Objective: To obtain the insight how striatum processes reward based learning and motor information, we explored the responses of D1 and D2 medium spiny neurons (MSNs) in the dorsal striatum of mice performing a probabilistic Pavlovian conditioning task and open field test.

Background: From the classic rate model of the basal ganglia, the direct and indirect pathway is known to be anatomically segregated and play an opposing role in both reinforcement learning and voluntary motor control. However, this classic dichotomous model has been recently challenged.

Method: We performed in-vivo single unit electrophysiologic recording and 1-photon endoscopic calcium imaging of dorsal striatum and examined the responses of dSPNs(D1) and iSPNs (D2) medium spiny neurons (MSNs) using D1-cre and D2-cre/A2a-cre transgenic mouse. Mice performed the head-fixed odor discriminating classical conditioning task and self-paced open field test on the same day.

Results: Neural encoding pattern of the two pathways were similar across reward and movement related parameters, but there were quantitative differences. dSPNs and iSPNs increased and decreased activity as a function of expected value, respectively, suggesting striatal value is represented by relative activity levels between direct and indirect pathway. dSPNs and iSPNs showed spatially clustered activity pattern throughout variables of reward based learning and self-paced locomotion behavior. The spatial clustering pattern was not overlapping but distinct across variables, which suggests dynamic functional clusters in the dorsal striatum. Furthermore, spatial correlation of neural encoding between different context (reward based learning and self-paced locomotion behavior) was significantly lower compared with correlation pattern from the same context. Spatial pattern for parameter which requires learning (expected value) was reinforced after days of training. On the contrary, spatial pattern for the parameters which doesn’t require training (outcome, lick, locomotion related parameters) were not changed from the first day.

Conclusion: This study showed context-dependent spatial organization of neural encoding of dorsal striatum across different context. This result suggests multiple dynamic parallel basal ganglia loop based on local clusters in the dorsal striatum may as a key to the novel model of the basal ganglia.

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MDS Abstracts - https://www.mdsabstracts.org/abstract/spatial-distribution-of-functional-clusters-coding-for-reward-and-movement-information-in-the-striatal-direct-and-indirect-pathways/