Decreased Electroencephalography Global Field Synchronization in Slow-Frequency Bands Characterizes Synaptic Dysfunction in Amnestic Subtypes of Mild Cognitive Impairment
BackgroundMild 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 Al...
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Frontiers Media S.A.
2022-04-01
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| Series: | Frontiers in Aging Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnagi.2022.755454/full |
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| author | Una Smailovic Una Smailovic Daniel Ferreira Daniel Ferreira Birgitta Ausén Birgitta Ausén Birgitta Ausén Nicholas James Ashton Nicholas James Ashton Nicholas James Ashton Nicholas James Ashton Nicholas James Ashton Thomas Koenig Henrik Zetterberg Henrik Zetterberg Henrik Zetterberg Henrik Zetterberg Henrik Zetterberg Kaj Blennow Kaj Blennow Vesna Jelic Vesna Jelic |
| author_facet | Una Smailovic Una Smailovic Daniel Ferreira Daniel Ferreira Birgitta Ausén Birgitta Ausén Birgitta Ausén Nicholas James Ashton Nicholas James Ashton Nicholas James Ashton Nicholas James Ashton Nicholas James Ashton Thomas Koenig Henrik Zetterberg Henrik Zetterberg Henrik Zetterberg Henrik Zetterberg Henrik Zetterberg Kaj Blennow Kaj Blennow Vesna Jelic Vesna Jelic |
| author_sort | Una Smailovic |
| collection | DOAJ |
| description | BackgroundMild 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.MethodsWe 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.ResultsPatients 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.ConclusionPatients 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. |
| first_indexed | 2024-12-13T22:12:44Z |
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| last_indexed | 2024-12-13T22:12:44Z |
| publishDate | 2022-04-01 |
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| series | Frontiers in Aging Neuroscience |
| spelling | doaj.art-2297a8216d30472e99dce2204f97d30f2022-12-21T23:29:40ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652022-04-011410.3389/fnagi.2022.755454755454Decreased Electroencephalography Global Field Synchronization in Slow-Frequency Bands Characterizes Synaptic Dysfunction in Amnestic Subtypes of Mild Cognitive ImpairmentUna Smailovic0Una Smailovic1Daniel Ferreira2Daniel Ferreira3Birgitta Ausén4Birgitta Ausén5Birgitta Ausén6Nicholas James Ashton7Nicholas James Ashton8Nicholas James Ashton9Nicholas James Ashton10Nicholas James Ashton11Thomas Koenig12Henrik Zetterberg13Henrik Zetterberg14Henrik Zetterberg15Henrik Zetterberg16Henrik Zetterberg17Kaj Blennow18Kaj Blennow19Vesna Jelic20Vesna Jelic21Division of Clinical Geriatrics, Center for Alzheimer Research, Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Huddinge, SwedenDepartment of Clinical Neurophysiology, Karolinska University Hospital, Stockholm, SwedenDivision of Clinical Geriatrics, Center for Alzheimer Research, Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Huddinge, SwedenDepartment of Radiology, Mayo Clinic, Rochester, MN, United StatesDivision of Clinical Geriatrics, Center for Alzheimer Research, Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Huddinge, SwedenClinic for Cognitive Disorders, Karolinska University Hospital-Huddinge, Stockholm, SwedenWomen’s Health and Allied Health Professionals Theme, Medical Unit Medical Psychology, Karolinska University Hospital, Huddinge, SwedenDepartment of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, The Sahlgrenska Academy at the University of Gothenburg, Mölndal, SwedenClinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, SwedenWallenberg Centre for Molecular and Translational Medicine, University of Gothenburg, Gothenburg, SwedenKing’s College London, Institute of Psychiatry, Psychology and Neuroscience, Maurice Wohl Institute Clinical Neuroscience Institute, London, United Kingdom0NIHR Biomedical Research Centre for Mental Health and Biomedical Research Unit for Dementia at South London and Maudsley NHS Foundation, London, United Kingdom1Psychiatric Electrophysiology Unit, Translational Research Center, University Hospital of Psychiatry, Bern, SwitzerlandDepartment of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, The Sahlgrenska Academy at the University of Gothenburg, Mölndal, SwedenClinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden2Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, Queen Square, London, United Kingdom3UK Dementia Research Institute at UCL, London, United Kingdom4Hong Kong Center for Neurodegenerative Diseases, Hong Kong, Hong Kong SAR, ChinaDepartment of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, The Sahlgrenska Academy at the University of Gothenburg, Mölndal, SwedenClinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, SwedenDivision of Clinical Geriatrics, Center for Alzheimer Research, Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Huddinge, SwedenClinic for Cognitive Disorders, Karolinska University Hospital-Huddinge, Stockholm, SwedenBackgroundMild 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.MethodsWe 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.ResultsPatients 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.ConclusionPatients 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.https://www.frontiersin.org/articles/10.3389/fnagi.2022.755454/fullelectroencephalographysynaptic dysfunctionamnestic mild cognitive impairment (aMCI)Alzheimer’s diseaseEEG powerglobal field synchronization (GFS) |
| spellingShingle | Una Smailovic Una Smailovic Daniel Ferreira Daniel Ferreira Birgitta Ausén Birgitta Ausén Birgitta Ausén Nicholas James Ashton Nicholas James Ashton Nicholas James Ashton Nicholas James Ashton Nicholas James Ashton Thomas Koenig Henrik Zetterberg Henrik Zetterberg Henrik Zetterberg Henrik Zetterberg Henrik Zetterberg Kaj Blennow Kaj Blennow Vesna Jelic Vesna Jelic Decreased Electroencephalography Global Field Synchronization in Slow-Frequency Bands Characterizes Synaptic Dysfunction in Amnestic Subtypes of Mild Cognitive Impairment Frontiers in Aging Neuroscience electroencephalography synaptic dysfunction amnestic mild cognitive impairment (aMCI) Alzheimer’s disease EEG power global field synchronization (GFS) |
| title | Decreased Electroencephalography Global Field Synchronization in Slow-Frequency Bands Characterizes Synaptic Dysfunction in Amnestic Subtypes of Mild Cognitive Impairment |
| title_full | Decreased Electroencephalography Global Field Synchronization in Slow-Frequency Bands Characterizes Synaptic Dysfunction in Amnestic Subtypes of Mild Cognitive Impairment |
| title_fullStr | Decreased Electroencephalography Global Field Synchronization in Slow-Frequency Bands Characterizes Synaptic Dysfunction in Amnestic Subtypes of Mild Cognitive Impairment |
| title_full_unstemmed | Decreased Electroencephalography Global Field Synchronization in Slow-Frequency Bands Characterizes Synaptic Dysfunction in Amnestic Subtypes of Mild Cognitive Impairment |
| title_short | Decreased Electroencephalography Global Field Synchronization in Slow-Frequency Bands Characterizes Synaptic Dysfunction in Amnestic Subtypes of Mild Cognitive Impairment |
| title_sort | decreased electroencephalography global field synchronization in slow frequency bands characterizes synaptic dysfunction in amnestic subtypes of mild cognitive impairment |
| topic | electroencephalography synaptic dysfunction amnestic mild cognitive impairment (aMCI) Alzheimer’s disease EEG power global field synchronization (GFS) |
| url | https://www.frontiersin.org/articles/10.3389/fnagi.2022.755454/full |
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