Slow wave synchrony during NREM sleep tracks cognitive impairment in prodromal Alzheimer's disease
O. Sharon, Vladislav Zhelezniakov, Yael Gat, Rotem Falach, Darya Narbayev, Tamara Shiner, Matthew P. Walker, Riva Tauman, Noa Bregman, Yuval Nir
Abstract
INTRODUCTION: Alzheimer's disease (AD) disrupts human sleep architecture more severely than normal aging. However, it remains unclear how AD changes oscillatory neural activity during sleep, and whether such changes foreshadow cognitive decline in AD. METHODS: We used high-density electroencephalography sleep recordings in 55 participants: (1) 21 healthy older adults, (2) 28 patients with amnestic mild cognitive impairment (aMCI)-a prodromal AD stage, and (3) 6 AD patients. RESULTS: Cognitive performance robustly decreases with the slow wave (SW) trough amplitude and its synchronization across broad frontocentral cortical areas. Thus, across the AD spectrum, slow wave synchrony declines with cognition, as in normal aging, but at an accelerated pace. Moreover, delayed rapid eye movement (REM) sleep onset in aMCI and AD patients was associated with deficient SW activity, suggesting insufficiently restorative non-REM sleep. DISCUSSION: These findings suggest that impaired slow waves are closely linked to cognitive impairment and mark disrupted neural activity in AD progression. HIGHLIGHTS: Detailed analysis of high-density sleep electroencephalography was performed in amnestic mild cognitive impairment and Alzheimer's disease (AD) patients. Cognitive status robustly correlates with slow wave trough and its cortical spread. Delayed rapid eye movement sleep onset associated with AD correlates with diminished slow wave troughs. Impaired slow waves mark progressively disrupted neural activity in prodromal AD.