Offline replay supports planning in human reinforcement learning

Elife. 2018 Dec 14:7:e32548. doi: 10.7554/eLife.32548.

Abstract

Making decisions in sequentially structured tasks requires integrating distally acquired information. The extensive computational cost of such integration challenges planning methods that integrate online, at decision time. Furthermore, it remains unclear whether 'offline' integration during replay supports planning, and if so which memories should be replayed. Inspired by machine learning, we propose that (a) offline replay of trajectories facilitates integrating representations that guide decisions, and (b) unsigned prediction errors (uncertainty) trigger such integrative replay. We designed a 2-step revaluation task for fMRI, whereby participants needed to integrate changes in rewards with past knowledge to optimally replan decisions. As predicted, we found that (a) multi-voxel pattern evidence for off-task replay predicts subsequent replanning; (b) neural sensitivity to uncertainty predicts subsequent replay and replanning; (c) off-task hippocampus and anterior cingulate activity increase when revaluation is required. These findings elucidate how the brain leverages offline mechanisms in planning and goal-directed behavior under uncertainty.

Keywords: Dyna; cognitive computational neuroscience; decision-making; fMRI; hippocampus; human; learning and memory; memory; model-based learning; neuroscience; offline memory processes; planning; prediction error; prioritized replay; reinforcement learning; replay; representation learning; reward revaluation; uncertainty.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain Mapping
  • Decision Making / physiology*
  • Female
  • Games, Experimental
  • Gyrus Cinguli / anatomy & histology
  • Gyrus Cinguli / diagnostic imaging
  • Gyrus Cinguli / physiology*
  • Hippocampus / anatomy & histology
  • Hippocampus / diagnostic imaging
  • Hippocampus / physiology*
  • Humans
  • Machine Learning
  • Magnetic Resonance Imaging
  • Male
  • Mental Recall / physiology*
  • Pattern Recognition, Visual / physiology*
  • Reinforcement, Psychology
  • Reward
  • Uncertainty