Cued reactivation during slow-wave sleep induces connectivity changes related to memory stabilization.

Abstract

Memory reprocessing following acquisition enhances memory consolidation. Specifically, neural activity during encoding is thought to be replayed during subsequent slow-wave sleep (SWS). This natural tendency of memory replay can be induced by external cueing, known as \"targeted memory reactivation\". Here, we analyzed data from a published study (van Dongen, Takashima, et al. 2012), where auditory cues reactivated learned visual object-location memories during SWS. Memory replay during sleep presumably involves a shift in connectivity across the brain. Therefore, we characterized the effects of memory reactivation on brain network connectivity using graph-theory. We found that cue presentation during SWS introduced increased network integration of the occipital cortex, a visual region that was also active during the object retrieval task. Importantly, enhanced network integration of the occipital cortex showed a behavioural benefit and predicted overnight memory stabilization. Furthermore, occipital cortex displayed enhanced connectivity with mnemonic regions, namely the hippocampus, parahippocampal gyrus, thalamus and medial prefrontal cortex during cue versus control sound presentation. Finally, network integration of early occipital cortex during cueing in SWS was related to increased activation of the bilateral parahippocampal gyrus, a region involved in coding for spatial associative information, at the post-sleep test. Together, these results support a neural mechanism where cue-induced replay during sleep promotes memory consolidation by increased integration of task-relevant perceptual regions with mnemonic regions.