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The Journal of Neuroscience, August 23, 2006, 26(34):8653-8661; doi:10.1523/JNEUROSCI.2582-06.2006

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Neurobiology of Disease
Phenotype of Striatofugal Medium Spiny Neurons in Parkinsonian and Dyskinetic Nonhuman Primates: A Call for a Reappraisal of the Functional Organization of the Basal Ganglia

Agnes Nadjar,¹ Jonathan M. Brotchie,^3,4 Celine Guigoni,¹ Qin Li,⁵ Shao-Bo Zhou,³ Gui-Jie Wang,³ Paula Ravenscroft,³ François Georges,² Alan R. Crossman,³ and Erwan Bezard¹

¹Centre National de la Recherche Scientifique Unité Mixte de Recherche 5543 et ²Institut National de la Santé et de la Recherche Médicale AVENIR 01, Université Victor Segalen-Bordeaux 2, 33076 Bordeaux, France, ³School of Biological Sciences, University of Manchester, Manchester M13 9PT, United Kingdom, ⁴Toronto Western Research Institute, Toronto Western Hospital, Toronto, Ontario, Canada M5T 2S8, and ⁵Laboratory Animal Research Center, China Agricultural University, Beijing 100101, China

Correspondence should be addressed to Dr. Erwan Bezard, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5543, Université Victor Segalen-Bordeaux 2, 146 rue Léo Saignat, 33076 Bordeaux Cedex, France. Email: erwan.bezard{at}umr5543.u-bordeaux2.fr

The classic view of anatomofunctional organization of the basal ganglia is that striatopallidal neurons of the "indirect" pathway express D₂ dopamine receptors and corelease enkephalin with GABA, whereas striatopallidal neurons of the "direct" pathway bear D₁ dopamine receptors and corelease dynorphin and substance P with GABA. Although many studies have investigated the pathophysiology of the basal ganglia after dopamine denervation and subsequent chronic levodopa (L-dopa) treatment, none has ever considered the possibility of plastic changes leading to profound reorganization and/or biochemical phenotype modifications of medium spiny neurons. Therefore, we studied the phenotype of striatal neurons in four groups of nonhuman primates, including the following: normal, parkinsonian, parkinsonian chronically treated with L-dopa without exhibiting dyskinesia, and parkinsonian chronically treated with L-dopa exhibiting overt dyskinesia. To identify striatal cells projecting to external (indirect) or internal (direct) segments of the globus pallidus, the retrograde tracer cholera toxin subunit B (CTb) was injected stereotaxically into the terminal areas. Using immunohistochemistry techniques, brain sections were double labeled for CTb and dopamine receptors, opioid peptides, or the substance P receptor (NK1). We also used HPLC-RIA to assess opioid levels throughout structures of the basal ganglia. Our results suggest that medium spiny neurons retain their phenotype because no variations were observed in any experimental condition. Therefore, it appears unlikely that dyskinesia is related to a phenotype modification of the striatal neurons. However, this study supports the concept of axonal collateralization of striatofugal cells that project to both globus pallidus pars externa and globus pallidus pars interna. Striatofugal pathways are not as segregated in the primate as previously considered.

Key words: globus pallidus; striatum; cholera toxin; dopamine receptor; dynorphin; enkephalin; immunohistochemistry; HPLC-RIA

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Received June 20, 2006; revised July 12, 2006; accepted July 15, 2006.

Correspondence should be addressed to Dr. Erwan Bezard, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5543, Université Victor Segalen-Bordeaux 2, 146 rue Léo Saignat, 33076 Bordeaux Cedex, France. Email: erwan.bezard{at}umr5543.u-bordeaux2.fr

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