Learning to select actions shapes recurrent dynamics in the corticostriatal system

Learning to select appropriate actions based on their values is fundamental to adaptive behavior. This form of learning is supported by fronto-striatal systems. The dorsal-lateral prefrontal cortex (dlPFC) and the dorsal striatum (dSTR), which are strongly interconnected, are key nodes in this circuitry. Substantial experimental evidence, including neurophysiological recordings, have shown that neurons in these structures represent key aspects of learning. The computational mechanisms that shape the neurophysiological responses, however, are not clear. To examine this, we developed a recurrent neural network (RNN) model of the dlPFC-dSTR circuit and trained it on an oculomotor sequence learning task. We compared the activity generated by the model to activity recorded from monkey dlPFC and dSTR in the same task. This network consisted of a striatal component which encoded action values, and a prefrontal component which selected appropriate actions. After training, this system was able to autonomously represent and update action values and select actions, thus being able to closely approximate the representational structure in corticostriatal recordings. We found that learning to select the correct actions drove action-sequence representations further apart in activity space, both in the model and in the neural data. The model revealed that learning proceeds by increasing the distance between sequence-specific representations. This makes it more likely that the model will select the appropriate action sequence as learning develops. Our model thus supports the hypothesis that learning in networks drives the neural representations of actions further apart, increasing the probability that the network generates correct actions as learning proceeds. Altogether, this study advances our understanding of how neural circuit dynamics are involved in neural computation, revealing how dynamics in the corticostriatal system support task learning.