Neuromuscular control of gait stability in older adults is adapted to environmental demands but not improved after standing balance training

TLDR: The adaptations of synergies to NBW can be interpreted as related to a more cautious weight transfer to the new stance leg and enhanced control over CoM movement in the stance phase, however, control of mediolateral gait stability and these adaptations were not affected by balance training.

Abstract: Balance training aims to improve balance and transfer acquired skills to real-life tasks and conditions. How older adults adapt gait control to different conditions, and whether these adaptations are altered by balance training remains unclear. We investigated adaptations in neuromuscular control of gait in twenty-two older adults (72.6 ± 4.2 years) between normal (NW) and narrow-base walking (NBW), and the effects of a standing balance training program shown to enhance unipedal balance control in the same participants. At baseline, after one session and after 3-weeks of training, kinematics and EMG of NW and NBW on a treadmill were measured. Gait parameters and temporal activation profiles of five synergies extracted from 11 muscles were compared between time-points and gait conditions. No effects of balance training or interactions between training and walking condition on gait parameters or synergies were found. Trunk center of mass (CoM) displacement and velocity (vCoM), and the local divergence exponent (LDE), were lower in NBW compared to NW. For synergies associated with stance of the non-dominant leg and weight acceptance of the dominant leg, full width at half maximum (FWHM) of the activation profiles was smaller in NBW compared to NW. For the synergy associated with non-dominant heel strike, FWHM was greater in NBW compared to NW. The Center of Activation (CoA) of the activation profile associated with dominant leg stance occurred earlier in NBW compared to NW. CoAs of activation profile associated with non-dominant stance and non-dominant and dominant heel strikes were delayed in NBW compared to NW. The adaptations of synergies to NBW can be interpreted as related to a more cautious weight transfer to the new stance leg and enhanced control over CoM movement in the stance phase. However, control of mediolateral gait stability and these adaptations were not affected by balance training.

Full text

1
Neuromuscular control of gait stability in older
adults is adapted to environmental demands but not
improved after standing balance training
Leila Alizadehsaravi
1
, Sjoerd M. Bruijn
1
, Wouter Muijres
1, #a
, Ruud A.J. Koster
1
, Jaap H. van
Dieën
1*
1
Department of Human Movement Sciences, Faculty of Behavioural and Movement
Sciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands
1
#a
Current Address: Human Movement Biomechanics Research Group, Katholieke
2 Universiteit Leuven, Leuven, Belgium
3
4
5 * Corresponding author
6 E-mail: j.van.dieen@vu.nl (J.H.v.D.)
.CC-BY 4.0 International licenseperpetuity. It is made available under a
preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in
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2
7 Abstract
8 Balance training aims to improve balance and transfer acquired skills to real-life tasks and
9 conditions. How older adults adapt gait control to different conditions, and whether these
10 adaptations are altered by balance training remains unclear. We investigated adaptations in
11 neuromuscular control of gait in twenty-two older adults (72.6 ± 4.2 years) between normal
12 (NW) and narrow-base walking (NBW), and the effects of a standing balance training program
13 shown to enhance unipedal balance control in the same participants. At baseline, after one
14 session and after 3-weeks of training, kinematics and EMG of NW and NBW on a treadmill
15 were measured. Gait parameters and temporal activation profiles of five synergies extracted
16 from 11 muscles were compared between time-points and gait conditions. No effects of balance
17 training or interactions between training and walking condition on gait parameters or synergies
18 were found. Trunk center of mass (CoM) displacement and velocity (vCoM), and the local
19 divergence exponent (LDE), were lower in NBW compared to NW. For synergies associated
20 with stance of the non-dominant leg and weight acceptance of the dominant leg, full width at
21 half maximum (FWHM) of the activation profiles was smaller in NBW compared to NW. For
22 the synergy associated with non-dominant heel strike, FWHM was greater in NBW compared
23 to NW. The Center of Activation (CoA) of the activation profile associated with dominant leg
24 stance occurred earlier in NBW compared to NW. CoAs of activation profile associated with
25 non-dominant stance and non-dominant and dominant heel strikes were delayed in NBW
26 compared to NW. The adaptations of synergies to NBW can be interpreted as related to a more
27 cautious weight transfer to the new stance leg and enhanced control over CoM movement in
28 the stance phase. However, control of mediolateral gait stability and these adaptations were not
29 affected by balance training.
30
.CC-BY 4.0 International licenseperpetuity. It is made available under a
preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in
The copyright holder for thisthis version posted October 28, 2020. ; https://doi.org/10.1101/2020.10.28.358788doi: bioRxiv preprint

3
31 Keywords: Balance training, postural balance, aging, skill transfer, gait control, narrow-base
32 walking, muscle synergy
33 Introduction
34 Falls in older adults mostly occur during walking [1]. Therefore, skills acquired during
35 standing balance training should transfer to gait and improve gait stability [2]. While on one
36 hand effects of balance training have been described as task specific [3], on the other hand,
37 transfer from standing balance training to gait stability has been suggested by improved clinical
38 balance scores and gait parameters [4,5]. Consequently, the existence of skill transfer from
39 standing balance training as well as the mechanisms underlying such transfer, if present, are
40 insufficiently clear.
41 Increased variability and decreased local dynamic stability of steady-state gait were shown
42 to be associated with a history of falls in older adults [6]. From a mechanical perspective, larger
43 mediolateral center of mass excursions and velocities would be expected to cause an increased
44 fall risk [7] and both these parameters as well as their variability are larger in older than young
45 adults [8]. When facing environmental challenges, such as when forced to walk with a narrow
46 step width, individuals need to adapt their gait. Older adults show more pronounced adaptations
47 to narrow-base walking compared to young adults [8], possibly because they are more cautious
48 in the presence of postural threats [9]. Transfer of standing balance training to gait would be
49 expected to result in increased gait stability, decreased CoM displacement and velocity, and
50 decreased CoM displacement variability. In addition, an interaction between training and
51 stabilizing demands may be expected. Increased confidence after training may result in less
52 adaptation to a challenging condition. On the other hand, balance training may enhance the
53 ability to adapt to challenging conditions.
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preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in
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4
54 The central nervous system is thought to simplify movement by activating muscles in
55 groups, called muscle synergies, with the combination of synergies shaping the overall motor
56 output [10,11]. Muscle synergies consist of time-dependent patterns (activation profiles) and
57 time-independent factors (muscle weightings). Human gait has been described with four to
58 eight muscle synergies [12–14] and reactive balance control was found to have four shared
59 synergies with walking [14], which could be important for transfer from balance training to
60 gait. Due to aging and changes in sensory and motor organs, adapted synergies are likely
61 required to maintain motor performance [15,16]. Synergy analyses of gait revealed either fewer
62 synergies in older adults than in young adults [17] or no differences [18]. Motor adaptation is
63 assumed to result from altering synergies in response to task and environmental demands
64 [19,20]. For example, widened activation profiles appear to be used to increase the robustness
65 of gait in the presence of unstable conditions or unpredictable perturbations [20,21]. Long-term
66 balance training might alter synergies in gait, and adaptation of synergies to task demands as
67 has been shown in dancers [22,23] to achieve the alterations in CoM kinematics.
68 We investigated the adaptations in neuromuscular control of gait in older adults between
69 normal and narrow-base walking, and the effect of short- and long-term standing balance
70 training on this. To this aim, we used data from a previous study on standing balance training,
71 from which we previously reported positive effects of training on standing balance robustness
72 and performance, both after a single training session and after three weeks of training [24].
73 Here, we evaluate skill transfer to normal walking and narrow-base walking on a virtual beam,
74 both on a treadmill. We used foot placement error to assess performance of narrow-base
75 walking [25]. We focused on mediolateral balance control, as larger mediolateral instability
76 has been shown to be associated with falls in older adults [26,27] and beam walking challenges
77 mediolateral stability. We calculated the CoM displacement and CoM displacement variability,
78 CoM velocity and the LDE as measures of gait stability and extracted muscle synergies to
.CC-BY 4.0 International licenseperpetuity. It is made available under a
preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in
The copyright holder for thisthis version posted October 28, 2020. ; https://doi.org/10.1101/2020.10.28.358788doi: bioRxiv preprint

5
79 characterize effects on the neuromuscular control of gait and of adaptations to narrow-base
80 walking.
81 Methods
82 The methods described here in part overlap with our previous paper [24], as data were
83 obtained in the same cohort.
84 Participants
85 Twenty-two older (72.6 ± 4.2 years old; mean ± SD, 11 females) healthy volunteers
86 participated in this study. Participants were recruited through a radio announcement, contacting
87 older adults who previously participated in our research, flyers and information meetings.
88 Individuals with obesity (BMI > 30), cognitive impairment (MMSE<24), peripheral
89 neuropathy, a history of neurological or orthopedic impairment, use of medication that may
90 negatively affect balance, inability to walk for 4 minutes without aid, and performing sports
91 with balance training as an explicit component (e.g., Yoga or Pilates) were excluded. All
92 participants provided written informed consent before participation and the procedures were
93 approved by the ethical review board of the Faculty of Behavioural & Movement Sciences,
94 VU Amsterdam (VCWE-2018-171).
95 Experimental procedures
96 Participants completed an initial measurement to determine baseline values (Pre), a single-
97 session balance training (30-minutes), a second measurement (Post1) to compare to baseline
98 to assess short-term training effects, a 3-week balance training program (9 sessions x 45
99 minutes training), and a third measurement (Post2) to compare to baseline to assess of long-
100 term training effects (Fig 1).
.CC-BY 4.0 International licenseperpetuity. It is made available under a
preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in
The copyright holder for thisthis version posted October 28, 2020. ; https://doi.org/10.1101/2020.10.28.358788doi: bioRxiv preprint

Frequently asked questions

Q1. What have the authors contributed in "Neuromuscular control of gait stability in older adults is adapted to environmental demands but not improved after standing balance training" ?

In this paper, the authors evaluated the transfer from standing balance training to gait stability in older adults. 

Q2. Why are adapted synergies required to maintain motor performance?

Due to aging and changes in sensory and motor organs, adapted synergies are likely 61 required to maintain motor performance [15,16]. 

Q3. How long did the participants walk on a treadmill?

To quantify transfer to gait, participants were instructed to walk 114 for 4.5 minutes at a constant speed of 3.5 km/h on a treadmill with an embedded force plate. 

Q4. How do the authors adapt their gait to the environment?

When facing environmental challenges, such as when forced to walk with a narrow 46 step width, individuals need to adapt their gait. 

Q5. What is the effect of the reduction in activation of the dominant leg?

This reduction in activation would reflect a decrease in 304 muscle activity related to push-off and possibly reflects a more cautious gait. 

Q6. Why do older adults show more pronounced adaptations to narrow-base walking compared to young?

Older adults show more pronounced adaptations 47 to narrow-base walking compared to young adults [8], possibly because they are more cautious 48 in the presence of postural threats [9]. 

Q7. How long does 66 balance training alter synergies in gait?

Long-term 66 balance training might alter synergies in gait, and adaptation of synergies to task demands as 67 has been shown in dancers [22,23] to achieve the alterations in CoM kinematics. 

Q8. What was the time normalized time-series of trunk vCoM?

The authors used the time normalized time-series (i.e. 161 160 strides of data were time normalized to 16000 samples, preserving between stride 162 variability) of trunk vCoM to reconstruct a state space with 5 embedding dimensions at 10 163 samples time delay [33]. 

Q9. How does the transfer of balance training affect the ability to walk?

While on one 36 hand effects of balance training have been described as task specific [3], on the other hand, 37 transfer from standing balance training to gait stability has been suggested by improved clinical 38 balance scores and gait parameters [4,5]. 

Q10. How many weeks of training are needed to transfer skills?

For transfer of acquired 314 skills to a new task, it may be necessary that a high skill level is achieved and possibly more 315 than 3 weeks are needed.