Cortical and striatal circuit dynamics during natural and learned actions

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The striatum is required for action selection and initiation, and regulates behavior via the striatonigral (direct) and striatopallidal (indirect) pathways. Both pathways are driven by cortical inputs and increase their activity at movement onset during natural and learned behaviors. Some models of striatal function propose that the direct pathway promotes specific actions (i.e., action facilitation) whereas the indirect pathway simultaneously suppresses conflicting actions (i.e., action suppression). However, we previously found that both striatal pathways are rather action-specific during natural behaviors. Here, we show that this striatal organization is in fact inherited from the cortex. Furthermore, to properly distinguish action facilitation from action suppression, we developed a probabilistic three-alternative choice task and recorded direct- and indirect-pathway neurons of the dorsolateral striatum and their motor cortex inputs in freely moving mice using intracellular calcium imaging of large neuronal populations. We found that activity in the motor cortex increases strongly before trial initiation and remains high until the choice was reported. In contrast, striatal activity in both pathways was highest when mice reported their choice. Thus, choice information appeared first in the cortex. Importantly, striatal direct- and indirect-pathway ensembles as well as motor cortex ensembles showed high specificity with regard to the chosen action. This result is not consistent with models that propose an action-suppressing function for striatal indirect-pathway neurons. In this seminar, I will discuss alternative models of cortico-striatal function that we are currently testing using optogenetic inhibition of the motor cortex and the dorsolateral striatum during this task.