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Chemical anatomy of pallidal afferents in primates

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Abstract

Neurons of the globus pallidus receive massive inputs from the striatum and the subthalamic nucleus, but their activity, as well as those of their striatal and subthalamic inputs, are modulated by brainstem afferents. These include serotonin (5-HT) projections from the dorsal raphe nucleus, cholinergic (ACh) inputs from the pedunculopontine tegmental nucleus, and dopamine (DA) afferents from the substantia nigra pars compacta. This review summarizes our recent findings on the distribution, quantitative and ultrastructural aspects of pallidal 5-HT, ACh and DA innervations. These results have led to the elaboration of a new model of the pallidal neuron based on a precise knowledge of the hierarchy and chemical features of the various synaptic inputs. The dense 5-HT, ACh and DA innervations disclosed in the associative and limbic pallidal territories suggest that these brainstem inputs contribute principally to the planification of motor behaviors and the regulation of attention and mood. Although 5-HT, ACh and DA inputs were found to modulate pallidal neurons and their afferents mainly through asynaptic (volume) transmission, genuine synaptic contacts occur between these chemospecific axon varicosities and pallidal dendrites, revealing that these brainstem projections have a direct access to pallidal neurons, in addition to their indirect input through the striatum and subthalamic nucleus. Altogether, these findings reveal that the brainstem 5-HT, ACh and DA pallidal afferents act in concert with the more robust GABAergic inhibitory striatopallidal and glutamatergic excitatory subthalamopallidal inputs. We hypothesize that a fragile equilibrium between forebrain and brainstem pallidal afferents plays a key role in the functional organization of the primate basal ganglia, in both health and disease.

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Acknowledgments

This study was supported by research grants from the Canadian Institutes of Health Research (CIHR MOP-115008) and the Natural Sciences and Engineering Research Council of Canada (NSERC 386396-2010). L.E. was the recipient of a doctoral fellowship from the Fonds de recherche du Québec en santé (FRQS 14D 29441). We thank Marie-Josée Wallman for her technical assistance.

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  1. Department of Psychiatry and Neuroscience, Faculty of Medicine, Centre de recherche de l’Institut universitaire en santé mentale de Québec (CRIUSMQ), Université Laval, F-6530-1, 2601, de la Canardière, Quebec, QC, G1J 2G3, Canada

    Lara Eid & Martin Parent

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  1. Lara Eid
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  2. Martin Parent
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Correspondence to Martin Parent.

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Eid, L., Parent, M. Chemical anatomy of pallidal afferents in primates. Brain Struct Funct 221, 4291–4317 (2016). https://doi.org/10.1007/s00429-016-1216-y

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