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Decreased Electroencephalography Global Field Synchronization in Slow-Frequency Bands Characterizes Synaptic
Una Smailovic1,2, Daniel Ferreira1,3, Birgitta Ausén1,4,5
1Division of Clinical Geriatrics, Center for Alzheimer Research, Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Huddinge, Sweden.
Background:
Mild cognitive impairment (MCI) is highly prevalent in a memory clinic setting and is heterogeneous regarding its clinical presentation, underlying pathophysiology, and prognosis. The most prevalent subtypes are single-domain amnestic MCI (sd-aMCI), considered to be a prodromal phase of Alzheimer's disease (AD), and multidomain amnestic MCI (md-aMCI), which is associated with multiple etiologies. Since synaptic loss and dysfunction are the closest pathoanatomical correlates of AD-related cognitive impairment, we aimed to characterize it in patients with sd-aMCI and md-aMCI by means of resting-state electroencephalography (EEG) global field power (GFP), global field synchronization (GFS), and novel cerebrospinal fluid (CSF) synaptic biomarkers.
Methods:
We included 52 patients with sd-aMCI (66.9 ± 7.3 years, 52% women) and 30 with md-aMCI (63.1 ± 7.1 years, 53% women). All patients underwent a detailed clinical assessment, resting-state EEG recordings and quantitative analysis (GFP and GFS in delta, theta, alpha, and beta bands), and analysis of CSF biomarkers of synaptic dysfunction, neurodegeneration, and AD-related pathology. Cognitive subtyping was based on a comprehensive neuropsychological examination. The Mini-Mental State Examination (MMSE) was used as an estimation of global cognitive performance. EEG and CSF biomarkers were included in a multivariate model together with MMSE and demographic variables, to investigate differences between sd-aMCI and md-aMCI.
Results:
Patients with sd-aMCI had higher CSF phosphorylated tau, total tau and neurogranin levels, and lower values in GFS delta and theta. No differences were observed in GFP. The multivariate model showed that the most important synaptic measures for group separation were GFS theta, followed by GFS delta, GFP theta, CSF neurogranin, and GFP beta.
Conclusion:
Patients with sd-aMCI when compared with those with md-aMCI have a neurophysiological and biochemical profile of synaptic damage, neurodegeneration, and amyloid pathology closer to that described in patients with AD. The most prominent signature in sd-aMCI was a decreased global synchronization in slow-frequency bands indicating that functional connectivity in slow frequencies is more specifically related to early effects of AD-specific molecular pathology.
Insights
Single-domain amnestic mild cognitive impairment (MCI) shows synaptic damage and neurodegeneration closer to Alzheimer's disease (AD). Decreased global synchronization in slow frequencies in sd-aMCI is linked to early AD molecular pathology.
Area of Science:
- Neuroscience
- Biochemistry
- Clinical Neurology
Background:
- Mild cognitive impairment (MCI) is a heterogeneous condition with various subtypes.
- Single-domain amnestic MCI (sd-aMCI) is considered a prodromal phase of Alzheimer's disease (AD).
- Multidomain amnestic MCI (md-aMCI) is associated with multiple etiologies.
Purpose of the Study:
- To characterize synaptic function in sd-aMCI and md-aMCI patients.
- To investigate differences using resting-state EEG (GFP, GFS) and CSF synaptic biomarkers.
- To correlate neurophysiological and biochemical profiles with AD-related pathology.
Main Methods:
- Included 52 sd-aMCI and 30 md-aMCI patients.
- Performed detailed clinical assessment, resting-state EEG, and CSF biomarker analysis.
- Utilized multivariate models with EEG, CSF, MMSE, and demographic data for group comparison.
Main Results:
- sd-aMCI patients exhibited higher CSF phosphorylated tau, total tau, and neurogranin levels.
- sd-aMCI patients showed lower GFS in delta and theta bands compared to md-aMCI.
- Multivariate analysis identified GFS theta, GFS delta, GFP theta, CSF neurogranin, and GFP beta as key discriminators.
Conclusions:
- sd-aMCI patients present a neurophysiological and biochemical profile similar to AD patients.
- Decreased global synchronization in slow frequencies in sd-aMCI is linked to early AD molecular pathology.
- Functional connectivity in slow frequencies may be a specific indicator of early AD effects.
