Abstract
How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selective interaction of these cardinal sleep oscillations is organized to support information reactivation and transfer. Here, using human intracranial recordings, we demonstrate that the prefrontal cortex plays a key role in organizing the ripple-mediated information transfer during non-rapid eye movement (NREM) sleep. We reveal a temporally precise form of coupling between prefrontal slow-wave and spindle oscillations, which actively dictates the hippocampal-neocortical dialogue and information transfer. Our results suggest a model of the human sleeping brain in which rapid bidirectional interactions, triggered by the prefrontal cortex, mediate hippocampal activation to optimally time subsequent information transfer to the neocortex during NREM sleep.
Highlights
How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations
The majority of medial temporal lobe (MTL) electrode contacts were placed in the hippocampus (CA1, CA3/DG, and Subiculum), but we assessed adjacent contacts in entorhinal cortex (ERC), perirhinal cortex (PRC), and parahippocampal gyrus (PHG) given that ripples have been observed in both the ERC24 as well as the PHG6
We collectively refer to this group as ‘MTL’ electrodes throughout the manuscript, unless we found effects that were specific to the hippocampus proper
Summary
How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. While several lines of research converged on the notion that the coupling of SOs, spindles and ripples is important for memory consolidation[4,5,10,16], it is unclear if coupled SO-spindles index preceding hippocampal processing, or instead, if they play a functional role in organizing hippocampal activity[1,9] The latter finding would indicate cortical control of hippocampal reactivations, one that may advantageously insure that the neocortex receives information at an optimal time point when information transfer[20,21] and plasticity dynamics[22,23] are maximal
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