Neuroimaging Insights into Sleep and Cognition across the Lifespan

Adolescence is a critical period of rapid growth and transformation, marked by significant biological, cognitive, psychological, and social changes that lay the foundation for adulthood. Cognitively, there is rapid development in both crystallized and fluid intelligence, accompanied by improvements in processing speed and robustness as individuals transition from childhood to adolescence. These changes appear alongside key markers of brain maturation, particularly decreases in synaptic density and cortical grey matter volumes, as well as reductions of slow-wave activity (SWA) during sleep - likely reflecting the complex neurological development that supports the increasing cognitive capabilities observed in older adolescents. In this talk, we first explore cross-sectionally how cortical thickness and sleep slow wave activity mediate age-related improvements in cognition using data from mid-late adolescents who had polysomnography-assessed sleep, cognitive test batteries (sustained attention, speed of processing and nonverbal intelligence), and structural brain measures. We then extend these findings to early adolescence by investigating the effect of non-adherence to 24h movement behaviors, i.e. insufficient sleep, excessive screen time use and physical inactivity, on cognition (crystallized and fluid intelligence) and brain structure in 10,574 participants of the Adolescent Brain and Cognitive Development (ABCD) study, at baseline (9-11yo) and 2 years later. These two studies underscore the importance of sleep not just as a marker of brain maturation but as a modulator of optimal brain development and cognitive function.  

Sleep is a state of reduced mental and physical activity, during which brain activity occurs to support a healthy life. Within each cycle, Rapid Eye Movement (REM) sleep (20% of total sleep time during which most recalled dreams occur), alternates with Non-Rapid Eye Movement (NREM) sleep (80% of total sleep time), subdivided into 3 stages evolving from drowsiness to deep sleep (N1, N2, N3). Measuring synchronized bioelectrical neuronal activity, EEG is the exam of choice to define sleep stages, allowing also the detection of sleep-specific transient oscillations. Bioelectrical neuronal activity is intrinsically associated with cerebral hemodynamic regulations and oxygen metabolism, which can be measured with fMRI or functional Near-Infrared Spectroscopy (fNIRS). Although fMRI combined with EEG has been considered for sleep studies, the strict immobility imposed by MRI limits acquisition duration and the noisy MRI scanner makes it difficult for participants to fall asleep. Alternatively, fNIRS is an emerging and non-invasive wearable brain imaging tool that can be combined with EEG to measure brain activity, offering a unique opportunity for prolonged sleep monitoring. fNIRS measures hemodynamic fluctuations of cortical oxygenated (HbO) and deoxygenated (HbR) hemoglobin concentration changes. Whereas most EEG/fNIRS sleep studies reported in the literature considered only few forehead channels, we are proposing whole night EEG/fNIRS, to assess HbO/HbR cortical fluctuations and memory consolidation processes during healthy sleep, using personalized fNIRS to map hemodynamic processes within the fronto-parietal network. To do so, we applied personalized fNIRS (Cai et al HBM 2021), estimating a personalized locally dense montage, optimizing the position of fNIRS optodes to target bilateral frontoparietal regions, before gluing fNIRS and EEG sensors to the scalp using a clinical adhesive. This approach limits sensitivity to motion and therefore ensures collecting good quality signals during whole-night recordings. We will then promote local 3D reconstruction of HbO/HbR signals within those four regions of interest, by converting scalp measurements into 3D reconstructions along the cortical surface (Cai et al Nature Sc. Report 2022). Therefore, our fNIRS scalp recordings using locally dense montages, could be converted into spatio-temporal neuroimaging results covering bilateral frontal and parietal regions for the whole night recording. For each region, using time-frequency analyses of reconstructed fNIRS signals during the whole night, we are reporting sleep stage specific signatures of HbO/HbR oscillatory patterns, comparing slow hemodynamic oscillatory components in all NREM sleep stages but also in REM phasic and tonic periods, while benefitting from EEG data to assess the contribution of sleep biomarkers (spindles, slow waves) in the generation of those hemodynamic responses. Using this approach, our objective is to build the first atlas of EEG/fNIRS sleep physiology in young healthy adults (18-35 years old). In the second part of the talk, we will present preliminary results from a two-night design that allowed to get insights from memory consolidation processes in the healthy brain, using both bioelectrical (EEG) and hemodynamic (HbO/HbR) signals.  

Sleep is one of many pillars of cognitive health, as it performs vital functions for maintaining optimal cognitive performance. In a major role, sleep sustains and prepares the ideal neurophysiological conditions for cognitive functions the following day. This is obvious given the drastic effects that sleep deprivation has on cognitive performance, however the processes for how sleep performs this vital function are still unclear. In this presentation I will describe studies using simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) that investigate the neural correlates of cognitive impairments due to sleep deprivation. By leveraging a bidirectional design of sleep deprivation and recovery sleep (Cross et al. 2021a), we are able to propose a neurophysiological model for how sleep loss may impair effective communication within the brain via altering the balance of integration and segregation of functional brain networks (Cross et al. 2021b). This imbalance can be observed through dynamic functional connectivity and will be discussed in the context of autonomic and other physiological (e.g. cardiovascular) mechanisms. The role of the BOLD global signal in this context will also be addressed. Finally, this presentation will describe ways in which these neurophysiological patterns can be used to not only understand cognitive processes, but how to leverage this knowledge in clinical research to gain important insight into sleep disorders such as central hypersomnolence (eg. narcolepsy) and their debilitating behavioural symptoms.  

Identifying novel factors which associate with inter-individual variability in -and can be considered protective for- cognitive decline is a promising area in aging research. Circadian rhythms -one of the most fundamental processes of living organisms- are present throughout the nervous system and act on cognition and underlying brain function and structure. Circadian rhythms shape the temporal organisation of sleep and wakefulness and evolve throughout the adult lifespan, leading to higher sleep-wake cycle fragmentation with aging. During this session, we will first revise the association between circadian sleep regulatory processes on microstructural brain integrity by focusing on rapid eye movement sleep (REMS). REMS is increasingly suggested as a discriminant sleep state for subtle signs of age-related neurodegeneration. We show that reduced circadian REMS amplitude is related to lower magnetization transfer saturation (MTsat), longitudinal relaxation rate (R1) and effective transverse relaxation rate (R2*) values in several white matter regions mostly located around the lateral ventricles, and with lower R1 values in grey matter clusters encompassing the hippocampus, parahippocampus, thalamus and hypothalamus (Deantoni et al., 2024). Our results highlight the importance of considering circadian regulation for understanding the association between sleep and brain structure in older individuals. In a next step, the impact of daytime napping, a visible manifestation of circadian sleep alteration, on cognition and brain structural-functional correlates will be highlighted. Our results suggest that increasing daytime rest observed during aging is underlined, at the neurobiological level, by an altered integrity of the wake-promoting posterior hypothalamic region (Baillet et al. 2022). Functional MRI data collected in the same population further speak in favor of reduced functional compensation, expressed by altered hemispheric asymmetry in task-related BOLD activation. This session integrates novel findings using a variety of approaches (quantitative structural MRI, functional MRI, EEG) to characterize pathways by which the sleep-wake cycle, or more specifically sleep schedules, affect cognition and underlying brain correlates during aging. The topic is of relevance, since both cognitive impairment and insufficient or mistimed sleep represent dominant health determinants across lifespan, and easy implementable interventions, potentially focused on sleep regulation, are urgently needed.