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      Spatial distribution of D1R- and D2R-expressing medium-sized spiny neurons differs along the rostro-caudal axis of the mouse dorsal striatum

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          Abstract

          The striatum projection neurons are striatonigral and striatopallidal medium-sized spiny neurons (MSNs) that preferentially express D1 (D1R) and D2 (D2R) dopamine receptors, respectively. It is generally assumed that these neurons are physically intermingled, without cytoarchitectural organization although this has not been tested. To address this question we used BAC transgenic mice expressing enhanced green fluorescence (EGFP) under the control of Drd1a or Drd2 promoter and spatial point pattern statistics. We demonstrate that D1R- and D2R-expressing MSNs are randomly distributed in most of the dorsal striatum, whereas a specific region in the caudal striatum, adjacent to the GPe, lacks neurons expressing markers for indirect pathway neurons. This area comprises almost exclusively D1R-expressing MSNs. These neurons receive excitatory inputs from the primary auditory cortex and the medial geniculate thalamic nucleus and a rich dopamine innervation. This area contains cholinergic and GABAergic interneurons but apparently no D2R/A2aR modulation because no fluorescence was detected in the neuropil of Drd2-EGFP or Drd2-Cre, and Adora-Cre BAC transgenic mice crossed with reporter mice. This striatal area that expresses calbindin D28k, VGluT1 and 2, is poor in μ opiate receptors and preproenkephalin. Altogether, the differences observed in D1R-MSNs, D2R-MSNs, and interneurons densities, as well as the anatomical segregation of D1R- and D2R/A2aR-expressing MSNs suggest that there are regional differences in the organization of the striatum.

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          Most cited references55

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          Modulation of striatal projection systems by dopamine.

          The basal ganglia are a chain of subcortical nuclei that facilitate action selection. Two striatal projection systems--so-called direct and indirect pathways--form the functional backbone of the basal ganglia circuit. Twenty years ago, investigators proposed that the striatum's ability to use dopamine (DA) rise and fall to control action selection was due to the segregation of D(1) and D(2) DA receptors in direct- and indirect-pathway spiny projection neurons. Although this hypothesis sparked a debate, the evidence that has accumulated since then clearly supports this model. Recent advances in the means of marking neural circuits with optical or molecular reporters have revealed a clear-cut dichotomy between these two cell types at the molecular, anatomical, and physiological levels. The contrast provided by these studies has provided new insights into how the striatum responds to fluctuations in DA signaling and how diseases that alter this signaling change striatal function.
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            A translational profiling approach for the molecular characterization of CNS cell types.

            The cellular heterogeneity of the brain confounds efforts to elucidate the biological properties of distinct neuronal populations. Using bacterial artificial chromosome (BAC) transgenic mice that express EGFP-tagged ribosomal protein L10a in defined cell populations, we have developed a methodology for affinity purification of polysomal mRNAs from genetically defined cell populations in the brain. The utility of this approach is illustrated by the comparative analysis of four types of neurons, revealing hundreds of genes that distinguish these four cell populations. We find that even two morphologically indistinguishable, intermixed subclasses of medium spiny neurons display vastly different translational profiles and present examples of the physiological significance of such differences. This genetically targeted translating ribosome affinity purification (TRAP) methodology is a generalizable method useful for the identification of molecular changes in any genetically defined cell type in response to genetic alterations, disease, or pharmacological perturbations.
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              Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning.

              The anterior cingulate and orbital cortices and the ventral striatum process different aspects of reward evaluation, whereas the dorsolateral prefrontal cortex and the dorsal striatum are involved in cognitive function. Collectively, these areas are critical to decision making. We mapped the striatal area that receives information about reward evaluation. We also explored the extent to which terminals from reward-related cortical areas converge in the striatum with those from cognitive regions. Using three-dimensional-rendered reconstructions of corticostriatal projection fields along with two-dimensional chartings, we demonstrate the reward and cognitive territories in the primate striatum and show the convergence between these cortical inputs. The results show two labeling patterns: a focal projection field that consists of densely distributed terminal patches, and a diffuse projection consisting of clusters of fibers, extending throughout a wide area of the striatum. Together, these projection fields demonstrate a remarkably large, rostral, reward-related striatal territory that reaches into the dorsal striatum. Fibers from different reward-processing and cognitive cortical areas occupy both separate and converging territories. Furthermore, the diffuse projection may serve a separate integrative function by broadly disseminating general cortical activity. These findings show that the rostral striatum is in a unique position to mediate different aspects of incentive learning. Furthermore, areas of convergence may be particularly sensitive to dopamine modulation during decision making and habit formation.
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                Author and article information

                Journal
                Front Neural Circuits
                Front Neural Circuits
                Front. Neural Circuits
                Frontiers in Neural Circuits
                Frontiers Media S.A.
                1662-5110
                29 July 2013
                2013
                : 7
                : 124
                Affiliations
                [1] 1CNRS, UMR 5203, Institut de Génomique Fonctionnelle Montpellier, France
                [2] 2INSERM, U661 Montpellier, France
                [3] 3Universités de Montpellier 1 & 2, UMR 5203 Montpellier, France
                [4] 4CNRS UMR 7224, INSERM UMRS 952, Université Pierre et Marie Curie Paris, France
                [5] 5Laboratory of Neurophysiology, ULB Neuroscience Institute, Université Libre de Bruxelles Brussels, Belgium
                [6] 6INSERM, UMRS 839 Paris, France
                [7] 7UMRS 839, Université Pierre et Marie Curie-Paris 6 Paris, France
                [8] 8Institut du Fer à Moulin Paris, France
                [9] 9Department of Neuroscience, Karolinska Institutet Stockholm, Sweden
                Author notes

                Edited by: Charles F. Stevens, The Salk Institute for Biological Studies, USA

                Reviewed by: Deborah Baro, Georgia State University, USA; David Parker, Cambridge University, UK

                *Correspondence: Emmanuel Valjent, Inserm U661, CNRS UMR 5203, Institut de Génomique Fonctionnelle, Universités de Montpellier 1 & 2, 141 rue de la Cardonille, 34094 Montpellier, Cedex 05, France e-mail: emmanuel.valjent@ 123456igf.cnrs.fr ; emmanuel.valjent@ 123456gmail.com
                Patrik Krieger, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden e-mail: patrik.krieger@ 123456ki.se

                †These authors have contributed equally to this work.

                Article
                10.3389/fncir.2013.00124
                3725430
                23908605
                963303b4-509c-433e-8972-5c9855688c28
                Copyright © 2013 Gangarossa, Espallergues, Mailly, De Bundel, de Kerchove d'Exaerde, Hervé, Girault, Valjent and Krieger.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 08 April 2013
                : 07 July 2013
                Page count
                Figures: 8, Tables: 1, Equations: 0, References: 69, Pages: 16, Words: 10409
                Categories
                Neuroscience
                Original Research Article

                Neurosciences
                medium-sized spiny neurons,bac transgenic mice,dopamine d1 and d2 receptors,adenosine a2a receptor

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