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Neuronal representation of a working memory-based decision strategy in the motor and prefrontal cortico-basal ganglia loops

While animal and human decision strategies are typically explained by model-free and model-based reinforcement learning, their choice sequences often follow simple procedures based on working memory of past actions and rewards. Here we address how working memory-based choice strategies, such as win-stay-lose-switch (WSLS), are represented in the prefrontal and motor cortico-basal ganglia loops by simultaneous recording of neuronal activities in the dorsomedial striatum (DMS), the dorsolateral striatum (DLS), the medial prefrontal cortex (mPFC), and the primary motor cortex (M1). In order to compare neuronal representations when rats employ working memory-based strategies, we developed a new task paradigm, a continuous/intermittent choice task, consisting of choice and no-choice trials. While the continuous condition (CC) consisted of only choice trials, in the intermittent condition (IC), a no-choice trial was inserted after each choice trial to disrupt working memory of the previous choice and reward. Behaviors in CC showed high proportions of win-stay and lose-switch choices, which could be regarded as “a noisy WSLS strategy.” Poisson regression of neural spikes revealed encoding specifically in CC of the previous action and reward before action choice and prospective coding of WSLS action during action execution. A striking finding was that the DLS and M1 in the motor cortico-basal ganglia loop carry substantial WM information about previous choices, rewards, and their interactions, in addition to current action coding. Significance Statement Working memory-based decision strategies, such as win-stay-lose-switch (WSLS), are widely observed in humans and animals. To address neuronal bases of these strategies, we recorded neuronal activities of rat prefrontal and motor cortico-basal ganglia loops during continuous/intermittent choice tasks. The rat choice strategy was a noisy WSLS in the continuous choice condition, whereas non-WSLS was selected in the intermittent choice condition. In the continuous choice condition, the primary motor cortex and the dorsolateral striatum in the motor loop more strongly conveyed information about previous choices, rewards, and their interactions than the medial prefrontal cortex and the dorsomedial striatum in the prefrontal loop. These results demonstrate that the motor cortico-basal ganglia loop contributes to working memory-based decision strategies.