Constructing future behaviour in the hippocampal formation through composition and replay

Abstract

Hippocampus is critical for memory, imagination and constructive reasoning. However, recent models have suggested that its neuronal responses can be well explained by graphs, or state-spaces, that model the transitions between experiences. Here we use simulations and hippocampal recordings to reconcile these views. We show that if state-spaces are constructed compositionally from existing building blocks, or primitives, hippocampal responses can be interpreted as compositional memories, binding these primitives together. Critically, this enables agents to behave optimally in novel environments with no new learning, inferring behaviour directly from the composition. We predict a role for hippocampal replay in building and consolidating these compositional memories. Importantly, due to their compositional nature, replay can construct states the agent has never experienced - effectively building memories of the future. We test these predictions in two datasets by showing that replay events from newly discovered landmarks induce and strengthen new remote firing fields. These memories, built in replay, are compositional. When the landmark is moved, replay builds a new firing field at the same vector to the new location. Together, these findings provide a framework for reasoning about compositional memories, and demonstrate that such memories are formed in hippocampal replay.