Abstract

The basal ganglia are known to play an essential role in decision-making. The striatum, the major input site of the basal ganglia, has a dorsal-ventral gradient in the input modality: the more dorsolateral part receives sensorimotor-related information and the more ventral part receives associative and motivational information. Previous lesion studies have suggested that subareas of the striatum have distinct roles: the dorsolateral striatum (DLS) functions in habitual action, the dorsomedial striatum (DMS) in goal-directed actions, and the ventral striatum (VS) in motivation. However, it has not been investigated what kind of roles are taken by these subareas concurrently during the same process of decision-making. In this study, we systematically investigated information represented by phasically active neurons in DLS, DMS, and VS during two types of choice tasks: fixed- and free-choice tasks. In both tasks, rats were required to perform nose poking to either the left or right hole after cue-tone presentation. A food pellet was delivered probabilistically depending on the presented cue and the selected action. The reward probability was fixed in fixed-choice task and varied in a block-wise manner in free-choice task. We found the following: (1) before rats started a trial, a majority of VS neurons increased their firing rates and information regarding task type and state value was most strongly represented in VS; (2) during action selection, information of action and action values was most strongly represented in DMS; and (3) activity peaks of DLS neurons were sharper and more uniformly distributed than those of DMS and VS. To explain our results, we proposed a hierarchical reinforcement learning hypothesis that VS, DMS, and DLS are hierarchical learning modules in charge of actions at different physical and temporal scales. VS is the coarsest module governing objects of actions, such as aiming for a goal, avoiding a danger, or just taking a rest. DMS is the middle module in charge of abstract actions, such as turn left, turn right, or go straight, by taking into account contextual information. DLS is the module in charge of the finest control of physical actions, such as the control of each limb.

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