Dynamics of striatal action selection and reinforcement learning

• DOI: 10.7554/elife.101747.3
• Publication Date: 2025-05-08T11:40:41Z
• Authors: Jack W Lindsey; Jeffrey Markowitz; Winthrop F Gillis; Sandeep R Datta; Ashok Litwin-Kumar
• Keywords: Action selection; Dynamics; Stochastic dynamics

Spiny projection neurons (SPNs) in dorsal striatum are often proposed as a locus of reinforcement learning the basal ganglia. Here, we identify and resolve fundamental inconsistency between striatal models known SPN synaptic plasticity rules. Direct-pathway (dSPN) indirect-pathway (iSPN) neurons, which promote suppress actions, respectively, exhibit that reinforces activity associated with elevated or suppressed dopamine release. We show iSPN prevents successful learning, it patterns negative outcomes. However, this pathological behavior is reversed if functionally opponent dSPNs iSPNs, current behavior, simultaneously activated by efferent input following action selection. This prediction supported recordings contrasts prior representations. In our model, selection signals can be multiplexed without interference, enabling algorithms beyond those standard temporal difference models.