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The Journal of Neuroscience, June 15, 2003, 23(12):5247-5257

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Three-Dimensional Organization of the Recurrent Axon Collateral Network of the Substantia Nigra Pars Reticulata Neurons in the Rat

Philippe Mailly,¹ Stéphane Charpier,² Annie Menetrey,² and Jean-Michel Deniau²

¹Neurobiologie des Signaux Intercellulaires, Centre National de la Recherche Scientifique, Université Pierre et Marie Curie, 75005 Paris, France, and ²Institut National de la Santé et de la Recherche Médicale, Unité 114, Chaire de Neuropharmacologie, Collège de France, 75231 Paris, France

The substantia nigra pars reticulata (SNR) constitutes a major output nucleus of the basal ganglia where the final stage of information processing within this system takes place. In this study, using juxtacellular labeling and three-dimensional reconstruction methods, we investigated the spatial organization of the intranigral innervation provided by single GABAergic projection neurons from the sensory-motor subdivision of the rat SNR. Confirming previous observations, most labeled SNR cells were found to possess a local axonal network innervating the pars reticulata and pars compacta (SNC). Within the SNR, axons of these cells were distributed along curved laminas enveloping a dorsolaterally located core, thus mostly respecting the onion-like compartmentalization of this nucleus. Although the axonal projection field mostly remained confined to the dendritic field of the parent neuron, it usually extended beyond its limits in caudal, lateral, and/or dorsal directions. Because SNR cells are GABAergic, this pattern of axonal projection suggests the existence of lateral inhibitory interactions between neurons belonging to the same as well as to adjacent functional subdivisions. Axonal projections of SNR cells to the SNC formed longitudinal bands. These bands partly occupied the SNC region projecting to the striatal sector from which parent SNR cells receive their afferents. These data indicate that SNR cells contribute to an indirect nigrostriatal loop circuit through which the striatum could upregulate its level of dopaminergic transmission via a disinhibition of nigrostriatal neurons. Spatial relationships between elements of this indirect nigrostriatonigral circuit indicate that this circuit operates in both a closed and open loop manner.

Key words: basal ganglia; juxtacellular labeling; parallel processing; nigrostriatal loop; substantia nigra pars compacta; three-dimensional reconstructions

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Received Feb. 14, 2003; revised Mar. 28, 2003; accepted Mar. 31, 2003.

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