A basal ganglia circuit for evaluating action outcomes

The basal ganglia, a group of subcortical nuclei, play a crucial role in decision making by selecting actions and evaluating their outcomes(1,2). While much is known about the function of the basal ganglia circuitry in selection(1,3,4), how these nuclei contribute to outcome evaluation is less clear. Here we show that neurons in the habenula-projecting globus pallidus (GPh) are essential for evaluating action outcomes and are regulated by a specific set of inputs from the basal ganglia. We found in a classical conditioning task that individual mouse GPh neurons bidirectionally encode whether an outcome is better or worse than expected. Mimicking these evaluation signals with optogenetic inhibition or excitation is sufficient to reinforce or discourage actions in a decision making task. Moreover, cell-type-specific synaptic manipulations revealed that the inhibitory and excitatory inputs to the GPh are necessary for mice to appropriately evaluate positive and negative feedback, respectively. Finally, using rabies virus-assisted monosynaptic tracing(5), we discovered that the GPh is embedded in a basal ganglia circuit wherein it receives inhibitory input from both striosomal and matrix compartments of the striatum, and excitatory input from the “limbic” regions of the subthalamic nucleus (STN). Our results provide the first direct evidence that information about the selection and evaluation of actions is channelled through distinct sets of basal ganglia circuits, with the GPh representing a key locus where information of opposing valence is integrated to determine whether action outcomes are better or worse than expected.