Disrupted Neural Synchrony Mediates the Relationship between White Matter Integrity and Cognitive Performance in Older Adults

Hinault, Thomas; Kraut, Michael A.; Bakker, Arnold B.; Courtney, Susan

doi:10.1093/cercor/bhaa141

Cited by 26 publications

(20 citation statements)

References 94 publications

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“…Maintenance-related patterns were also observed in healthy older individuals, with a relative absence of impairments in frontoparietal communication dynamics associated with preserved cognitive performance (Rondina et al, 2019 ; Hinault et al, 2020 , 2021 ). The brain's structure-function interplay appears to be at the heart of the heterogeneity associated with maintenance during aging (Courtney and Hinault, 2021 ; Jauny et al, 2022 ).…”

Section: Discussionmentioning

confidence: 94%

“…As we have seen in these different sections, changes in synchrony vary over time and with task difficulty, and increased synchrony is not always beneficial. These changes appear to be related to changes in the level of white matter fibers integrity (Hinault et al, 2020 , 2021 ). Indeed, the presence of white matter lesions has been associated with decreased brain synchrony (Wessel et al, 2016 ).…”

Section: Normal Agingmentioning

confidence: 99%

“…This functional maintenance seems to critically depend on the maintenance of the underlying structures of the brain networks. Hinault et al ( 2020 ) investigated the structure-function relationship between diffusion tensor imaging (DTI) and EEG data of neuronal synchrony (PLV) of young and old healthy participants. The authors used an arithmetic task, in which participants had to maintain, or update, arithmetic operations (addition, multiplication) in working memory to determine whether the proposed equation results (e.g., 8 × 4 = 36) were correct or incorrect.…”

Section: Normal Agingmentioning

confidence: 99%

“…Given the critical involvement of coordinated brain rhythms in higher-order cognitive processing, age-related changes in the dynamic of brain communications may act as a marker for cognitive decline in older adults. Such complex interplay across rhythms is highly sensitive to structural changes and the progression of neurodegenerative disorders (e.g., Gaubert et al, 2019 ; Courtney and Hinault, 2021 ) as even small changes of dynamic synchrony can lead to cognitive decline with aging (e.g., Hinault et al, 2020 , 2021 ; Kumral et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

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M/EEG Dynamics Underlying Reserve, Resilience, and Maintenance in Aging: A Review

2022

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Cognitive reserve and resilience refer to the set of processes allowing the preservation of cognitive performance in the presence of structural and functional brain changes. Investigations of these concepts have provided unique insights into the heterogeneity of cognitive and brain changes associated with aging. Previous work mainly relied on methods benefiting from a high spatial precision but a low temporal resolution, and thus the temporal brain dynamics underlying these concepts remains poorly known. Moreover, while spontaneous fluctuations of neural activity have long been considered as noise, recent work highlights its critical contribution to brain functions. In this study, we synthesized the current state of knowledge from magnetoencephalography (MEG) and electroencephalography (EEG) studies that investigated the contribution of maintenance of neural synchrony, and variability of brain dynamics, to cognitive changes associated with healthy aging and the progression of neurodegenerative disease (such as Alzheimer's disease). The reviewed findings highlight that compensations could be associated with increased synchrony of higher (>10 Hz) frequency bands. Maintenance of young-like synchrony patterns was also observed in healthy older individuals. Both maintenance and compensation appear to be highly related to preserved structural integrity (brain reserve). However, increased synchrony was also found to be deleterious in some cases and reflects neurodegenerative processes. These results provide major elements on the stability or variability of functional networks as well as maintenance of neural synchrony over time, and their association with individual cognitive changes with aging. These findings could provide new and interesting considerations about cognitive reserve, maintenance, and resilience of brain functions and cognition.

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Section: Discussionmentioning

confidence: 94%

Section: Normal Agingmentioning

confidence: 99%

Section: Normal Agingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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M/EEG Dynamics Underlying Reserve, Resilience, and Maintenance in Aging: A Review

2022

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“…With aging, PAF will typically drift lower once again, with the average PAF of those near 70 years old being closer to 8 Hz (Dustman et al, 1999;Scally et al, 2018). The typical developmental trajectory of increasing working memory performance and capacity, followed by subsequent advanced-age declines (e.g., Park et al, 2002;Hamilton et al, 2003;Reuter-Lorenz and Park, 2010;Hinault et al, 2020), occur in seeming parallel to these described increases and decreases in PAF.…”

Section: Peak Alpha Frequencymentioning

confidence: 95%

Modulation of Peak Alpha Frequency Oscillations During Working Memory Is Greater in Females Than Males

Ghazi

Blacker

Hinault

et al. 2021

Front. Hum. Neurosci.

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Peak alpha frequency is known to vary not just between individuals, but also within an individual over time. While variance in this metric between individuals has been tied to working memory performance, less understood are how short timescale modulations of peak alpha frequency during task performance may facilitate behavior. This gap in understanding may be bridged by consideration of a key difference between individuals: sex. Inconsistent findings in the literature regarding the relationship between peak alpha frequency and cognitive performance, as well as known sex-related-differences in peak alpha frequency and its modulation motivated our hypothesis that cognitive and neural processes underlying working memory—modulation of peak alpha frequency in particular—may differ based upon sex. Targeting sex as a predictive factor, we analyzed the EEG data of participants recorded while they performed four versions of a visual spatial working memory task. A significant difference between groups was present: females modulated peak alpha frequency more than males. Task performance did not differ by sex, yet a relationship between accuracy and peak alpha frequency was present in males, but not in females. These findings highlight the importance of considering sex as a factor in the study of oscillatory activity, particularly to further understanding of the neural mechanisms that underlie working memory.

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The link between executive skills and neural dynamics during encoding, inhibition, and retrieval of visual information in the elderly

Parviainen,

Alexandrou,

Lapinkero

et al. 2024

Human Brain Mapping

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During aging the inter‐individual variability in both the neural and behavioral functions is likely to be emphasized. Decreased competence particularly in working memory and general executive control compromises many aspects of the quality of life also within the nonclinical population. We aimed, first, to clarify the brain basis of visual working memory and inhibition during multi‐stage natural‐like task performance, and second, to identify associations between variation in task‐related neural activity and relevant cognitive skills, namely inhibition and general working memory capacity. We recorded, using magnetoencephalography (MEG), the neural modulations associated with encoding, maintenance, and retrieval, as well as interference suppression during a visual working memory task in older adults. We quantified the neural correlates of these cognitive processes through two complementary approaches: evoked responses and oscillatory activity. Neural activity during memory retrieval and interference suppression were correlated with behavioral measures of task switching and general executive functions. Our results show that general inhibitory control induced frontocentral neural modulation across a broad range of frequencies whereas domain‐specific inhibition was limited to right posterior areas. Our findings also suggest that modulations particularly in phase‐locked evoked neural activity can be reliably associated with explicit measures of cognitive skills, with better inhibitory control linked with an early neural effect of distractor inhibition during retrieval. In general, we show that exploiting the inherent inter‐individual variability in neural measures and behavioral markers of cognition in aging populations can help establish reliable links between specific brain functions and their behavioral manifestations.

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Disrupted Neural Synchrony Mediates the Relationship between White Matter Integrity and Cognitive Performance in Older Adults

Cited by 26 publications

References 94 publications

M/EEG Dynamics Underlying Reserve, Resilience, and Maintenance in Aging: A Review

M/EEG Dynamics Underlying Reserve, Resilience, and Maintenance in Aging: A Review

Modulation of Peak Alpha Frequency Oscillations During Working Memory Is Greater in Females Than Males

The link between executive skills and neural dynamics during encoding, inhibition, and retrieval of visual information in the elderly

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