Odor cueing of declarative memories during sleep enhances coordinated spindles and slow oscillations

Abstract

Long-term memories are formed by repeated reactivation of newly encoded information during sleep. This process can be enhanced by using memory-associated reminder cues like sounds and odors. While auditory cueing has been researched extensively, few electrophysiological studies have exploited the various benefits of olfactory cueing. We used high-density electroencephalography in an odor-cueing paradigm that was designed to isolate the neural responses specific to the cueing of declarative memories. We show widespread cueing-induced increases in the duration and rate of sleep spindles. Higher spindle rates were most prominent over centro-parietal areas and largely overlapping with a concurrent increase in the amplitude of slow oscillations (SOs). Interestingly, greater SO amplitudes were linked to a higher likelihood of coupling a spindle and coupled spindles expressed during cueing were more numerous in particular around SO up states. We thus identify temporally and spatially coordinated enhancements to sleep spindles and slow oscillations as a candidate mechanism behind the benefits of odor cueing. Our results further demonstrate the feasibility of studying neural activity patterns related to memory processing using olfactory cueing during sleep. Statement of SignificanceMemory cueing during sleep allows insights into memory consolidation. This study is the first to investigate olfactory cueing-induced declarative memory processing using high-density EEG, while robustly controlling for critical confounding factors. The use of odors as cues, instead of more common auditory stimuli, further minimizes possible distortions due to sensory-evoked potentials. We demonstrate intricate changes in brain activity in response to cueing, such as the patterns of sleep spindles, slow oscillations, and their spatiotemporal coupling. We provide evidence that the enhancement of slow oscillation amplitudes, together with associated increases in sleep spindle rates, could be the key mechanism behind cueing-related memory benefits. We moreover show that prior findings obtained using auditory cueing are not the mere result of tone-evoked responses but might be genuine signatures of memory processing.