Three brain states in the hippocampus and cortex

Abstract

Contemporary brain research seeks to understand how cognition is reducible to neural activity. Crucially, much of this effort is guided by a scientific paradigm that views neural activity as essentially driven by external stimuli. In contrast, recent perspectives argue that this paradigm is by itself inadequate and that understanding patterns of activity intrinsic to the brain is needed to explain cognition. Yet, despite this critique, the stimulus-driven paradigm still dominates-possibly because a convincing alternative has not been clear. Here, we review a series of findings suggesting such an alternative. These findings indicate that neural activity in the hippocampus occurs in one of three brain states that have radically different anatomical, physiological, representational, and behavioral correlates, together implying different functional roles in cognition. This three-state framework also indicates that neural representations in the hippocampus follow a surprising pattern of organization at the timescale of ∼1 s or longer. Lastly, beyond the hippocampus, recent breakthroughs indicate three parallel states in the cortex, suggesting shared principles and brain-wide organization of intrinsic neural activity.

Keywords: brain state; cortex; hippocampus; imagination; memory; naturalistic behavior; prospection; sharp wave-ripple.