Visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer’s disease spectrum

Abstract Background Entrainment of neural oscillations in occipital cortices by external rhythmic visual stimuli has been proposed as a novel therapy for patients with Alzheimer’s disease (AD). Despite this increased interest in visual neural oscillations in AD, little is known regarding their role...

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Main Authors: Alex I. Wiesman, Daniel L. Murman, Pamela E. May, Mikki Schantell, Sara L. Wolfson, Craig M. Johnson, Tony W. Wilson
Format: Article
Language:English
Published: BMC 2021-08-01
Series:Alzheimer’s Research & Therapy
Subjects:
Online Access:https://doi.org/10.1186/s13195-021-00881-w
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author Alex I. Wiesman
Daniel L. Murman
Pamela E. May
Mikki Schantell
Sara L. Wolfson
Craig M. Johnson
Tony W. Wilson
author_facet Alex I. Wiesman
Daniel L. Murman
Pamela E. May
Mikki Schantell
Sara L. Wolfson
Craig M. Johnson
Tony W. Wilson
author_sort Alex I. Wiesman
collection DOAJ
description Abstract Background Entrainment of neural oscillations in occipital cortices by external rhythmic visual stimuli has been proposed as a novel therapy for patients with Alzheimer’s disease (AD). Despite this increased interest in visual neural oscillations in AD, little is known regarding their role in AD-related cognitive impairment and in particular during visuospatial processing. Methods We used source-imaged magnetoencephalography (MEG) and an established visuospatial processing task to elicit multi-spectral neuronal responses in 35 biomarker-confirmed patients on the AD spectrum and 20 biomarker-negative older adults. Neuronal oscillatory responses were imaged to the level of the cortex, and group classifications and neurocognitive relationships were modeled using logistic and linear regression, respectively. Results Visuospatial neuronal oscillations in the theta, alpha, and gamma ranges significantly predicted the classification of patients on the AD spectrum. Importantly, the direction of these effects differed by response frequency, such that patients on the AD spectrum exhibited weaker alpha-frequency responses in lateral occipital regions, and stronger gamma-frequency responses in the primary visual cortex, as compared to biomarker-negative older adults. In addition, alpha and gamma, but not theta, oscillations robustly predicted cognitive status (i.e., MoCA and MMSE scores), such that patients with neural responses that deviated more from those of healthy older adults exhibited poorer cognitive performance. Conclusions We find that the multi-spectral neural dynamics supporting visuospatial processing differentiate patients on the AD spectrum from cognitively normal, biomarker-negative older adults. Oscillations in the alpha and gamma bands also relate to cognitive status in ways that are informative for emerging clinical interventions.
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spelling doaj.art-0cf67b2bee6248e5b94c5b57204a19402022-12-21T18:50:13ZengBMCAlzheimer’s Research & Therapy1758-91932021-08-0113111210.1186/s13195-021-00881-wVisuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer’s disease spectrumAlex I. Wiesman0Daniel L. Murman1Pamela E. May2Mikki Schantell3Sara L. Wolfson4Craig M. Johnson5Tony W. Wilson6Montreal Neurological Institute, McGill UniversityDepartment of Neurological Sciences, University of Nebraska Medical CenterDepartment of Neurological Sciences, University of Nebraska Medical CenterInstitute for Human Neuroscience, Boys Town National Research HospitalGeriatrics Medicine Clinic, UNMCDepartment of Radiology, UNMCInstitute for Human Neuroscience, Boys Town National Research HospitalAbstract Background Entrainment of neural oscillations in occipital cortices by external rhythmic visual stimuli has been proposed as a novel therapy for patients with Alzheimer’s disease (AD). Despite this increased interest in visual neural oscillations in AD, little is known regarding their role in AD-related cognitive impairment and in particular during visuospatial processing. Methods We used source-imaged magnetoencephalography (MEG) and an established visuospatial processing task to elicit multi-spectral neuronal responses in 35 biomarker-confirmed patients on the AD spectrum and 20 biomarker-negative older adults. Neuronal oscillatory responses were imaged to the level of the cortex, and group classifications and neurocognitive relationships were modeled using logistic and linear regression, respectively. Results Visuospatial neuronal oscillations in the theta, alpha, and gamma ranges significantly predicted the classification of patients on the AD spectrum. Importantly, the direction of these effects differed by response frequency, such that patients on the AD spectrum exhibited weaker alpha-frequency responses in lateral occipital regions, and stronger gamma-frequency responses in the primary visual cortex, as compared to biomarker-negative older adults. In addition, alpha and gamma, but not theta, oscillations robustly predicted cognitive status (i.e., MoCA and MMSE scores), such that patients with neural responses that deviated more from those of healthy older adults exhibited poorer cognitive performance. Conclusions We find that the multi-spectral neural dynamics supporting visuospatial processing differentiate patients on the AD spectrum from cognitively normal, biomarker-negative older adults. Oscillations in the alpha and gamma bands also relate to cognitive status in ways that are informative for emerging clinical interventions.https://doi.org/10.1186/s13195-021-00881-wNeural oscillationsVisuospatial processingMagnetoencephalographySource imagingAlzheimer’s disease
spellingShingle Alex I. Wiesman
Daniel L. Murman
Pamela E. May
Mikki Schantell
Sara L. Wolfson
Craig M. Johnson
Tony W. Wilson
Visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer’s disease spectrum
Alzheimer’s Research & Therapy
Neural oscillations
Visuospatial processing
Magnetoencephalography
Source imaging
Alzheimer’s disease
title Visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer’s disease spectrum
title_full Visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer’s disease spectrum
title_fullStr Visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer’s disease spectrum
title_full_unstemmed Visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer’s disease spectrum
title_short Visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer’s disease spectrum
title_sort visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the alzheimer s disease spectrum
topic Neural oscillations
Visuospatial processing
Magnetoencephalography
Source imaging
Alzheimer’s disease
url https://doi.org/10.1186/s13195-021-00881-w
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