Striatal dopamine signals internal states related to behavioral performance over prolonged timescales in monkeys

Abstract

Slowly varying internal states govern our ability to sustain goal-directed behavior over minutes to hours, imposing fundamental constraints on cognitive performance, yet the neural signals that track these states remain poorly defined. Dopamine is a powerful modulator of motivated behavior, but its best-characterized signals are in the form of reward prediction errors (RPEs) that operate at seconds timescales. Whether these fast signals also carry information about slower, ongoing states of behavioral performance has not been directly tested. Here, we recorded subsecond dopamine concentration changes across multiple sites in the caudate nucleus (CN) and putamen of rhesus monkeys performing a reward-guided saccade task. Task performance oscillated over tens to hundreds of trials, demonstrating fluctuating internal states of sustained engagement. We found that single-trial dopamine signals were strongly modulated by these slowly evolving performance states, in a manner dissociable from both trial-level RPE and cumulative reward rate. This relationship was biased toward future rather than past performance windows, indicating that dopamine tracks motivational state prospectively rather than simply reflecting the reward history on which prediction errors are computed. Furthermore, performance-state modulation was concentrated in the CN rather than the putamen, consistent with the distinct roles of these regions in oculomotor and skeletomotor control and suggesting that state-dependent dopamine signals are organized according to the behavioral demands of the task. These findings demonstrate that phasic dopamine signals in the dorsal striatum simultaneously reflect fast learning signals and slowly evolving internal states, linking dopamines canonical RPE function to its broader role in sustaining motivated performance.