Complementary roles for hippocampus and anterior cingulate in composing continuous choice

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Abstract

Naturalistic, goal directed behavior often requires continuous actions directed at dynamically changing goals. In this context, the closest analogue to choice is a strategic reweighting of multiple goal-specific control policies in response to shifting environmental pressures. To understand the algorithmic and neural bases of choice in continuous contexts, we examined behavior and brain activity in humans performing a continuous prey-pursuit task. Using a newly developed control-theoretic decomposition of behavior, we find pursuit strategies are well described by a meta-controller dictating a mixture of lower-level controllers, each linked to specific pursuit goals. Examining hippocampus and anterior cingulate cortex (ACC) population dynamics during goal switches revealed distinct roles for the two regions in parameterizing continuous controller mixing and meta-control. Hippocampal ensemble dynamics encoded the controller blending dynamics, suggesting it implements a mixing of goal-specific control policies. In contrast, ACC ensemble activity exhibited value-dependent ramping activity before goal switches, linking it to a meta-control process that accumulates evidence for switching goals. Our results suggest that hippocampus and ACC play complementary roles corresponding to a generalizable mixture controller and meta-controller that dictates value dependent changes in controller mixing.

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