Parallel basal ganglia and frontal cortical outputs differentially encode context-dependent evaluation and categorical commitment during choice

Abstract

Adaptive choice requires transforming the evaluation of available options into commitment to a specific action but understanding how this transformation is implemented across neural circuits remains a central challenge. Here we recorded well-isolated neurons in the substantia nigra pars reticulata (SNr) and frontal eye field (FEF), which send parallel projections to the superior colliculus for driving the eye movement choice, while monkeys performed a sequential-offer choice task designed to partially dissociate scene-defined ordinal rank from the categorical commitment. Before target onset, SNr displayed stronger scene-related modulation than FEF. During target evaluation, SNr activity showed ordered modulation across behavioral outcomes dominated by ordinal rank, whereas FEF activity categorically separated acceptance from rejection and strongly encoded target direction. Behavioral model decomposition revealed that ordinal rank alone best explained SNr activity, outperforming both reward magnitude and even a composite acceptability measure that incorporated rank together with reward, scene context, and waiting cost, whereas FEF activity was best explained by categorical commitment. This dissociation was consistent across multivariable modeling, single-neuron response patterns, and all three monkeys. Together, these findings support a division of labor in which context-dependent evaluation and categorical commitment are distributed across parallel basal ganglia and frontal cortical output pathways to efficiently guide voluntary choices.