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Age-Related Differences in Muscle Synergy Organization During Step

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Age-Related Differences in Muscle Synergy Organization During Step applied sciences Article Age-Related Differences in Muscle Synergy Organization during Step Ascent at Different Heights and Directions Remco J. Baggen 1,2 , Jaap H. van Dieën 2 , Evelien Van Roie 1 , Sabine M. Verschueren 3, Georgios Giarmatzis 4, Christophe Delecluse 1 and Nadia Dominici 2,* 1 Department of Movement Sciences, Physical Activity, Sports and Health Research Group, KU Leuven, 3001 Leuven, Belgium 2 Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, Institute for Brain and Behavior Amsterdam & Amsterdam Movement Sciences, 1081 BT Amsterdam, The Netherlands 3 Department of Rehabilitation Sciences, Research Group for Musculoskeletal Rehabilitation, KU Leuven, 3001 Leuven, Belgium 4 Department of Electrical and Computer Engineering, Visualization & Virtual Reality Group, University of Patras, 26504 Rio Achaia, Greece * Correspondence: [email protected]; Tel.: +31-20-59-88-591 Received: 30 January 2020; Accepted: 5 March 2020; Published: 14 March 2020 Abstract: The aim of this study was to explore the underlying age-related differences in dynamic motor control during different step ascent conditions using muscle synergy analysis. Eleven older women (67.0 y 2.5) and ten young women (22.5 y 1.6) performed stepping in forward and lateral directions ± ± at step heights of 10, 20 and 30 cm. Surface electromyography was obtained from 10 lower limb and torso muscles. Non-negative matrix factorization was used to identify sets of (n) synergies across age groups and stepping conditions. In addition, variance accounted for (VAF) by the detected number of synergies was compared to assess complexity of motor control. Finally, correlation coefficients of muscle weightings and between-subject variability of the temporal activation patterns were calculated and compared between age groups and stepping conditions. Four synergies accounted for >85% VAF across age groups and stepping conditions. Age and step height showed a significant negative correlation with VAF during forward stepping but not lateral stepping, with lower VAF indicating higher synergy complexity. Muscle weightings showed higher similarity across step heights in older compared to young women. Neuromuscular control of young and community-dwelling older women could not be differentiated based on the number of synergies extracted. Additional analyses of synergy structure and complexity revealed subtle age- and step-height-related differences, indicating that older women rely on more complex neuromuscular control strategies. Keywords: EMG; muscle synergies; forward stepping; lateral stepping; aging; neural control 1. Introduction Aging is associated with gradual changes in neuromuscular control [1,2]. Eventually, these changes can have a major impact on fall risk, mobility and independence in older adults [3–5], which may be exacerbated in post-menopausal women due to accelerated muscle wasting [5]. One major challenge with assessing changes in neuromuscular control in healthy community-dwelling older adults is that, due to the gradual nature of age-related neuromuscular deterioration, pre-clinical changes in neuromuscular control of everyday tasks may go undetected [6]. In healthy older adults, changes in Appl. Sci. 2020, 10, 1987; doi:10.3390/app10061987 www.mdpi.com/journal/applsci Appl. Sci. 2020, 10, 1987 2 of 15 neuromuscular control can be revealed by increasing task challenge. For example, by increasing gait speed, cadence, step length, and step height [7–9]. Step ascent, a functional task in daily life, provides a challenge that can easily be modified by increasing step height and has been demonstrated to be an effective training stimulus to improve muscle volume and functional ability in older women [10,11]. However, the effects of aging and task challenge on the neuromuscular control strategies behind step ascent have not yet been thoroughly explored. In a previous study conducted with older women, we found that peak activation of several major lower limb muscles occurred during the ascent phase of stepping and that there is a positive dose-response relationship between step height and peak muscle activation [10]. However, the increase in step height was also accompanied by increased between-subject variance of peak activation magnitudes [10]. This could be attributable to a tendency of older adults to modulate their motor strategies (e.g., shifting joint moment generation from the knee to the ankle), in order to operate within the limits of their physical capacity when ascending steps [12,13]. Additionally, it is unknown if other observed age-related changes in neuromuscular control strategies, such as increased antagonistic co-contraction of quadriceps and hamstrings to help maintain postural control during dynamic tasks [14–17], may interact with increased task challenge. One way to assess neuromuscular control is through muscle synergy analysis. Previous studies have found that low-dimensional sets of motor modules, also known as muscle synergies, can be used to reconstruct muscle activation patterns during various motor tasks [18–22]. These synergies are composed of groups of muscles that are assumed to be activated by a single neural command [23]. It is thought that the central nervous system employs this modular organization to reduce the large number of degrees of freedom inherent to the redundancy of the human musculoskeletal system [24], and to allow for flexible but accurate response selection during motor tasks [25]. However, some researchers have argued that modular recruitment of muscles might represent predetermined control strategies and could merely be an effect of task constraints or optimized performance criteria, rather than reflecting neural control strategies employed by the central nervous system [23,26]. Regardless of the mechanisms underlying modular organization of muscle activation, extracting muscle synergies from electromyographic (EMG) signals can provide important insights about neuromuscular control strategies used to perform functional tasks [27]. In older adults with a history of falls, declines in neuromuscular control are reflected in a decreased number of extracted synergies from walking tasks that challenge dynamic balance [6]. A decreased number of synergies is indicative of decreased complexity of motor control or a decreased motor repertoire. These underlying changes in synergy complexity can be quantified using variance account for (VAF) by a given set of extracted synergies and defining the number of synergies required to adequately reconstruct the original EMG signals (indicated by a-priori or a-posteriori set thresholds for VAF) [28]. For example, high VAF by a limited number of synergies represents decreased complexity of motor control, which is often associated with neuromuscular pathologies such as cerebral palsy and stroke [6,27,29] and characterized by increased levels of co-activation between individual muscles [30]. However, healthy aging is associated with a more gradual process of physical decline and thus changes in complexity of motor control may not manifest in a decreased number of synergies [8]. Consequently, age-related changes in motor control may be better reflected by comparisons of VAF for a fixed number of synergies [29,31,32] or by assessing changes in spatio-temporal organization of muscle synergies, such as altered module composition and shifts in activation patterns [2,6]. Differences in spatio-temporal organization within a stable number of synergies can arguably be considered more subtle than differences in the total number of synergies as they tend to reflect compensatory or alternative motor strategies in order to overcome increased or altered task challenges, whereas a decreased number of synergies is usually used as an indication of neural impairments. Although it is currently unknown how aging and task intensity affect muscle synergy organization during stair ascent, analyses of underlying differences could provide a basis to improve detection of pre-clinical age-related deterioration in neuromuscular control and more effectively target fall prevention programs at individuals most at risk. Appl. Sci. 2020, 10, 1987 3 of 15 Therefore, the purpose of this study was to explore muscle synergy recruitment during step ascent in forward and lateral directions and with incremental step heights in young and older adults. Specifically, we aimed to assess the effects of age-related changes, task intensity, and their interaction on complexity and organization of motor control by comparing the number of extracted synergies, variance accounted for (VAF) by a fixed number of synergies, and spatio-temporal characteristics of the extracted synergies across conditions. 2. Materials and Methods 2.1. Participants Eleven older women (67.0 y 2.5, 161.3 cm 4.9, 64.4 kg 6.8) and ten young women (22.5 y 1.6, ± ± ± ± 168.9 cm 1.7, 64.2 kg 7.9) were recruited for this study. Potential participants were excluded if they ± ± suffered from neurological or motor disorders, impaired balance control, or if they had been involved in a structured training program in the last 6 months prior to participation in the study. This study was approved by the Human Ethics Committee of KU Leuven in accordance with the Declaration of Helsinki and registered with the Clinical Trial Center UZ Leuven (S56405). All participants signed informed consent prior to participation in the study. 2.2. Experimental Protocol Participants performed a series of stepping tasks consisting of stepping onto
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