Control of basal ganglia output by direct and indirect pathway projection neurons

The direct and indirect efferent pathways from striatum ultimately reconverge to influence basal ganglia output nuclei, which in turn regulate behavior via thalamocortical and brainstem motor circuits. However, the distinct contributions of these two efferent pathways in shaping basal ganglia output...

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Bibliographic Details
Published in:The Journal of neuroscience 2013-11, Vol.33 (47), p.18531-18539
Main Authors: Freeze, Benjamin S, Kravitz, Alexxai V, Hammack, Nora, Berke, Joshua D, Kreitzer, Anatol C
Format: Article
Language:English
Subjects:
Animals
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Basal Ganglia - cytology
Channelrhodopsins
Electric Stimulation
Locomotion - physiology
Luminescent Proteins - genetics
Luminescent Proteins - metabolism
Mice
Mice, Inbred C57BL
Mice, Transgenic
Neural Inhibition - physiology
Neural Pathways - physiology
Neurons - physiology
Optogenetics
Proto-Oncogene Proteins c-fos - metabolism
Receptors, Adenosine A2 - genetics
Receptors, Dopamine D1 - genetics
Substantia Nigra - cytology
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Summary:The direct and indirect efferent pathways from striatum ultimately reconverge to influence basal ganglia output nuclei, which in turn regulate behavior via thalamocortical and brainstem motor circuits. However, the distinct contributions of these two efferent pathways in shaping basal ganglia output are not well understood. We investigated these processes using selective optogenetic control of the direct and indirect pathways, in combination with single-unit recording in the basal ganglia output nucleus substantia nigra pars reticulata (SNr) in mice. Optogenetic activation of striatal direct and indirect pathway projection neurons produced diverse cellular responses in SNr neurons, with stimulation of each pathway eliciting both excitations and inhibitions. Despite this response heterogeneity, the effectiveness of direct pathway stimulation in producing movement initiation correlated selectively with the subpopulation of inhibited SNr neurons. In contrast, effective indirect pathway-mediated motor suppression was most strongly influenced by excited SNr neurons. Our results support the theory that key basal ganglia output neurons serve as an inhibitory gate over motor output that can be opened or closed by striatal direct and indirect pathways, respectively.
ISSN:0270-6474
1529-2401
1529-2401
DOI:10.1523/jneurosci.1278-13.2013