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Spatial organization of functional clusters representing reward and movement information in the striatal direct and indirect pathways

Significance The striatum is critically involved in voluntary motor control and reward-based learning. To formulate a nuanced model of the striatum, it would be important to understand how functional ensembles of striatal neurons are organized in the spatiotemporal domain. In this perspective, we monitored ensemble activity of a large number of striatal neurons in mice performing a classical conditioning task and a self-paced open-field test. We found partially overlapping and learning-dependent spatial organizations of striatal neuronal clusters for movement- as well as reward-related variables in both the direct and indirect pathways. These findings provide insights into striatal neural circuit operations underlying reward-based learning and movement control. To obtain insights into striatal neural processes underlying reward-based learning and movement control, we examined spatial organizations of striatal neurons related to movement and reward-based learning. For this, we recorded the activity of direct- and indirect-pathway neurons (D1 and A2a receptor-expressing neurons, respectively) in mice engaged in probabilistic classical conditioning and open-field free exploration. We found broadly organized functional clusters of striatal neurons in the direct as well as indirect pathways for both movement- and reward-related variables. Functional clusters for different variables were partially overlapping in both pathways, but the overlap between outcome- and value-related functional clusters was greater in the indirect than direct pathway. Also, value-related spatial clusters were progressively refined during classical conditioning. Our study shows the broad and learning-dependent spatial organization of functional clusters of dorsal striatal neurons in the direct and indirect pathways. These findings further argue against the classic model of the basal ganglia and support the importance of spatiotemporal patterns of striatal neuronal ensemble activity in the control of behavior.