Spontaneous sensorimotor beta power and cortical thickness uniquely predict motor function in healthy aging

Background: Spontaneous beta activity in the primary motor cortices has been shown to increase in amplitude with advancing age, and that such increases are tightly coupled to stronger motor-related beta oscillations during movement planning. However, the relationship between these age-related change...

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Main Authors: Maggie P. Rempe, Brandon J. Lew, Christine M. Embury, Nicholas J. Christopher-Hayes, Mikki Schantell, Tony W. Wilson
Format: Article
Language:English
Published: Elsevier 2022-11-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811922007662
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author Maggie P. Rempe
Brandon J. Lew
Christine M. Embury
Nicholas J. Christopher-Hayes
Mikki Schantell
Tony W. Wilson
author_facet Maggie P. Rempe
Brandon J. Lew
Christine M. Embury
Nicholas J. Christopher-Hayes
Mikki Schantell
Tony W. Wilson
author_sort Maggie P. Rempe
collection DOAJ
description Background: Spontaneous beta activity in the primary motor cortices has been shown to increase in amplitude with advancing age, and that such increases are tightly coupled to stronger motor-related beta oscillations during movement planning. However, the relationship between these age-related changes in spontaneous beta in the motor cortices, local cortical thickness, and overall motor function remains unclear. Methods: We collected resting-state magnetoencephalography (MEG), high-resolution structural MRI, and motor function scores using a neuropsychological battery from 126 healthy adults (56 female; age range = 22–72 years). MEG data were source-imaged and a whole-brain vertex-wise regression model was used to assess age-related differences in spontaneous beta power across the cortex. Cortical thickness was computed from the structural MRI data and local beta power and cortical thickness values were extracted from the sensorimotor cortices. To determine the unique contribution of age, spontaneous beta power, and cortical thickness to the prediction of motor function, a hierarchical regression approach was used. Results: There was an increase in spontaneous beta power with age across the cortex, with the strongest increase being centered on the sensorimotor cortices. Sensorimotor cortical thickness was not related to spontaneous beta power, above and beyond age. Interestingly, both cortical thickness and spontaneous beta power in sensorimotor regions each uniquely contributed to the prediction of motor function when controlling for age. Discussion: This multimodal study showed that cortical thickness and spontaneous beta activity in the sensorimotor cortices have dissociable contributions to motor function across the adult lifespan. These findings highlight the complexity of interactions between structure and function and the importance of understanding these interactions in order to advance our understanding of healthy aging and disease.
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spelling doaj.art-ca6af3bc6c5b47d985ca4d809c99923e2022-12-22T02:42:51ZengElsevierNeuroImage1095-95722022-11-01263119651Spontaneous sensorimotor beta power and cortical thickness uniquely predict motor function in healthy agingMaggie P. Rempe0Brandon J. Lew1Christine M. Embury2Nicholas J. Christopher-Hayes3Mikki Schantell4Tony W. Wilson5Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Psychology, University of Nebraska - Omaha (UNO), Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Center for Mind and Brain, University of California - Davis, Davis, CA, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USA; Corresponding author at: Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USABackground: Spontaneous beta activity in the primary motor cortices has been shown to increase in amplitude with advancing age, and that such increases are tightly coupled to stronger motor-related beta oscillations during movement planning. However, the relationship between these age-related changes in spontaneous beta in the motor cortices, local cortical thickness, and overall motor function remains unclear. Methods: We collected resting-state magnetoencephalography (MEG), high-resolution structural MRI, and motor function scores using a neuropsychological battery from 126 healthy adults (56 female; age range = 22–72 years). MEG data were source-imaged and a whole-brain vertex-wise regression model was used to assess age-related differences in spontaneous beta power across the cortex. Cortical thickness was computed from the structural MRI data and local beta power and cortical thickness values were extracted from the sensorimotor cortices. To determine the unique contribution of age, spontaneous beta power, and cortical thickness to the prediction of motor function, a hierarchical regression approach was used. Results: There was an increase in spontaneous beta power with age across the cortex, with the strongest increase being centered on the sensorimotor cortices. Sensorimotor cortical thickness was not related to spontaneous beta power, above and beyond age. Interestingly, both cortical thickness and spontaneous beta power in sensorimotor regions each uniquely contributed to the prediction of motor function when controlling for age. Discussion: This multimodal study showed that cortical thickness and spontaneous beta activity in the sensorimotor cortices have dissociable contributions to motor function across the adult lifespan. These findings highlight the complexity of interactions between structure and function and the importance of understanding these interactions in order to advance our understanding of healthy aging and disease.http://www.sciencedirect.com/science/article/pii/S1053811922007662MagnetoencephalographyMultimodalSensorimotorResting-stateOscillations
spellingShingle Maggie P. Rempe
Brandon J. Lew
Christine M. Embury
Nicholas J. Christopher-Hayes
Mikki Schantell
Tony W. Wilson
Spontaneous sensorimotor beta power and cortical thickness uniquely predict motor function in healthy aging
NeuroImage
Magnetoencephalography
Multimodal
Sensorimotor
Resting-state
Oscillations
title Spontaneous sensorimotor beta power and cortical thickness uniquely predict motor function in healthy aging
title_full Spontaneous sensorimotor beta power and cortical thickness uniquely predict motor function in healthy aging
title_fullStr Spontaneous sensorimotor beta power and cortical thickness uniquely predict motor function in healthy aging
title_full_unstemmed Spontaneous sensorimotor beta power and cortical thickness uniquely predict motor function in healthy aging
title_short Spontaneous sensorimotor beta power and cortical thickness uniquely predict motor function in healthy aging
title_sort spontaneous sensorimotor beta power and cortical thickness uniquely predict motor function in healthy aging
topic Magnetoencephalography
Multimodal
Sensorimotor
Resting-state
Oscillations
url http://www.sciencedirect.com/science/article/pii/S1053811922007662
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