Hippocampal sharp wave ripples and coincident cortical ripples orchestrate human semantic networks

Abstract

Episodic memory function is predicated upon the precise coordination between the hippocampus and widespread cortical regions. However, our understanding of the neural mechanisms involved in this process is incomplete. In this study, human subjects undergoing intracranial electroencephalography (iEEG) monitoring performed a list learning task. We show sharp-wave ripple (SWR)-locked reactivation of specific semantic processing regions during free recall. This cortical activation consists of both broadband high frequency (non-oscillatory) and cortical ripple (oscillatory) activity. SWRs and cortical ripples in the anterior temporal lobe, a major semantic hub, co-occur and increase in rate prior to recall. Coincident hippocampal-ATL ripples are associated with a greater increase in cortical reactivation, show specificity in location based on recall content, and are preceded by cortical theta oscillations. These findings may represent a reactivation of hippocampus and cortical semantic regions orchestrated by an interplay between hippocampal SWRs, cortical ripples, and theta oscillations.