System-Wide Replay in the Sensory Cortical-Hippocampal Hierarchy is Associated with Reward Anticipation

Abstract

Replay of hippocampal place cell information has been associated with memory storage, retrieval and planning, but it remains unclear how it aligns with activity in the sensory and parahippocampal cortices. During a visuospatial discrimination task, neurons in the somatosensory and perirhinal cortex were significantly coordinated with awake hippocampal replay. Perirhinal coordination was particularly strong during CA1 replay events that were forward, local, and occurred near reward sites. Perirhinal activity was roughly aligned with the timing of hippocampal representations. Triple coordination of CA1, perirhinal and somatosensory cortex defined a system-wide replay, which was prominent during goal site approach and reiterated recent, local paths. The increased likelihood of system-wide replay during reward anticipation contrasted with CA1 replay events in general, which occurred throughout different phases of behavioral trials and were highly heterogeneous. Thus, recent sequences of sensory-spatial representations in anticipation of trial outcome are recapitulated by temporally aligned replay in the sensory cortical-to-hippocampal hierarchy.