Non-REM Sleep Characteristics Predict Early Cognitive Impairment in an Aging Population.

Published on Mar 13, 2019in Frontiers in Neurology2.635
· DOI :10.3389/fneur.2019.00197
Jacques Taillard32
Estimated H-index: 32
(University of Bordeaux),
Patricia Sagaspe25
Estimated H-index: 25
(University of Bordeaux)
+ 7 AuthorsPierre Philip45
Estimated H-index: 45
(University of Bordeaux)
Objective Recent studies suggest that sleep disorders or modifications of sleep stages or EEG waveform precede over the years the onset of clinical signs of pathological cognitive impairment (e.g., Alzheimer's disease). The aim of this study is to identify biomarkers based on EEG power values and spindles characteristics during sleep that occur early in mild cognitive impairment in older adults. Methods This study is a case-control cross-sectional study and one-year follow-up of the cases. Patients with isolated subjective cognitive complaints or mild cognitive impairment were recruited in Memory Clinic of Bordeaux (MEMENTO cohort). Cognitively normal controls were recruited. All participants were recorded with two successive polysomnography recordings one year apart. Delta, theta and sigma absolute spectral power and spindle characteristics (density, amplitude and frequency) were computed from purified CzOz EEG derivation during NREM sleep periods (ASEEGA software) across the whole second night. Results Twenty-nine patients (21 females, age=71 years ±7) and 29 controls were evaluated at T0. Logistic regression analyses showed that a reduced delta power (odds ratio (OR) 0.996, P<.05), theta power (OR 0.950, P<.05), sigma power (OR 0.662, P<.05), and spindle maximal amplitude (OR 0.728, P<.05) during NREM sleep periods were associated with cognitive impairment in aging. Variables were adjusted on age, gender, Body Mass Index, educational level and medication use. Seventeen patients were evaluated at one-year follow-up. Correlations showed that changes in self-reported sleep complaints, sleep consolidation and spindle characteristics (spectral power, maximal amplitude, duration and frequency) were associated with cognitive impairment (P<.05). Conclusion A reduction in slow-wave, theta and sigma activities, and a modification of spindle characteristics during NREM sleep, are associated very early with a higher risk of occurrence of cognitive impairment. Poor sleep consolidation, lower amplitude and faster frequency of spindles may be potentially early sleep biomarkers of worsening cognitive decline in older adults.
Figures & Tables
  • References (67)
  • Citations (2)
📖 Papers frequently viewed together
8 Authors (Ina Djonlagic, ..., Susan Redline)
1 Citations
78% of Scinapse members use related papers. After signing in, all features are FREE.
#1Echeverria RamirezH-Index: 1
#2Andrea CatalinaH-Index: 1
El sueno y la lactancia son dos fenomenos fisiologicos y comportamentales interrelacionados evolutivamente, que comparten una funcion homeostatica y se enmarcan en una influencia circadiana. El periodo neonatal y los primeros meses de vida representan una etapa crucial para el desarrollo de procesos de organizacion sinaptica, donde el sueno es considerado uno de los marcadores del neurodesarrollo y la lactancia materna como mecanismo complejo de alimentacion temprana, es imprescindible para opti...
867 CitationsSource
#1Ina Djonlagic (Harvard University)H-Index: 8
#2Daniel Aeschbach (Brigham and Women's Hospital)H-Index: 27
Last. Susan Redline (Harvard University)H-Index: 111
view all 8 authors...
The pathophysiological processes of Alzheimer’s dementia predate its clinical manifestation. Sleep disturbances can accelerate the aging process and are common features of dementia. This study examined whether quantitative sleep electroencephalogram changes predate the clinical development of mild cognitive impairment and/or incident dementia. We collected data from a nested case-control sample of women (mean age 83 years) from the Sleep and Cognition Study, an ancillary study to the longitudina...
4 CitationsSource
#1Véronique Latreille (UdeM: Université de Montréal)H-Index: 14
#2Malo Gaubert (UQAM: Université du Québec à Montréal)H-Index: 2
Last. Julie Carrier (UdeM: Université de Montréal)H-Index: 51
view all 6 authors...
Abstract Accumulating evidence demonstrates a direct relationship between impaired neural integrity and disrupted sleep physiology in normal and pathological aging. However, previous work has focus almost exclusively on nonrapid eye movement sleep electroencephalography as a proxy of cortical integrity with aging. Whether this relationship holds true for rapid eye movement sleep electroencephalography is unknown. Our results show that age-related reduction in low-frequency delta activity during ...
2 CitationsSource
#1Péter P. Ujma (Semmelweis University)H-Index: 8
#2Péter HalászH-Index: 31
Last. Raffaele FerriH-Index: 58
view all 5 authors...
Slow waves recorded with EEG in NREM sleep are indicative of the strength and spatial extent of synchronized firing in neuronal assemblies of the cerebral cortex. Slow waves often appear in the A1 part of the cyclic alternating patterns (CAP), which correlate with a number of behavioral and biological parameters, but their physiological significance is not adequately known. We automatically detected slow waves from the scalp recordings of 37 healthy patients, visually identified CAP A1 events an...
3 CitationsSource
#1Seung Wan SuhH-Index: 2
#2Ji Won HanH-Index: 17
Last. Ki Woong KimH-Index: 41
view all 25 authors...
9 CitationsSource
#1Carole Dufouil (University of Bordeaux)H-Index: 54
#2Bruno Dubois (UPMC: Pierre-and-Marie-Curie University)H-Index: 107
Last. Geneviève Chêne (University of Bordeaux)H-Index: 64
view all 41 authors...
Background The natural history and disease mechanisms of Alzheimer’s disease and related disorders (ADRD) are still poorly understood. Very few resources are available to scrutinise patients as early as needed and to use integrative approaches combining standardised, repeated clinical investigations and cutting-edge biomarker measurements.
6 CitationsSource
#1Thien Thanh Dang-VuH-Index: 30
#2Benjamin Hatch (Concordia University)H-Index: 1
Last. Jean-Philippe Gouin (Concordia University)H-Index: 16
view all 9 authors...
Abstract Background While cognitive-behavioral therapy for insomnia constitutes the first-line treatment for chronic insomnia, only few reports have investigated how sleep architecture relates to response to this treatment. In this pilot study, we aimed to determine whether pre-treatment sleep spindle density predicts treatment response to cognitive-behavioral therapy for insomnia. Methods Twenty-four participants with chronic primary insomnia participated in a 6-week cognitive-behavioral therap...
1 CitationsSource
#1Julia Ladenbauer (Charité)H-Index: 3
#2Josef Ladenbauer (Technical University of Berlin)H-Index: 9
Last. Agnes Flöel (Charité)H-Index: 49
view all 7 authors...
Alzheimer9s disease (AD) not only involves loss of memory functions, but also prominent deterioration of sleep physiology, which is already evident at the stage of mild cognitive impairment (MCI). Cortical slow oscillations (SO; 0.5–1 Hz) and thalamocortical spindle activity (12–15 Hz) during sleep, and their temporal coordination, are considered critical for memory formation. We investigated the potential of slow oscillatory transcranial direct current stimulation (so-tDCS), applied during a da...
39 CitationsSource
#1Carolin Reichert (University of Basel)H-Index: 10
#2Micheline Maire (University of Basel)H-Index: 10
Last. Christina Schmidt (University of Basel)H-Index: 22
view all 13 authors...
The two-process model of sleep-wake regulation posits that sleep-wake-dependent homeostatic processes interact with the circadian timing system to affect human behavior. The circadian timing system is fundamental to maintaining stable cognitive performance, as it counteracts growing homeostatic sleep pressure during daytime. Using magnetic resonance imaging, we explored brain responses underlying working memory performance during the time of maximal circadian wake-promotion under varying sleep p...
18 CitationsSource
#2Hong-Viet V. Ngo (University of Tübingen)H-Index: 4
Last. Hee-Sup ShinH-Index: 42
view all 4 authors...
Summary While the interaction of the cardinal rhythms of non-rapid-eye-movement (NREM) sleep—the thalamo-cortical spindles, hippocampal ripples, and the cortical slow oscillations—is thought to be critical for memory consolidation during sleep, the role spindles play in this interaction is elusive. Combining optogenetics with a closed-loop stimulation approach in mice, we show here that only thalamic spindles induced in-phase with cortical slow oscillation up-states, but not out-of-phase-induced...
108 CitationsSource
Cited By2
#1Abdellah Ahnaou (Janssen Pharmaceutica)H-Index: 12
#2D. Rodriguez-Manrique (Janssen Pharmaceutica)
Last. Wilhelmus Drinkenburg (Janssen Pharmaceutica)H-Index: 25
view all 7 authors...
The aging process eventually causea breakdown in critical synaptic plasticity and connectivity leading to deficits in memory function. The olfactory bulb (OB) and the hippocampus, both regions of the brain considered critical for the processing of odors and spatial memory, are commonly affected by aging. Using an aged wild-type C57B/6 mouse model, we sought to define the effects of aging on hippocampal plasticity and the integrity of cortical circuits. Specifically, we measured the long-term pot...
Symptomatic interventions for patients with dementia involve anti-dementia drugs to improve cognition, psychotropic drugs for the treatment of behavioral disorders (BDs), and different categories of drugs for concomitant disorders. Demented patients may take >6–10 drugs/day with the consequent risk for drug–drug interactions and adverse drug reactions (ADRs >80%) which accelerate cognitive decline. The pharmacoepigenetic machinery is integrated by pathogenic, mechanistic, metabolic, transporter,...
1 CitationsSource
#1Coleman B. Calva (USC: University of South Carolina)H-Index: 2
#2Habiba Fayyaz (USC: University of South Carolina)H-Index: 1
Last. Jim R. Fadel (USC: University of South Carolina)H-Index: 26
view all 3 authors...
Cognitive function represents a key determinative factor for independent functioning amongst the elderly, especially among those with age-related cognitive disorders. However; existing pharmacotherapeutic tactics for treating these disorders provide only modest benefits on cognition. The hypothalamic orexin (hypocretin) system is uniquely positioned, anatomically and functionally, to integrate physiological functions that support proper cognition. The ongoing paucity of orexin receptor agonists ...
#1Robin K. Yuan (Harvard University)H-Index: 5
#1Robin K. Yuan (UTSA: University of Texas at San Antonio)
Last. Isabel A. Muzzio (UTSA: University of Texas at San Antonio)H-Index: 1
view all 9 authors...
Age-related changes in sleep patterns have been linked to cognitive decline. Specifically, age is associated with increased fragmentation of sleep and wake cycles. Yet it remains unknown if improvements in sleep architecture can ameliorate cellular and cognitive deficits. We evaluated how changes in sleep architecture following sleep restriction affected hippocampal representations and memory in young and old mice. Following training in a hippocampus dependent object/place recognition task, cont...
#1Shunjie Liu (SYSU: Sun Yat-sen University)H-Index: 1
#2Junhao Pan (SYSU: Sun Yat-sen University)H-Index: 1
Last. Zhong Li (SYSU: Sun Yat-sen University)H-Index: 3
view all 8 authors...
Purpose Sleep disturbances are common in Alzheimer’s disease (AD) and mild cognitive impairment (MCI) patients. Non-rapid eye movement stage 3 (N3), rapid eye movement stage (REM), spindle density, and K-complex (KC) density are decreased in MCI and AD patients. Periodic limb movements in sleep (PLMS) are increased in other neurodegenerative diseases. We aimed to distinguish amnestic mild cognitive impairment (aMCI) patients from the overall population of MCI patients by comparing the N3 and REM...
1 CitationsSource
#1Pace Marta (IIT: Istituto Italiano di Tecnologia)
#2Colombi Ilaria (IIT: Istituto Italiano di Tecnologia)
Last. Tucci Valter (IIT: Istituto Italiano di Tecnologia)
view all 12 authors...
Prader-Willi syndrome (PWS) is a neurodevelopmental disorder that is characterized by rapid eye movement (REM) sleep abnormalities. The disease is caused by genomic imprinting defects that are inherited through the paternal line. Among the genes located in the PWS region on chromosome 15 (15q11-q13), small nucleolar RNA 116 (Snord116) has been previously associated with intrusions of REM sleep into wakefulness in both humans and mice. Here, we further explore the processes of sleep regulation by...
#1George A. Edwards Iii (University of Texas Health Science Center at Houston)H-Index: 1
#2Nazaret Gamez (UMA: University of Málaga)H-Index: 1
Last. Ines Moreno-Gonzalez (UMA: University of Málaga)H-Index: 15
view all 5 authors...
Since first described in the early 1900s, Alzheimer’s disease (AD) has risen exponentially in prevalence and concern. Research still drives to understand the etiology and pathogenesis of this disease and what risk factors can attribute to AD. With a majority of AD cases being of sporadic origin, the increasing exponential growth of an aged population and a lack of treatment, it is imperative to discover an easy accessible preventative method for AD. Some risk factors can increase the propensity ...
1 CitationsSource
Cognitive deterioration caused by illness or aging often occurs before symptoms arise, and its timely diagnosis is crucial to reducing its medical, personal, and societal impacts. Brain–computer interfaces (BCIs) stimulate and analyze key cerebral rhythms, enabling reliable cognitive assessment that can accelerate diagnosis. The BCI system presented analyzes steady-state visually evoked potentials (SSVEPs) elicited in subjects of varying age to detect cognitive aging, predict its magnitude, and ...