Muscle synergies are similar when typically developing children walk on a treadmill at different speeds and slopes
Introduction
Recent research suggests that the central nervous system (CNS) uses a modular approach to controlling movement (Bizzi et al., 2002, Cheung et al., 2005, Tresch et al., 2006). These modules reduce the number of degrees of freedom the CNS needs to control by allowing groups of muscles to be recruited together as one unit. These groups of muscles are commonly referred to as synergies or modes. It has been shown that similar synergies are recruited during many different physical activities (e.g., walking, running, cycling, etc.) (Barroso et al., 2014, Hagio et al., 2015). However, it is still unclear whether these synergies are neurological in origin (i.e., the neurological pathways exist specifically to recruit muscles together) or mechanical in origin (i.e., mechanical constraints dictate certain patterns of muscle coordination) (Kutch et al., 2008, Kutch and Valero-Cuevas, 2012).
Individuals with neurological deficits, such as stroke or cerebral palsy, use fewer synergies in order to complete a movement task (Cheung et al., 2012, Clark et al., 2010, Li et al., 2013, Steele et al., 2015). If synergies truly have a neural origin, this could be an adaptation to the injury that further simplifies control. However, this simplification comes at a cost. The movement patterns of individuals with neurological deficits are significantly different from, and less efficient than, the movement patterns of intact individuals (Gage, 2004). If synergies are mechanical in origin, the reduction in the number of synergies could be explained by the fact that the simplified movement pattern favors a certain muscle activation pattern independent of neural control (Kutch and Valero-Cuevas, 2012). Understanding the etiology of synergies is important for interpreting the impact that altered synergies may have in cerebral palsy and other neurological disorders. These factors may help guide treatment decisions in these patient populations.
Synergies are identified from electromyography (EMG) data using algorithms such as non-negative matrix factorization. A small number of synergies can be used to describe the activity of a larger number of muscles. In one study of normal walking, only 6 synergies were required to describe over 90% of the variance in 38 muscles (Allen and Neptune, 2012). Synergies with similar structures have been found in several independent studies of walking (Bizzi et al., 2002, d’Avella and Bizzi, 2005, Gonzalez-Vargas et al., 2015, Ting and Macpherson, 2005). Furthermore, the same synergies can be used for several different activities. One recent study of adults found that synergies remained constant when the participants were asked to voluntarily change their stepping pattern on a treadmill (Routson et al., 2014). This would suggest that synergies do have a neural origin. However, other studies have explored the biomechanical constraints of the task performed in order to assess the range of possible control strategies. They found that some activities, like controlling the fingers, have only a small set of possible activation patterns, regardless of neurological input (Kutch et al., 2008). Clearly synergies cannot describe muscle activity across all possible tasks. Still, studying how individuals adapt their muscle activation patterns to variations in mechanical constraints can provide valuable insight into how movement is directed by the CNS.
The aim of this study was to investigate if synergies change when unimpaired individuals walk on a treadmill at different speeds and slopes. In this study, children with normal motor control walked at several different speeds and slopes on an instrumented treadmill to test their ability to actively adapt their muscle activations in response to the changing conditions on the treadmill (biomechanical task constraints). Changes in speed and slope have been shown to elicit significant changes in lower limb kinematics and kinetics (Lay et al., 2006, Schwartz et al., 2008). This requires adaptations of both the position of the joints, and the force produced by various muscle groups. In other words, changes in speed and slope change the mechanical constraints of gait. If there were no measureable changes in synergies, this would imply that there was an underlying tendency, independent of the biomechanical task constraints, for certain muscle groups to be activated together. Our hypothesis was that the significant changes in movement pattern associated with the slopes and speeds would not be accompanied by significant changes in synergies. By examining this question, we can gain insight into the neural and mechanical origins of synergies which may be important in the clinical recommendations and rehabilitation strategies for individuals with neurological deficits.
Section snippets
Methods
Sixteen typically developing children (10 male) were recruited for this study with an age range of 6–18 years old. There was a wide variety of experience with using a treadmill; with many of the younger participants having no prior treadmill experience.
Each participant completed a full over-ground gait analysis (Rozumalski et al., 2015). They were then asked to walk on an instrumented tandem belt treadmill (AMTI, Watertown, MA) starting at a speed matched to their self-selected over-ground
Synergies
The structure of the synergies at each stage was nearly identical (Fig. 3). The correlations of the synergies between the stages were higher than the group of random synergies (Fig. 4A) with an average correlation coefficient ranging from 0.71 to 0.96. The linear regression model showed that, within subjects, the correlations between stages were not significantly different from each other (P = 0.65). These correlations were also significantly higher than what would be expected from a random group
Discussion
The lack of differences in muscle synergies between stages indicates that the participants in this study consistently activated similar synergies, even as speed and slope were increased while walking on a treadmill. This was quantified with two separate methods: using walk-DMC to evaluate synergy complexity at each stage, and by calculating the correlation of synergy structure between stages. Despite the fact that synergies did not change, the participants’ kinematics and kinetics changed
Conclusions
In this study, typically developing children walked at several different speeds and slopes on a treadmill. The results show that their muscle synergies do not change in response to changing biomechanical task constraints. Those changes required adjustments to both joint position and muscle force generation. This supports our hypothesis that significant changes in movement pattern are not accompanied by significant changes in synergies. It remains to be seen if these insights into the
Conflicts of interest
The authors have no conflicts of interest to disclose related to this work.
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2024, Journal of BiomechanicsNumber of synergies impacts sensitivity of gait to weakness and contracture
2022, Journal of BiomechanicsCitation Excerpt :Fewer synergies simulated more severe neuromuscular impairments (Cheung et al., 2012; Steele et al., 2015). We selected 5 synergies to reflect unimpaired control (Rozumalski et al., 2017; Shuman et al., 2019b) and 3–4 to reflect the altered control observed in CP (Bekius et al., 2020; Shuman et al., 2019a; Steele et al., 2015; Tang et al., 2015) and stroke (Clark et al., 2010). Two synergy control, sometimes reported in stroke (Clark et al., 2010) and CP (Shuman et al., 2019a; Tang et al., 2015), could not track unimpaired gait and was excluded (Mehrabi et al., 2019).
Synergies are minimally affected during emulation of cerebral palsy gait patterns
2022, Journal of BiomechanicsCitation Excerpt :The observed similarity of synergy weights during baseline and emulated gait patterns aligns with previous work. In ND adults, prior work has found that similar synergies are recruited with varying gait speed (Ivanenko et al., 2004), incline (Rozumalski et al., 2017), bodyweight loading (McGowan et al., 2010), and stepping condition (Routson et al., 2014). This observation also extends to clinical populations where synergy structure was similar following surgical intervention and gait biofeedback training in CP (Booth et al., 2019; Shuman et al., 2019) and across stepping patterns in stroke (Routson et al., 2014), despite significant changes in gait.
The effect of prolonged walking on muscle fatigue and neuromuscular control in children with cerebral palsy
2022, Gait and PostureCitation Excerpt :Previous research showed that similar muscle synergies are activated during different types of activities, such as walking, running and cycling [36]. Moreover, it has been shown that changes in muscle synergies are minimal across different conditions, for instance during treadmill walking at a range of speeds in TD children [37] and during walking with biofeedback in both TD children and children with CP [23]. It has also been found that CP-related treatments can alter the gait pattern in children with CP, but do not change muscle synergies [38].
The effects of fatigue on synergy of selected lower limb muscles during running
2020, Journal of BiomechanicsCitation Excerpt :Serrancoli et al. studied muscular synergies in patients with ACL rupture and showed that muscular synergy has remained unchanged (Serrancolí et al., 2016). Rozumalski et al. studied the muscular synergy in various speeds and different slope conditions on treadmill, and pointed out that in spite of several changes in movement kinematics, the synergy of the muscles remained constant (Rozumalski et al., 2017). Also, Saito et al. showed that muscular synergies are similar during running in different speeds and slopes (Saito et al., 2018a,b).