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

Abstract

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.

Keywords: CP: Neuroscience; action selection; auditory perception; decision making; direct pathway; dynamic balance; indirect pathway; neuronal ensemble; striatum; two-photon imaging.