Individualized temporal patterns dominate cortical upstate and sleep depth in driving human sleep spindle timing

Abstract

Sleep spindles are critical for memory consolidation and strongly linked to neurological disease and aging. Despite their significance, the relative influences of factors like sleep depth, cortical up/down states, and spindle temporal patterns on individual spindle production remain poorly understood. Moreover, spindle temporal patterns are typically ignored in favor of an average spindle rate. Here, we analyze spindle dynamics in 1008 participants from the Multi-Ethnic Study of Atherosclerosis using a point process framework. Results reveal fingerprint-like temporal patterns, characterized by a refractory period followed by a period of increased spindle activity, which are highly individualized yet consistent night-to-night. We observe increased timing variability with age and distinct gender/age differences. Strikingly, and in contrast to the prevailing notion, individualized spindle patterns are the dominant determinant of spindle timing, accounting for over 70% of the statistical deviance explained by all of the factors we assessed, surpassing the contribution of slow oscillation (SO) phase (~14%) and sleep depth (~16%). Furthermore, we show spindle/SO coupling dynamics with sleep depth are preserved across age, with a global negative shift towards the SO rising slope. These findings offer novel mechanistic insights into spindle dynamics with direct experimental implications and applications to individualized electroencephalography biomarker identification.