Dynamic ensemble balance in direct- and indirect-pathway striatal projection neurons underlying decision-related action selection

The posterior dorsal striatum (pDS) plays an essential role in sensory-guided decision-making. However, it remains unclear how the antagonizing direct- and indirect-pathway striatal projection neurons (dSPNs and iSPNs) work in concert to support action selection. Here, we employed deep-brain two-photon imaging to investigate pathway-specific single-neuron and population representations during an auditory-guided decision-making task. We found that the majority of pDS projection neurons predominantly encode choice information. Both dSPNs and iSPNs comprise divergent subpopulations of comparable sizes representing competing choices, rendering a multi-ensemble balance between the two pathways. Intriguingly, such ensemble balance displays a dynamic shift during the decision period: dSPNs show a significantly stronger preference for the contraversive choice than iSPNs. This dynamic shift is further manifested in the inter-neuronal coactivity and population trajectory divergence. Our results support a balance-shift model as a neuronal population mechanism coordinating the direct and indirect striatal pathways for eliciting selected actions during decision-making. [Display omitted] •dSPNs and iSPNs both exhibit heterogeneous coding for competing choices•Balance between dSPNs and iSPNs dynamically shifts preceding the chosen actions•dSPNs exhibit stronger synchrony than iSPNs during decision-making behavior•Choice-coding population activity shows greater divergence in dSPNs than in iSPNs Tang et al. perform pathway-specific two-photon imaging from the direct- and indirect-pathway striatal projection neurons (dSPNs and iSPNs) during decision-making behavior. dSPNs and iSPNs both comprise multiple choice-coding ensembles, balanced between the two pathways. These SPN ensembles display a dynamic shift in coding strengths, favoring the decided action.