Rapid coordination of effective learning by the human hippocampus

Abstract

Although the human hippocampus is necessary for long-term memory, controversial findings suggest that hippocampal computations support short-term memory in the service of guiding effective behaviors during learning. We tested the counterintuitive theory that the hippocampus contributes to long-term memory through remarkably short-term processing, as reflected in the sequence of eye movements during encoding of naturalistic scenes. While viewing scenes for the first time, participants generated patterns of eye movements that reflected a shift from stimulus-driven to memory-driven viewing and signaled effective spatiotemporal memory formation. Hippocampal theta oscillations recorded from depth electrodes predicted this viewing pattern. Moreover, effective viewing patterns were preceded by shifts towards top-down influence of hippocampal theta on activity within cortical networks that support visual perception and visuospatial attention. The hippocampus thus supports short-term memory processing that coordinates perception, attention, and behavior in the service of effective spatiotemporal learning. These findings motivate re-interpretation of long-term memory disorders as reflecting loss of the organizing influence of hippocampal short-term memory on learning.