Elsevier

Clinical Biomechanics

Volume 59, November 2018, Pages 94-100
Clinical Biomechanics

Age and falls history effects on antagonist leg muscle coactivation during walking with balance perturbations

https://doi.org/10.1016/j.clinbiomech.2018.09.011Get rights and content

Highlights

  • Antagonist muscle coactivation improves joint stability to preserve balance.

  • Quantified age and falls history on antagonist leg muscle coactivation during walking

  • Optical flow perturbations using virtual reality provoked lateral gait instability.

  • Antagonistic coactivation increased due to aging and falls history

  • Larger between-group differences in the presence of optical flow perturbations

Abstract

Background

Inspired by a reliance on visual feedback for movement control in older age, optical flow perturbations provide a unique opportunity to study the neuromuscular mechanisms involved in walking balance control, including aging and falls history effects on the response to environmental balance challenges. Specifically, antagonist leg muscle coactivation, which increases with age during walking, is considered a neuromuscular defense against age-associated deficits in balance control. The purpose of this study was to investigate the effects of age and falls history on antagonist leg muscle coactivation during walking with and without optical flow perturbations of different amplitudes.

Methods

Eleven young adults [mean (standard deviation) age: 24.8 (4.8) years], eleven older non-fallers [75.3 (5.4) years] and eleven older fallers [age: 78 (7.6) years] participated in this study. Participants completed 2-minute walking trials while watching a speed-matched virtual hallway that, in some conditions, included mediolateral optical flow perturbations designed to elicit the visual perception of imbalance.

Findings

We first found that lower leg antagonist muscle coactivation during normal walking increased with age, independent of falls history. We also found that older but not young adults increased antagonist leg muscle coactivation in the presence of optical flow perturbations, with more pervasive effects in older adults with a history of falls.

Interpretation

Our findings allude to a greater susceptibility to optical flow perturbations in older fallers during walking, which points to a higher potential for risk of instability in more complex and dynamic everyday environments. These findings may also have broader impacts related to the design of innovative training paradigms and neuromuscular targets for falls prevention.

Introduction

Roughly a third of people over the age of 65 fall at least once annually and 25–30% of these falls lead to moderate to severe injury (Alexander et al., 1992). The consequences may be functionally devastating for the individual and yield an enormous financial burden on the health care system. Unfortunately, evidence even suggests that the rate of injurious falls is accelerating, with 2.4 million fall-related emergency department visits in 2011, up 46% from 2001 despite only a 17% increase in the older adult population (Centers for Disease Control and Prevention and National Center for Injury Prevention and Control, 2017). Indeed, while numerous studies and clinical trials have attempted to decrease the prevalence and severity of falls, fall rates have been resistant to change (Gardner et al., 2000; Kraemer et al., 2009; Rubenstein et al., 2000). The physiological mechanisms underlying age-related falls risk are likely multifactorial, but may include declines in somatosensory acuity and a decreased neuromuscular capacity to respond to unexpected balance challenges. Accordingly, balance perturbations have become highly prevalent in studying the fidelity of walking balance control in older adults due to their capacity to elicit age-associated differences that are not otherwise apparent during normal, unperturbed walking (Franz et al., 2015; Martelli et al., 2017).

As a potential neuromuscular defense mechanism for deficits in balance control, the concurrent activation of antagonist muscles during walking (i.e., antagonist coactivation), increases in old age (Hortobagyi et al., 2009; Hortobagyi et al., 2011; Hortobagyi and DeVita, 2000; Mian et al., 2006; Ortega and Farley, 2015; Peterson and Martin, 2010). This age-related increase in antagonist coactivation is thought to bolster leg joint stiffness and thereby improve joint stability as a means to mitigate or improve the response to balance disturbances (Finley et al., 2012; Hortobagyi and DeVita, 2000). Indeed, evidence from arm reaching tasks shows that antagonist coactivation and limb stiffness concurrently increase with the magnitude of external force perturbations (Wong et al., 2009). Moreover, another study found a significant positive correlation (i.e., r = 0.42) between antagonist coactivation and the quality of standing postural control among older adults (Nagai et al., 2011). However, although intuitive and consistent with the prevailing mechanistic interpretation, it remains unclear whether the coactivation of antagonistic leg muscles in older adults increases further in the presence of walking balance perturbations. This may be particularly prevalent in older adults with a history of falls; compared to non-fallers, older fallers exhibit disproportionate decrements in metrics of walking balance control (Cebolla et al., 2015; Svoboda et al., 2017).

Due to their ability to elicit corrective motor responses, optical flow perturbations (i.e., eliciting the visual perception of imbalance) have increasingly been used to study balance control during walking (Franz et al., 2015; Jeka et al., 2010; O'Connor and Kuo, 2009; McAndrew et al., 2011). Moreover, this class of perturbations is uniquely well-suited to study the neuromuscular control of walking balance in older age; compared to young adults, older adults rely more on visual feedback for motor planning and execution (Franz et al., 2015; Jeka et al., 2010) – an effect that becomes even more pronounced in older adults with a history of falls (Lord and Webster, 1990). Accordingly, optical flow perturbations applied during walking can elicit age-related differences in many metrics of walking balance control that are not otherwise apparent during unperturbed walking, including increased gait variability and decreased local dynamic stability (Francis et al., 2015; Franz et al., 2015). More recently, we incorporated electromyographic (EMG) recordings of leg muscle activities to show that young adults walking with similar perturbations do show evidence of elevated antagonist coactivation compared to normal, unperturbed walking – particularly during limb loading in early stance (Stokes et al., 2017). However, despite longstanding scientific and clinical interest, our understanding of age and falls history effects on the neuromuscular mechanisms involved in walking balance control and the response to optical flow perturbations remains fundamentally incomplete.

Therefore, the purpose of this study was to investigate the effects of age and falls history on antagonist leg muscle coactivation during walking with and without optical flow perturbations of different amplitudes. We used a virtual reality environment to apply continuous mediolateral optical flow perturbations during treadmill walking while recording EMG activities of antagonist upper and lower leg muscle pairs. We hypothesized that: (1) compared to young adults, aging and falls history would increase antagonist muscle coactivation during walking, and (2) these between-group differences would increase in the presence of optical flow perturbations.

Section snippets

Participants

Eleven healthy young adults [6 female, mean (standard deviation, SD), age: 24.8(4.8) years, height: 1.72(0.01) m, mass: 67.2(8.8) kg], eleven healthy older adults [6 female, age: 75.3(5.4) years, height: 1.75(0.01) m, mass: 73.4(16.1) kg] and eleven older adults with a history of falls [7 female, age: 78(7.6) years, height: 1.6(0.12) m, mass: 69.3(14.0) kg] participated in this study. Older adults were considered to be fallers if they had fallen one or more times in the past year. For this

Age and perturbation effects on step kinematics

Table 1 summarizes optical flow perturbation effects on step kinematics as a function of group to provide context for the primary EMG-based outcomes. Group main effects revealed that older fallers averaged shorter and more variable step widths and step lengths than young adults (Table 1). Compared to unperturbed walking, perturbations elicited larger step length and width variabilities and wider steps in all groups, and shorter steps in older but not young adults.

Group effects on antagonist coactivation

The two-way ANOVA revealed

Discussion

We investigated differences in step kinematics and antagonist leg muscle coactivation during walking between healthy young adults, older adult non-fallers, and older adults with a history of falls and changes thereof when responding to optical flow perturbations of different amplitudes. We first hypothesized that aging and falls history would increase antagonist leg muscle coactivation during walking. In partial support of this hypothesis, lower leg muscle coactivation during the stance phase

Conclusion

This study provides insight into aging and falls history effects on the neural control strategies used to maintain walking balance and respond to optical flow perturbations. Our findings suggest that older adults, particularly those with a falls history, may rely more on increased leg joint stiffness than young adults to accommodate balance challenges during walking. Moreover, elevated antagonist upper leg muscle coactivation at larger perturbation amplitudes, unique to older adults with a

Acknowledgements

We gratefully acknowledge Ms. Heather Stokes and Dr. Jody Feld for their help with data collection. This study was supported in part by the North Carolina State University Abrams scholarship program and by grants from the National Center for Advancing Translational Sciences (UL1TR001111), UNC/NC State CLEAR core, and the National Institutes of Health (R56AG054797).

Conflict of interest

The authors have no conflicts of interest.

References (34)

  • D.S. Peterson et al.

    Effects of age and walking speed on coactivation and cost of walking in healthy adults

    Gait Posture

    (2010)
  • M. Qiao et al.

    Aging effects on leg joint variability during walking with balance perturbations

    Gait Posture

    (2018)
  • J.A. Zeni et al.

    Two simple methods for determining gait events during treadmill and overground walking using kinematic data

    Gait Posture

    (2008)
  • B.H. Alexander et al.

    The cost and frequency of hospitalization for fall-related injuries in older adults

    Am. J. Public Health

    (1992)
  • E.C. Cebolla et al.

    Balance, gait, functionality and strength: comparison between elderly fallers and non-fallers

    Braz. J. Phys. Ther.

    (2015)
  • Centers for Disease Control and Prevention et al.

    Web-based injury statistics query and reporting system (WISQARS)

    (2017)
  • J.R. Cram et al.

    Introduction to Surface Electromyography

    (1998)
  • Cited by (22)

    • The metabolic cost of walking balance control and adaptation in young adults

      2022, Gait and Posture
      Citation Excerpt :

      Perturbation-induced changes in step kinematics reported here are fully consistent with those reported in earlier studies. The onset of perturbations led to the shorter, wider, and more variable steps we have considered hallmark in our earlier interpretation of a generalized anticipatory control strategy in response to balance challenges. [3,5] We add here that this strategy appears to exact a metabolic penalty, most likely due to the instinctive prioritization of lateral stability in the presence of perturbations.

    • Coactivation pattern in leg muscles during treadmill walking in patients suffering from intermittent claudication

      2021, Gait and Posture
      Citation Excerpt :

      Schieber et al. observed that the second peak of vertical ground reaction force is decreased after supervised walking exercise therapy in PAD-IC patients, unlike other parameters such as power generation at the ankle and hip [32]. In addition, an altered coactivation is known to induce walking balance disorders [33]. In our study, we found that a decrease of the second peak of vertical ground reaction force is related to an increased coactivation.

    • Keep your head down: Maintaining gait stability in challenging conditions

      2020, Human Movement Science
      Citation Excerpt :

      Unfortunately, some of these cautious behavioural changes that are intended to reduce fall risk may be dangerous in that they can lead to increased fall risk. For example, increased leg muscle coactivation (simultaneous contraction of an agonist and antagonist muscle) helps to stabilise the leg when walking (Thompson, Plummer, & Franz, 2018). However, a stiff leg is less flexible and therefore has a reduced range of motion which, in itself, is a known risk factor for falls (Chiacchiero, Dresely, Silva, DeLosReyes, & Vorik, 2010; Reddy & Alahmari, 2016).

    View all citing articles on Scopus
    View full text