Abstract

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.

Highlights

  • Aging is associated with deterioration in maximum force production independent of muscle size (Ojanen et al, 2007), worse rapid force production (Skelton et al, 1994), decreased low-force contraction steadiness (Galganski et al, 1993), and poorer dynamic balance control during perturbations (Piirainen et al, 2013)

  • The present study investigated the age-related differences in sensorimotor cortex oscillations in the 15–30 Hz beta band at rest and following rapid involuntary stretches to the triceps surae muscles in adults

  • Baseline beta power was stronger in older compared to young adults

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Summary

Introduction

Aging is associated with deterioration in maximum force production independent of muscle size (Ojanen et al, 2007), worse rapid force production (Skelton et al, 1994), decreased low-force contraction steadiness (Galganski et al, 1993), and poorer dynamic balance control during perturbations (Piirainen et al, 2013). Proprioception is not solely a peripheral phenomenon, and recently we have observed impaired proprioceptive processing within the primary sensorimotor cortex (SM1; Piitulainen et al, 2018) These age-related maladaptations suggest altered neuronal motor control, but the exact causes of the modified neuronal control in various conditions (e.g., during perturbed balance control) remain elusive. Based on transcranial magnetic stimulation findings, it has been suggested that altered cortical control modifies (spinal-level) reflexes during upright standing, in older adults (Baudry et al, 2015), which may lead to greater cortical influence during standing balance in older adults (Baudry, 2016) This may reflect compensation to overall age-related impairment of the sensorimotor system both at cortical and spinal levels that may lead to greater demand on cortical influence during motor actions. Our findings of altered cortical proprioceptive processing was related to standing balance performance (Piitulainen et al, 2018)

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