Altered rhythmic and arrhythmic electroencephalographic activity during non-rapid eye movement sleep in amnestic mild cognitive impairment

Abstract

Non-rapid eye movement sleep electroencephalographic activity has been proposed to provide helpful markers for the early detection of Alzheimer’s disease. However, studies have produced mixed results regarding the impact of mild cognitive impairment—a prodromal stage—when using traditional spectral power analyses during this sleep phase. It is increasingly recognized that electrophysiological power spectra are composed of two components: a rhythmic part, which reflects oscillatory activity, and an arrhythmic part, which represents the balance of neuronal excitation and inhibition. In this cross-sectional study, our objective was thus to determine whether cognitive impairment is associated with the non-rapid eye movement sleep rhythmic and arrhythmic components in older adults. Fifty-six cognitively normal participants (68.3 ± 7.1 years old, 41% women) and 56 participants with amnestic mild cognitive impairment (69.9 ± 8.6 years old, 41% women) matched on multiple variables (age, sex, education, body mass index, apnoea–hypopnoea index) underwent a neuropsychological assessment and a night of polysomnography. Analyses focused on six channels of interest (F3, F4, C3, C4, P3 and P4). Significant between-group differences were observed for non-rapid eye movement sleep rhythmic and arrhythmic activity. Participants with amnestic mild cognitive impairment had lower rhythmic power in the fast-sigma/slow-beta range across all topographies investigated and higher gamma rhythmic power in the left parietal area. Participants with amnestic mild cognitive impairment also showed lower mean gamma aperiodic exponents—an arrhythmic activity measure—across all topographies. Frontal rhythmic power in the fast-sigma/slow-beta range predicted episodic memory in the amnestic mild cognitive impairment group. Our findings reveal alterations in both rhythmic and arrhythmic brain activity, indicating oscillatory changes and signs of hyperexcitability during non-rapid eye movement sleep in individuals with amnestic mild cognitive impairment.