Internal and external contexts drive distinct dynamics in shared action-encoding striatal neurons

Kavli Affiliate: Rui Costa

| Authors: Tanya Sippy, Jan L. Klee, Sulekh Fernando-Peiris, Sahil Suresh, Ines Rodrigues-Vaz, Rui M. Costa and Vivek R. Athalye

| Summary:

Animals can flexibly initiate actions guided by external cues or by internal drive. Disease states often disrupt cue-driven and self-paced actions in distinct ways, underscoring separable neural mechanisms. Such differences could arise from specialized circuits dedicated to each action mode or shared neuronal populations that shift their dynamics across contexts. To distinguish between these possibilities, we developed a task in which mice performed a lever press either spontaneously or in response to a cue, enabling direct comparison of internally and externally triggered movements. Two-photon calcium imaging in dorsolateral striatum revealed subpopulations of neurons tuned to the cue, movement, or post-movement periods. One cluster was consistently active around movement regardless of context, yet population dynamics diverged prior to action. Support vector machine decoding and subspace analyses revealed distinct “context” and “action” components within the same population. Both D1- and D2-SPNs contributed to both subspaces, with D1-SPNs more active at the time of the sensory stimulus. These results show that context shapes dynamics in shared action-encoding neurons within striatal circuits, suggesting that different initiation contexts are funneled into a common action space that flexibly supports movement execution.

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