The hippocampal-striatal circuit for goal-directed and habitual choice

Abstract

It is now widely accepted that one of the roles of the hippocampus is to maintain episodic spatial representations, while parallel striatal pathways contribute to both declarative and procedural value computations by encoding different input-specific outcome predictions. In this paper we investigate the use of these brain mechanisms for action selection, linking them to model-based and model-free controllers for decision making. To this aim we propose a biologically inspired computational model that embodies these theories and explains the functioning of the hippocampal-striatal circuit in a rat navigation task. Its main characteristic is to allow the cooperation of habitual and goal-directed behaviors, with the hippocampus primarily involved in encoding spatial information and simulating possible navigation paths, and the ventral and dorsal striatum involved in learning stimulus-response behaviors and evaluating the reward expectancies associated to predicted locations and sensed stimuli, respectively. The architecture we present employs an unsupervised reinforcement learning rule for the hippocampal-striatal network that is able to build a representation of the environment in which rewarding sites and informative landmarks produce value gradients that are used for planning and decision making. Additionally, it utilizes an arbitration mechanism that balances between exploitation, i.e. stimulus-response behaviors, and mental exploration, i.e. motor imagery processes, based on the intensity and the variability of the responses of striatal neurons. We interpret these results in light of recent experimental data that show anticipatory activations in hippocampal and striatal areas.