Replay as structural inference in the hippocampal-entorhinal system

Abstract

Model-based decision making relies on the construction of an accurate representation of the underlying state-space, and localization of ones current state within it. One way to localize is to recognize the state with which incoming sensory observations have been previously associated. Another is to update a previous state estimate given a known transition. In practice, both strategies are subject to uncertainty and must be balanced with respect to their relative confidences; robust learning requires aligning the predictions of both models over historic observations. Here, we propose a dual-systems account of the hippocampal-entorhinal system, where sensory prediction errors between these models during online exploration of state space initiate offline probabilistic inference. Offline inference computes a metric embedding on grid cells of an associative place graph encoded in the recurrent connections between place cells, achieved by message passing between cells representing non-local states. We provide testable explanations for coordinated place and grid cell replay as efficient message passing, and for distortions, partial rescaling and direction-dependent offsets in grid patterns as the confidence weighted balancing of model priors, and distortions to grid patterns as reflecting inhomogeneous sensory inputs across states. Author SummaryO_LIMinimising prediction errors between transition and sensory input (observation) models predicts partial rescaling and direction-dependent offsets in grid cell firing patterns. C_LIO_LIInhomogeneous sensory inputs predict distortions of grid firing patterns during online localisation, and local changes of grid scale during offline inference. C_LIO_LIPrincipled information propagation during offline inference predicts coordinated place and grid cell replay, where sequences propagate between structurally related features. C_LI