Effects of aperiodic neural activity on sleep-based emotional memory consolidation across the lifespan

Abstract

Sleep neurophysiology undergoes significant changes across the lifespan, which coincide with age-related differences in memory, particularly for emotional information. However, the mechanisms that underlie these effects remain poorly understood. One potential mechanism is the aperiodic component, which reflects "neural noise", differs across age, and is predictive of perceptual and cognitive processes. In this study, we investigated how intrinsic (i.e., resting-state) aperiodic neural activity modulates sleep-based emotional memory consolidation across the human lifespan. In a within-subjects, repeated measures design, forty-two participants aged 7–72 years (M = 26.60, SD = 17.45; 26 female) completed a learning and baseline recognition emotional memory task before a 2hr afternoon sleep opportunity and an equivalent period of wake. Recognition accuracy was also assessed post-delay. We found that aperiodic slopes follow a u-shaped trajectory across the lifespan: slopes flatten from childhood to young adulthood, before steepening thereafter, with this effect most prominent in frontal regions. Age-related differences in aperiodic slopes also explained interindividual differences in emotional memory consolidation, with less age-related flattening of slopes associated with stronger consolidation of negative stimuli post-sleep but not post-wake. Lastly, independent of aperiodic activity, age-related differences in NREM oscillatory activity predicted emotional memory consolidation. These findings suggest that the efficiency of sleep-based emotional memory consolidation is modulated by age-related differences in aperiodic neural and NREM oscillatory activities, providing novel insights into the neurophysiological mechanisms underpinning emotional memory across the lifespan.