Hippocampal Planning: Linking Actions and Outcomes to Guide Behavior

Humans and animals construct internal models linking actions with their likely outcomes, and use these models to guide behavior. Such model-based cognition is often referred to as planning, and its neural mechanisms remain poorly understood (Miller & Venditto, 2021). The hippocampus, known for its role in spatial learning and memory, is necessary for planning (Miller et al., 2017; Vikbladh et al., 2019). Specifically, hippocampal sequences, which “sweep out” nonlocal trajectories both during active behavior (“theta sequences”) and at rest (“sharp-wave ripple sequences”; SWR), have been proposed to link actions to subsequent outcomes in a manner suitable for planning (Mattar & Daw, 2018; Pezzulo et al., 2019). Here, we investigate the role of these sequences in detail using Neuropixel 2.0 probes (Steinmetz et al., 2021) to record many simultaneous units while rats perform a multi-step decision task that elicits planned behavior (Miller et al., 2017). We find that hippocampus encodes states of the task with periods of action and outcome co-representation. We find action-outcome links during theta sequences before trial initiation, biased towards upcoming choices and previously experienced outcomes, and during theta sequences approaching outcomes, biased towards previous choices. Choices paired with unexpected outcomes have increased representation of non-chosen actions, reflecting knowledge of the task’s transition structure and suggesting credit assignment towards relevant, non-chosen actions. SWR sequences between trials are biased towards previously rewarded outcomes but show no significant choice modulation. These results suggest that theta sequences, but not SWR sequences, support choice evaluation and model-based credit assignment.