Age-related decrease in cortical excitability circadian variations during sleep loss and its links with cognition.

Published on Jun 1, 2019in Neurobiology of Aging4.398
· DOI :10.1016/J.NEUROBIOLAGING.2019.02.004
Giulia Gaggioni6
Estimated H-index: 6
(University of Liège),
Julien Q. M. Ly4
Estimated H-index: 4
(University of Liège)
+ 16 AuthorsGilles Vandewalle38
Estimated H-index: 38
(University of Liège)
Abstract Cortical excitability depends on sleep-wake regulation, is central to cognition, and has been implicated in age-related cognitive decline. The dynamics of cortical excitability during prolonged wakefulness in aging are unknown, however. Here, we repeatedly probed cortical excitability of the frontal cortex using transcranial magnetic stimulation and electroencephalography in 13 young and 12 older healthy participants during sleep deprivation. Although overall cortical excitability did not differ between age groups, the magnitude of cortical excitability variations during prolonged wakefulness was dampened in older individuals. This age-related dampening was associated with mitigated neurobehavioral consequences of sleep loss on executive functions. Furthermore, higher cortical excitability was potentially associated with better and lower executive performance, respectively, in older and younger adults. The dampening of cortical excitability dynamics found in older participants likely arises from a reduced impact of sleep homeostasis and circadian processes. It may reflect reduced brain adaptability underlying reduced cognitive flexibility in aging. Future research should confirm preliminary associations between cortical excitability and behavior and address whether maintaining cortical excitability dynamics can counteract age-related cognitive decline.
  • References (64)
  • Citations (6)
📖 Papers frequently viewed together
7 Citations
78% of Scinapse members use related papers. After signing in, all features are FREE.
#1L E McKillop (University of Oxford)H-Index: 5
#2Simon P. Fisher (University of Oxford)H-Index: 13
Last. Vladyslav V. Vyazovskiy (University of Oxford)H-Index: 33
view all 7 authors...
Healthy ageing is associated with marked effects on sleep, including its daily amount and architecture, as well as the specific electroencephalogram (EEG) oscillations. Neither the neurophysiological underpinnings, nor the biological significance of these changes are understood, and crucially the question remains whether ageing is associated with reduced sleep need or a diminished capacity to generate sufficient sleep. Here we tested the hypothesis that ageing may affect local cortical networks,...
17 CitationsSource
Working memory (WM) performance decreases with age. A promising method to improve WM is physical or cognitive training. The present randomized controlled study is aimed at evaluating the effects of different training methods on WM. A sample of 141 healthy older adults (mean age 70 years) was assigned to one of four groups: physical training, cognitive training, a social control group, and a no-contact control group. The participants trained for four months. Before and after the training, n-back ...
10 CitationsSource
#1Byron C. Jaeger (UNC: University of North Carolina at Chapel Hill)H-Index: 6
#2Lloyd J. Edwards (UNC: University of North Carolina at Chapel Hill)H-Index: 38
Last. Pranab Kumar Sen (UNC: University of North Carolina at Chapel Hill)H-Index: 44
view all 4 authors...
Measuring the proportion of variance explained ( R^2 R2) by a statistical model and the relative importance of specific predictors (semi-partial R^2 R2) can be essential considerations when building a parsimonious statistical model. The R^2 R2 statistic is a familiar summary of goodness-of-fit for normal linear models and has been extended in various ways to more general models. In particular, the generalized linear mixed model (GLMM) extends the normal linear model and is used to an...
109 CitationsSource
#1Florinda Ferreri (Università Campus Bio-Medico)H-Index: 12
#2Fabrizio VecchioH-Index: 41
Last. Vincenzo Di Lazzaro (Università Campus Bio-Medico)H-Index: 42
view all 11 authors...
Abstract It was recently demonstrated that the characteristics of EEG rhythms preceding a transcranial magnetic stimulation (TMS) of the motor cortex (M1) influence the motor-evoked potential (MEP) amplitude with a peculiar pattern, thus reflecting the M1 functional state. As physiological aging is related to a decrease in motor performance and changes in excitability and connectivity strength within cerebral sensorimotor circuits, we aimed to explore whether aging affects EEG-MEP interactions. ...
12 CitationsSource
#1Luisa de Vivo (UW: University of Wisconsin-Madison)H-Index: 11
#2Michele Bellesi (Marche Polytechnic University)H-Index: 20
Last. Chiara Cirelli (UW: University of Wisconsin-Madison)H-Index: 58
view all 7 authors...
It is assumed that synaptic strengthening and weakening balance throughout learning to avoid runaway potentiation and memory interference. However, energetic and informational considerations suggest that potentiation should occur primarily during wake, when animals learn, and depression should occur during sleep. We measured 6920 synapses in mouse motor and sensory cortices using three-dimensional electron microscopy. The axon-spine interface (ASI) decreased ~18% after sleep compared with wake. ...
200 CitationsSource
#1Julien Q. M. LyH-Index: 4
#2Giulia Gaggioni (University of Liège)H-Index: 6
Last. Gilles Vandewalle (University of Liège)H-Index: 38
view all 16 authors...
Cognitive performance is impaired after prolonged wakefulness, yet the contribution of circadian rhythms for proper brain function remains unclear. Here the authors show that cortical excitability measured using TMS exhibits robust circadian dynamics which is correlated with cognitive performance.
56 CitationsSource
#1Mara Mather (SC: University of Southern California)H-Index: 50
#2Carolyn W. Harley (MUN: Memorial University of Newfoundland)H-Index: 35
Research on cognitive aging has focused on how decline in various cortical and hippocampal regions influence cognition. However, brainstem regions play essential modulatory roles, and new evidence suggests that, among these, the integrity of the locus coeruleus (LC)–norepinephrine (NE) system plays a key role in determining late-life cognitive abilities. The LC is especially vulnerable to toxins and infection and is often the first place Alzheimer's-related pathology appears, with most people sh...
122 CitationsSource
#1Cho-Yi Chen (University of Pittsburgh)H-Index: 10
#2Ryan W. Logan (University of Pittsburgh)H-Index: 19
Last. Colleen A. McClung (University of Pittsburgh)H-Index: 36
view all 7 authors...
Abstract With aging, significant changes in circadian rhythms occur, including a shift in phase toward a “morning” chronotype and a loss of rhythmicity in circulating hormones. However, the effects of aging on molecular rhythms in the human brain have remained elusive. Here, we used a previously described time-of-death analysis to identify transcripts throughout the genome that have a significant circadian rhythm in expression in the human prefrontal cortex [Brodmann’s area 11 (BA11) and BA47]. ...
88 CitationsSource
#1Christian MeiselH-Index: 17
#2Andreas Schulze-Bonhage (University Medical Center Freiburg)H-Index: 58
Last. Dietmar PlenzH-Index: 38
view all 6 authors...
Pathological changes in excitability of cortical tissue commonly underlie the initiation and spread of seizure activity in patients suffering from epilepsy. Accordingly, monitoring excitability and controlling its degree using antiepileptic drugs (AEDs) is of prime importance for clinical care and treatment. To date, adequate measures of excitability and action of AEDs have been difficult to identify. Recent insights into ongoing cortical activity have identified global levels of phase synchroni...
55 CitationsSource
#1Bérengère Staub (French Institute of Health and Medical Research)H-Index: 5
#2Nadège Doignon-Camus (French Institute of Health and Medical Research)H-Index: 10
Last. Anne Bonnefond (French Institute of Health and Medical Research)H-Index: 15
view all 5 authors...
Previous studies examining sustained attention ability in older adults have yielded inconsistent results: age-related decline in studies using traditionally formatted tasks (TFT), in which subjects have to respond to rare targets, and preservation in studies using Go/No-Go tasks, in which subjects have to withhold response to rare targets. The purpose of this study was to examine whether these discrepancies could be explained by a differential use of automatic and controlled processes according ...
11 CitationsSource
Cited By6
#1Brian V. Lananna (WashU: Washington University in St. Louis)H-Index: 3
#2Erik S. Musiek (WashU: Washington University in St. Louis)H-Index: 28
A substantial body of research now implicates the circadian clock in the regulation of an array of diverse biological processes including glial function, metabolism, peripheral immune responses, and redox homeostasis. Sleep abnormalities and other forms of circadian disruption are common symptoms of aging and neurodegeneration. Circadian clock disruption may also influence the aging processes and the pathogenesis of neurodegenerative diseases. The specific mechanisms governing the interaction be...
#1Paolo Cardone (University of Liège)H-Index: 1
#2Maxime Van Egroo (University of Liège)H-Index: 2
Last. Gilles Vandewalle (University of Liège)H-Index: 38
view all 6 authors...
Modern lifestyle curtails sleep and increases nighttime work and leisure activities. This has a deleterious impact on vigilance and attention, exacerbating chances of committing attentional lapses, with potential dramatic outcomes. A full characterization of the brain mechanisms associated with lapses is still lacking. Here, we investigated the brain signature of attentional lapses and assessed whether cortical excitability and brain response propagation were modified during lapses and whether t...
#1Fang Zhou (Shanxi Medical University)H-Index: 2
#2Xu-Dong Yan (Shanxi Medical University)H-Index: 1
Last. Mei-Na Wu (Shanxi Medical University)H-Index: 12
view all 10 authors...
Abstract Cognitive impairments and circadian rhythm disorders (CRD) are the main clinical manifestations of Alzheimer's disease (AD). Orexin has been reported abnormally elevated in the cerebrospinal fluid of AD patients, accompanied with cognitive impairments. Our recent research revealed that suvorexant, a dual orexin receptor antagonist, could improve behavioral CRD in 9-month-old APP/PS1 mice. Considering the close relationship between cognition and circadian rhythm, here we further observed...
#1Yexin He (Shanxi Medical University)H-Index: 2
#2Yiying Li (Shanxi Medical University)H-Index: 1
Last. Mei-Na Wu (Shanxi Medical University)H-Index: 12
view all 5 authors...
Cognitive decline, memory impairment and circadian rhythm disturbance are iconic manifestations of Alzheimer’s disease (AD). APPswe/PS1dE9 (APP/PS1) mice, a model of AD, show deficits in multiple learning and memory abilities, synaptic plasticity, and behavioral circadian rhythm, but whether circadian differences in cognitive performance and synaptic plasticity could be affected in AD remain unclear. Here, the cognitive behaviors of 6-month-old APP/PS1 mice were assessed by multiple behavior tes...
2 CitationsSource
#1Maxime Van Egroo (University of Liège)H-Index: 2
#2Justinas Narbutas (University of Liège)H-Index: 2
Last. Gilles Vandewalle (University of Liège)H-Index: 38
view all 22 authors...
Age-related cognitive decline arises from alterations in brain structure as well as in sleep-wake regulation. Here, we investigated whether preserved wake-dependent regulation of cortical function could represent a positive factor for cognitive fitness in aging. We quantified cortical excitability dynamics during prolonged wakefulness as a sensitive marker of age-related alteration in sleep-wake regulation in 60 healthy older individuals (50–69 y; 42 women). Brain structural integrity was assess...
2 CitationsSource