Prefrontal default-mode network interactions with posterior hippocampus during exploration

Abstract

Hippocampal maps and ventral prefrontal cortex (vPFC) value and goal representations support foraging in continuous spaces. How might hippocampal-vPFC interactions control the balance between behavioral exploration and exploitation? Using fMRI and reinforcement learning modeling, we investigated vPFC and hippocampal responses as humans explored and exploited a continuous one-dimensional space, with out-of-session and out-of-sample replication. The spatial distribution of rewards, or value landscape, modulated activity in the hippocampus and default network vPFC subregions, but not in ventrolateral prefrontal control subregions or medial orbitofrontal limbic subregions. While prefrontal default network and hippocampus displayed higher activity in less complex, easy-to-exploit value landscapes, vPFC-hippocampal connectivity increased in uncertain landscapes requiring exploration. Further, synchronization between prefrontal default network and posterior hippocampus scaled with behavioral exploration. Considered alongside electrophysiological studies, our findings suggest that locations to be explored are identified through coordinated activity binding prefrontal default network value representations to posterior hippocampal maps. Significance StatementThe ventral prefrontal cortex represents goals and values, while the hippocampus contains maps of physical and abstract spaces. In recent years, neuroscientists have sought to understand how hippocampal-prefrontal interactions help us to solve complex problems such as deciding whether to exploit known rewards or explore in search of better alternatives. Using functional magnetic resonance imaging and reinforcement learning modeling, we examine these interactions as humans explore and exploit an environment with a complex distribution of rewards or value landscape. We describe how this value landscape modulates activity and connectivity between prefrontal cortex and hippocampus, controlling the balance between exploration and exploitation.