Striatal dopamine reflects individual long-term learning trajectories

Abstract

AbstractLearning from naïve to expert occurs over long periods of time, accompanied by changes in the brain’s neuronal signals. The principles governing behavioural and neuronal dynamics during long-term learning remain unknown. We developed a psychophysical visual decision task for mice that allowed for studying learning trajectories from naïve to expert. Mice adopted sequences of strategies that became more stimulus-dependent over time, showing substantial diversity in the strategies they transitioned through and settled on. Remarkably, these transitions were systematic; the initial strategy of naïve mice predicted their strategy several weeks later. Longitudinal imaging of dopamine release in dorsal striatum demonstrated that dopamine signals evolved over learning, reflecting stimulus-choice associations linked to each individual’s strategy. A deep neural network model trained on the task with reinforcement learning captured behavioural and dopamine trajectories. The model’s learning dynamics accounted for the mice’s diverse and systematic learning trajectories through a hierarchy of saddle points. The model used prediction errors mirroring recorded dopamine signals to update its parameters, offering a concrete account of striatal dopamine’s role in long-term learning. Our results demonstrate that long-term learning is governed by diverse yet systematic transitions through behavioural strategies, and that dopamine signals exhibit key characteristics to support this learning.