Older Age Increases the Amplitude of Muscle Stretch-Induced Cortical Beta-Band Suppression But Does not Affect Rebound Strength

Healthy aging is associated with deterioration of the sensorimotor system, which impairs balance and somatosensation. However, the exact age-related changes in the cortical processing of sensorimotor integration are unclear. This study investigated primary sensorimotor cortex (SM1) oscillations in t...

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Main Authors: Simon Walker, Simo Monto, Jarmo M. Piirainen, Janne Avela, Ina M. Tarkka, Tiina M. Parviainen, Harri Piitulainen
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Aging Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnagi.2020.00117/full
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author Simon Walker
Simo Monto
Jarmo M. Piirainen
Janne Avela
Ina M. Tarkka
Tiina M. Parviainen
Harri Piitulainen
Harri Piitulainen
author_facet Simon Walker
Simo Monto
Jarmo M. Piirainen
Janne Avela
Ina M. Tarkka
Tiina M. Parviainen
Harri Piitulainen
Harri Piitulainen
author_sort Simon Walker
collection DOAJ
description Healthy aging is associated with deterioration of the sensorimotor system, which impairs balance and somatosensation. However, the exact age-related changes in the cortical processing of sensorimotor integration are unclear. This study investigated primary sensorimotor cortex (SM1) oscillations in the 15–30 Hz beta band at rest and following (involuntary) rapid stretches to the triceps surae muscles (i.e., proprioceptive stimulation) of young and older adults. A custom-built, magnetoencephalography (MEG)-compatible device was used to deliver rapid (190°·s−1) ankle rotations as subjects sat passively in a magnetically-shielded room while MEG recorded their cortical signals. Eleven young (age 25 ± 3 years) and 12 older (age 70 ± 3 years) adults matched for physical activity level demonstrated clear 15–30 Hz beta band suppression and rebound in response to the stretches. A sub-sample (10 young and nine older) were tested for dynamic balance control on a sliding platform. Older adults had greater cortical beta power pre-stretch (e.g., right leg: 4.0 ± 1.6 fT vs. 5.6 ± 1.7 fT, P = 0.044) and, subsequently, greater normalized movement-related cortical beta suppression post-proprioceptive stimulation (e.g., right leg: −5.8 ± 1.3 vs. −7.6 ± 1.7, P = 0.01) than young adults. Furthermore, poorer balance was associated with stronger cortical beta suppression following proprioceptive stimulation (r = −0.478, P = 0.038, n = 19). These results provide further support that cortical processing of proprioception is hindered in older adults, potentially (adversely) influencing sensorimotor integration. This was demonstrated by the impairment of prompt motor action control, i.e., regaining perturbed balance. Finally, SM1 cortex beta suppression to a proprioceptive stimulus seems to indicate poorer sensorimotor functioning in older adults.
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spelling doaj.art-6b0ca862d5684e1d8cdcc56a47f936c62022-12-22T00:08:07ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652020-05-011210.3389/fnagi.2020.00117521967Older Age Increases the Amplitude of Muscle Stretch-Induced Cortical Beta-Band Suppression But Does not Affect Rebound StrengthSimon Walker0Simo Monto1Jarmo M. Piirainen2Janne Avela3Ina M. Tarkka4Tiina M. Parviainen5Harri Piitulainen6Harri Piitulainen7NeuroMuscular Research Center, Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, FinlandDepartment of Psychology, Centre for Interdisciplinary Brain Research, University of Jyväskylä, Jyväskylä, FinlandNeuroMuscular Research Center, Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, FinlandNeuroMuscular Research Center, Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, FinlandFaculty of Sport and Health Sciences and Centre for Interdisciplinary Brain Research, University of Jyväskylä, Jyväskylä, FinlandDepartment of Psychology, Centre for Interdisciplinary Brain Research, University of Jyväskylä, Jyväskylä, FinlandNeuroMuscular Research Center, Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, FinlandDepartment of Neuroscience and Biomedical Engineering, Aalto University School of Science, Espoo, FinlandHealthy aging is associated with deterioration of the sensorimotor system, which impairs balance and somatosensation. However, the exact age-related changes in the cortical processing of sensorimotor integration are unclear. This study investigated primary sensorimotor cortex (SM1) oscillations in the 15–30 Hz beta band at rest and following (involuntary) rapid stretches to the triceps surae muscles (i.e., proprioceptive stimulation) of young and older adults. A custom-built, magnetoencephalography (MEG)-compatible device was used to deliver rapid (190°·s−1) ankle rotations as subjects sat passively in a magnetically-shielded room while MEG recorded their cortical signals. Eleven young (age 25 ± 3 years) and 12 older (age 70 ± 3 years) adults matched for physical activity level demonstrated clear 15–30 Hz beta band suppression and rebound in response to the stretches. A sub-sample (10 young and nine older) were tested for dynamic balance control on a sliding platform. Older adults had greater cortical beta power pre-stretch (e.g., right leg: 4.0 ± 1.6 fT vs. 5.6 ± 1.7 fT, P = 0.044) and, subsequently, greater normalized movement-related cortical beta suppression post-proprioceptive stimulation (e.g., right leg: −5.8 ± 1.3 vs. −7.6 ± 1.7, P = 0.01) than young adults. Furthermore, poorer balance was associated with stronger cortical beta suppression following proprioceptive stimulation (r = −0.478, P = 0.038, n = 19). These results provide further support that cortical processing of proprioception is hindered in older adults, potentially (adversely) influencing sensorimotor integration. This was demonstrated by the impairment of prompt motor action control, i.e., regaining perturbed balance. Finally, SM1 cortex beta suppression to a proprioceptive stimulus seems to indicate poorer sensorimotor functioning in older adults.https://www.frontiersin.org/article/10.3389/fnagi.2020.00117/fullevent-related desynchronization (ERD)sensorimotorlower limbsproprioceptionsomatosensory processingMEG
spellingShingle Simon Walker
Simo Monto
Jarmo M. Piirainen
Janne Avela
Ina M. Tarkka
Tiina M. Parviainen
Harri Piitulainen
Harri Piitulainen
Older Age Increases the Amplitude of Muscle Stretch-Induced Cortical Beta-Band Suppression But Does not Affect Rebound Strength
Frontiers in Aging Neuroscience
event-related desynchronization (ERD)
sensorimotor
lower limbs
proprioception
somatosensory processing
MEG
title Older Age Increases the Amplitude of Muscle Stretch-Induced Cortical Beta-Band Suppression But Does not Affect Rebound Strength
title_full Older Age Increases the Amplitude of Muscle Stretch-Induced Cortical Beta-Band Suppression But Does not Affect Rebound Strength
title_fullStr Older Age Increases the Amplitude of Muscle Stretch-Induced Cortical Beta-Band Suppression But Does not Affect Rebound Strength
title_full_unstemmed Older Age Increases the Amplitude of Muscle Stretch-Induced Cortical Beta-Band Suppression But Does not Affect Rebound Strength
title_short Older Age Increases the Amplitude of Muscle Stretch-Induced Cortical Beta-Band Suppression But Does not Affect Rebound Strength
title_sort older age increases the amplitude of muscle stretch induced cortical beta band suppression but does not affect rebound strength
topic event-related desynchronization (ERD)
sensorimotor
lower limbs
proprioception
somatosensory processing
MEG
url https://www.frontiersin.org/article/10.3389/fnagi.2020.00117/full
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