Slow waves (SW; < 4 Hz and > 75 μV) during non-rapid eye movement (NREM) sleep in humans are characterized by hyperpolarization [surface electroencephalogram (EEG) SW negative phase], during which cortical neurons are silent, and depolarization (surface EEG positive phase), during which the cortical neurons fire intensively. We assessed the effects of age, sex and topography on the dynamics of SW characteristics in a large population (n=87) of healthy young (23.3 ± 2.4 years) and middle-aged (51.9 ± 4.6 years) volunteers. Older subjects showed lower SW density and amplitude than young subjects. Age-related lower SW density in men was especially marked in prefrontal/frontal brain areas, where they originate more frequently. Older subjects also showed longer SW positive and negative phase durations. These last results indicate that, in young subjects, cortical neurons would synchronously enter the SW hyperpolarization and depolarization phases, whereas this process would take longer in older subjects, leading to lower slope and longer SW positive and negative phases. Importantly, after controlling for SW amplitude, middle-aged subjects still showed lower slope than young subjects in prefrontal, frontal, parietal and occipital derivations. Age-related effects on SW density, frequency and positive phase duration were more prominent at the beginning of the night, when homeostatic sleep pressure is at its highest. Age-related SW changes may be associated with changes in synaptic density and white matter integrity and may underlie greater sleep fragmentation and difficulty in recuperating and maintaining sleep under challenges in older subjects.
Sleep slow waves (SWs) change considerably throughout normal aging. In humans, SWs are generated and propagate on a structural backbone of highly interconnected cortical regions that form most of the default mode network, such as the insula, cingulate cortices, temporal lobe, parietal lobe, and medial frontal lobe. Regions in this network undergo cortical thinning and breakdown in structural and functional connectivity over the course of normal aging. In this study, we investigated how changes in cortical thickness (CT), a measure of gray matter integrity, are involved in modifications of sleep SWs during adulthood in humans. Thirty young (mean age ϭ 23.49 years; SD ϭ 2.79) and 33 older (mean age ϭ 60.35 years; SD ϭ 5.71) healthy subjects underwent a nocturnal polysomnography and T1 MRI. We show that, when controlling for age, higher SW density (nb/min of nonrapid eye movement sleep) was associated with higher CT in cortical regions involved in SW generation surrounding the lateral fissure (insula, superior temporal, parietal, middle frontal), whereas higher SW amplitude was associated with higher CT in middle frontal, medial prefrontal, and medial posterior regions. Mediation analyses demonstrated that thinning in a network of cortical regions involved in SW generation and propagation, but also in cognitive functions, explained the age-related decrease in SW density and amplitude. Altogether, our results suggest that microstructural degradation of specific cortical regions compromise SW generation and propagation in older subjects, critically contributing to age-related changes in SW oscillations.
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