In prior studies, we described the differential organization of corticostriatal andthalamostriatal inputs to the spines of direct pathway (dSPNs) and indirectpathway striatal projection neurons (iSPNs) of the matrix compartment. In thepresent electron microscopic (EM) analysis, we have refined understanding ofthe relative amounts of cortical axospinous vs. axodendritic input to the twotypes of SPNs. Of note, we found that individual dSPNs receive about twice asmany axospinous synaptic terminals from IT-type (intratelencephalically projecting)cortical neurons as they do from PT-type (pyramidal tract projecting) corticalneurons. We also found that PT-type axospinous synaptic terminals were about 1.5times as common on individual iSPNs as IT-type axospinous synaptic terminals.Overall, a higher percentage of IT-type terminals contacted dSPN than iSPNspines, while a higher percentage of PT-type terminals contacted iSPN thandSPN spines. Notably, IT-type axospinous synaptic terminals were significantlylarger on iSPN spines than on dSPN spines. By contrast to axospinousinput, the axodendritic PT-type input to dSPNs was more substantial than thatto iSPNs, and the axodendritic IT-type input appeared to be meager andcomparable for both SPN types. The prominent axodendritic PT-type input todSPNs may accentuate their PT-type responsiveness, and the large size ofaxospinous IT-type terminals on iSPNs may accentuate their IT-type responsiveness.Using transneuronal labeling with rabies virus to selectively label the corticalneurons with direct input to the dSPNs projecting to the substantia nigra parsreticulata, we found that the input predominantly arose from neurons in the upperlayers of motor cortices, in which IT-type perikarya predominate. The differentialcortical input to SPNs is likely to play key roles in motor control and motorlearning.
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