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Electroencephalographic Cross-Frequency Coupling as a Sign of Disease Progression in Patients With Mild Cognitive Impairment: A Pilot Study.

ABSTRACT: Mild cognitive impairment (MCI) refers to mild objective cognitive deficits and is associated with the later development of Alzheimer's disease (AD). However, not all patients with MCI convert to AD. EEG spectral power has shown promise as a marker of progression, but brain oscillations in different frequencies are not isolated entities. Coupling between different frequency bands, so-called cross-frequency coupling (CFC), has been associated with memory function and may further contribute to our understanding of what characterizes patients with MCI who progress to AD. In the current study, we wanted to investigate the changes in gamma/theta CFC in patients with AD and MCI compared to HC and in patients with pMCI compared to patients with sMCI. Furthermore, we wanted to investigate the association with cognitive test scores. EEGs were included at baseline for 15 patients with AD, 25 patients with MCI, and 36 older HC, and the participants were followed for up to 3 years. To investigate CFC, we calculated the modulation index (MI), which has been shown to be less affected by noisy data compared to other techniques. We found that patients with pMCI showed a significantly lower global gamma/theta CFC compared to patients with sMCI. In addition, global gamma/theta CFC was significantly correlated with Addenbrooke's Cognitive Examination (ACE) score (p-value = 0.030, rho = 0.527). Although not significant, patients with AD and MCI showed a lower gamma/theta CFC compared to HC. These findings suggest that gamma/theta CFC is important for proper cognitive functioning and that a decrease in gamma/theta CFC in patients with MCI may be a sign of progression. Gamma/theta CFC may therefore serve as a progression marker in MCI, but larger studies are needed to validate these findings.

SUBMITTER: Musaeus CS

PROVIDER: S-EPMC7431634 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Electroencephalographic Cross-Frequency Coupling as a Sign of Disease Progression in Patients With Mild Cognitive Impairment: A Pilot Study.

Musaeus Christian Sandøe CS Nielsen Malene Schjønning MS Musaeus Jørgen Sandøe JS Høgh Peter P

Frontiers in neuroscience 20200811

Mild cognitive impairment (MCI) refers to mild objective cognitive deficits and is associated with the later development of Alzheimer's disease (AD). However, not all patients with MCI convert to AD. EEG spectral power has shown promise as a marker of progression, but brain oscillations in different frequencies are not isolated entities. Coupling between different frequency bands, so-called cross-frequency coupling (CFC), has been associated with memory function and may further contribute to our ...[more]

PMID: 32848563

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Project description:IntroductionElectroencephalographic (EEG) abnormalities are seen in patients with Alzheimer's disease (AD) and mild cognitive impairment (MCI) with characteristic features of cognitive impairment. The most common findings of EEG features in AD and MCI patients are increased relative power of slow oscillations (delta and theta rhythms) and decreased relative power of fast oscillations (alpha, beta and gamma rhythms). However, impairments in cognitive processes in AD and MCI are not sufficiently reflected by brain oscillatory activity in a particular frequency band. MCI patients are at high risk of progressing to AD. Cross-frequency coupling (CFC), which refers to coupling between different frequency bands, is a crucial tool for comprehending changes in brain oscillations and cognitive performance. CFC features exhibit some specificity in patients with AD and MCI, but a comparison between CFC features in individuals with these disorders is still lacking. The aim of this study was to explore changes in CFC properties in MCI and AD and to explore the relationship between CFC properties and multiple types of cognitive functional performance.MethodsWe recorded resting-state EEG (rsEEG) signals in 46 MCI patients, 43 AD patients, and 43 cognitively healthy controls (HCs) and analyzed the changes in CFC as well as the relationship between CFC and scores on clinical tests of cognitive function.Results and discussionMultiple couplings between low-frequency oscillations and high-frequency oscillations were found to be significantly enhanced in AD patients compared to those of HCs and MCI, while delta-gamma as well as theta-gamma couplings in the right temporal and parietal lobes were significantly enhanced in MCI patients compared to HCs. Moreover, theta-gamma coupling in the right temporal lobe tended to be stronger in MCI patients than in HCs, and it was stronger in AD than in MCI. Multiple CFC properties were found to correlate significantly with various cognitive domains, especially the memory function domain. Overall, these findings suggest that AD and MCI patients must use more neural resources to maintain a resting brain state and that alterations in theta-gamma coupling in the temporal lobe become progressively obvious during disease progression and are likely to be a valuable indicator of MCI and AD pathology.

Project description:BackgroundStudies at specific frequencies have shown abnormalities in brain functional networks among mild cognitive impairment (MCI) and Alzheimer's disease (AD) patients. Previous studies have failed to take into account the possibility that optimal cognitive integration requires interactions between different frequency bands.PurposeTo study whether there is abnormal cross-frequency integration in patients' brains during disease progression.Study typeRetrospective.PopulationForty-six normal control (NC), 85 patients with MCI, and 31 patients with AD.Field strength/sequence3T.AssessmentMultilayer network models were constructed for NC, MCI, and AD, and multilayer participation coefficient (MPC) was used to study the changes of the interlayer relationship in the course of disease development. In addition, MPC and an overlapping degree were combined to classify nodes in the network, and the role of key nodes in the interlayer interaction was mainly observed. Finally, the correlation between multilayer network measures and cognitive function was investigated.Statistical testsPearson chi-squared two-tailed test, one-way analysis of variance (ANOVA), nonparametric Spearman correlation coefficient r, and the false discovery rate.ResultsThe MPC of the network decreased significantly in MCI (P < 0.05) and AD (P < 0.05). The number of intralayer nodes increased significantly (MCI [P < 0.05], AD [P < 0.05]) and the number of interlayer nodes decreased significantly. Centrality loss between frequencies of a large number of hub nodes, among which the damaged hub nodes included the left hippocampus, left precuneus, right precuneus, left posterior cingulate gyrus, left precentral gyrus, right precentral gyrus, left medial superior frontal gyrus, and right postcentral gyrus. MPC was significantly associated with memory impairment in patients (AD [Spearman's r = 0.526, P < 0.05], MCI [Spearman's r = 0.229, P < 0.05]), and these related regions included damaged hub nodes in patients.Data conclusionIn the multilayer networks of patients, there was an obvious deficit in cross-frequency integration and the hub nodes were preferentially damaged. Moreover, these vulnerable hubs are associated with patients' cognitive scores.Level of evidence1 TECHNICAL EFFICACY STAGE: 3.

Dataset Information

Electroencephalographic Cross-Frequency Coupling as a Sign of Disease Progression in Patients With Mild Cognitive Impairment: A Pilot Study.

Publications

Electroencephalographic Cross-Frequency Coupling as a Sign of Disease Progression in Patients With Mild Cognitive Impairment: A Pilot Study.

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