522.
70. Reiner, A. Anderson, K.D. (1990) The patterns of neurotransmitter and neuropeptide co-occurrence among striatal projection neurons: conclusions based on recent findings. Brain Res. Brain Res. Rev., 15, 251 265.
71. Ribak, C.E. Roberts, R.C. (1990) GABAergic synapses in the brain identified with antisera to GABA and its synthesizing enzyme, glutamate decarboxylase. J. Electron Microsc. Tech., 15, 34 48.
72. Richardson, P.J., Kase, H. Jenner, P.G. (1997) Adenosine A2A receptor antagonists as new agents for the treatment of Parkinson's disease. Trends Pharmacol. Sci., 18, 338 344.
73. Salin, P. Chesselet, M.F. (1992) Paradoxical increase in striatal neuropeptide gene expression following ischemic lesions of the cerebral cortex. Proc. Natl Acad. Sci. USA, 89, 9954 9958.
74. Salin, P., Dziewczapolski, G., Gershanik, O.S., Nieoullon, A. Raisman-Vozari, R. (1997) Differential regional effects of long-term L-DOPA treatment on preproenkephalin and preprotachykinin gene expression in the striatum of 6-hydroxydopamine-lesioned rat. Brain Res.Mol. Brain Res., 47, 311 321.
75. Schiffmann, S.N., Jacobs, O. Vanderhaeghen, J.J. (1991) Striatal restricted adenosine A2 receptors (RDC8) is expressed by enkephalin but not substance P neurons: an in situ hybridization histochemistry study. J. Neurochem., 57, 1062 1067.
76. Schwarting, R.K.W. Huston, J.P. (1996) Unilateral 6-hydroxydopamine lesions of meso-striatal dopamine neurons and their physiological sequelae. Prog. Neurobiol., 49, 215 266.
77. Smith, Y. Kieval, J.Z. (2000) Anatomy of the dopamine system in the basal ganglia. Trends Neurosci., 23, S28 S33.
78. Smith, Y., Bennett, B.D., Bolam, J.P., Parent, A. Sadikot, A.F. (1994) Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey. J. Comp. Neurol., 344, 1 19.
79. Somogyi, P., Priestley, J.V., Cuello, A.C., Smith, A.D. Takagi, H. (1982) Synaptic connections of enkephalin-immunoreactive nerve terminals in the neostriatum: a correlated light and electron microscopic study. J. Neurocytol., 11, 779 807. (Pubitemid 12031247)
80. Stephens, B., Mueller, A.J., Shering, A.F., Hood, S.H., Taggart, P., Arbuthnott, G.W., Bell, J.E., Kilford, L., Kingsbury, A.E., Daniel, S.E. Ingham, C.A. (2005) Evidence of a breakdown of corticostriatal connections in Parkinson's disease. Neuroscience, 132, 741 754.
81. Surgand, J., Rodrigo, J., Kellenberger, E. Rognan, D. (2006) A chemogenomic analysis of the transmembrane binding cavity of human G-protein-coupled receptors. Proteins, 62, 509 538.
82. Surmeier, D.J., Ding, J., Day, M., Wang, Z. Shen, W. (2007) D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci., 30, 228 235.
83. Svenningsson, P., Fourreau, L., Bloch, B., Fredholm, B.B., Gonon, F. Le Moine, C. (1999) Opposite tonic modulation of dopamine and adenosine on c-fos gene expression in striatopallidal neurons. Neuroscience, 89, 827 837.
84. Svenningsson, P., Gunne, L. Andren, P.E. (2000) L-DOPA produces strong induction of c-fos messenger RNA in dopamine-denervated cortical and striatal areas of the common marmoset. Neuroscience, 99, 457 468.
85. Taymans, J.M., Kia, H.K., Groenewegen, H.J., Leysen, J.E. Langlois, X. (2005) Bilateral control of brain activity by dopamine D1 receptors: evidence from induction patterns of regulator of G protein signalling 2 and c-fos mRNA in D1-challenged hemiparkinsonian rats. Neuroscience, 134, 643 656.
86. Uhl, G.R., Navia, B. Douglas, J. (1988) Differential expression of preproenkephalin and preprodynorphin mRNAs in striatal neurons: high levels of preproenkephalin expression depend on cerebral cortical afferents. J. Neurosci., 8, 4755 4764.
87. Ungerstedt, U. (1971) Striatal dopamine release after amphetamine or nerve degeneration revealed by rotational behaviour. Acta Physiol. Scand. Suppl., 367, 49 68.
88. Voorn, P., Vanderschuren, L.J.M.J., Groenewegen, H.J., Robbins, T.W. Pennartz, C.M.A. (2004) Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci., 27, 468 474.
89. Wang, H., Katz, J., Dagostino, P. Soghomonian, J.-J. (2007) Chronic L-DOPA treatment increases Extracellular glutamate levels and GLT1 expression in the basal ganglia in a rat model of Parkinson's disease. Eur. J. Neurosci., 20, 1255 1266.
90. White, F.J. (1996) Synaptic regulation of mesocorticolimbic dopamine neurons. Annu. Rev. Neurosci., 19, 405 436.
91. Wickens, J.R., Reynolds, J.N.J. Hyland, B.I. (2003) Neural mechanisms of reward-related motor learning. Curr. Opin. Neurobiol., 13, 685 690.
92. Zaja-Milatovic, S., Milatovic, D., Schantz, A.M., Zhang, J., Montine, K.S., Samii, A., Deutch, A.Y. Montine, T.J. (2005) Dendritic degeneration in neostriatal medium spiny neurons in Parkinson disease. Neurology, 64, 545 547.
93. Zeng, B.-Y., Jolkkonen, J., Jenner, P. Marsden, C.D. (1995) Chronic L-DOPA treatment differentially regulates gene expression of glutamate decarboxylase, preproenkephalin and preprotachykinin in the striatum of 6-hydroxydopamine-lesioned rat. Neuroscience, 66, 19 28.
94. Zeng, B.Y., Pearce, R.K., MacKenzie, G.M. Jenner, P. (2000) Alterations in preproenkephalin and adenosine-2a receptor mRNA, but not preprotachikinin mRNA correlate with occurrence of dyskinesia in normal monkeys chronically treated with L-DOPA. Eur. J. Neurosci., 12, 1096 1104.