Abstract
[Purpose] This study aimed to investigate variations in step time and trunk acceleration during the first five steps of walking initiation when rhythmic auditory stimuli matched to a comfortable walking tempo, were provided before walking. [Participants and Methods] Seventeen healthy, right-foot dominant adults (10 males, 7 females; mean age 23.2 ± 4.9 years; mean height 165.3 ± 10.2 cm) without orthopedic or neurological abnormalities were enrolled in this study. The participants were instructed to perform 10 steps of indoor-level walking with rhythmic auditory stimulation in two tasks. In Task 1, participants began walking after hearing the 1st auditory stimulus, while in Task 2, they initiated walking after the 10th auditory stimulus. Step times; peak trunk acceleration values in the vertical, lateral, and forward/backward directions; and the coefficients of variation for these measures over the first five steps were compared between the two tasks. [Results] The step time during Task 2 was significantly longer than that during Task 1. The coefficients of variation for step time and lateral and forward trunk accelerations during Task 2 were significantly lower than those during Task 1. [Conclusion] This study found that the variability in step time and lateral and forward trunk accelerations during the five steps of walking initiation decreased when healthy participants listened to rhythmic auditory stimuli 10 times before walking.
Key words: Rhythm auditory stimulation, Walking initiation, Trunk acceleration
INTRODUCTION
Walking initiation is defined as the transient movement between an upright posture and steady-state walking1). Walking falls among the elderly commonly occur within the first few steps of walking initiation2), due largely to the increase in step-time variability (time change per step)3). In physical therapy, periodic auditory stimulation is commonly used to decrease step time variability during walking4,5,6). Such auditory stimuli are termed “Rhythmic Auditory Stimulation”4), and the stimulus interval is set based on the step time of the participant’s comfortable walking4, 5). Rhythmic auditory stimulation is commonly used as a neurological therapy that applies the physiological prompting effect of constant rhythmic auditory stimulation to the upper motor neuron system, including the basal ganglia, cerebellum, dorsal premotor cortex, and supplementary motor cortex. As an example, previous studies have shown that participants performed movements in time with rhythmic auditory stimulus, which stabilized the tempo of rhythmic movements such as walking7). In healthy participants, walking speed with rhythmic auditory stimulation at regular intervals is faster than comfortable walking8). However, the step time of walking in normal participants varied slightly. Stepping on the swing side of the lower limb in response to rhythmic auditory stimuli requires motor coordination of the lower limb joints, resulting in large fluctuations in step time and length9). These studies analyzed steady-state walking, excluding walking initiation and termination. On the other hand, these studies did not examine walking initiation, which need for voluntary motor coordination of the lower limb joints. Rhythmic auditory stimuli are “disturbance stimulation”. We consider it important to examine the effect of rhythmic auditory stimulation on walking tempo at walking initiation in healthy adults.
Our previous study10) showed that walking in response to rhythmic auditory stimuli at the same tempo as comfortable walking in healthy adults increases the variability in step time and trunk acceleration (changes in speed during body center of gravity shifts) during the first five steps of walking initiation, due to the delayed onset of the first step of walking, and the need for motor coordination in response to auditory stimuli after the second step. This rhythmic auditory stimulus disturbed the participants’ comfortable walking. Walking initiation on a cue requires the voluntary motor coordination of the lower limb joints to step on the swinging side of the lower limb in response to rhythmic auditory stimulation. To decrease the variability of step time and trunk acceleration at the walking initiation with rhythmic auditory stimulation, it is necessary to make participants aware of the tempo of the rhythmic auditory stimulation prior to walking. Fujiwara et al.11) further showed that the standard deviation of the reaction time of the lower limb to rhythmic auditory stimuli decreased following the 10th stimulus. This result indicate that participants can perform movements with tempo prediction after listening to rhythmic auditory stimuli 10 times, and provide a basis for setting the number of rhythmic auditory stimuli before walking in this study. We hypothesize that exposure to rhythmic auditory stimulation multiple times before walking initiation will decrease variability in step time and trunk acceleration during the first five steps of walking initiation, thereby improving walking stability. The purpose of this study was to investigate the variations in step time and trunk acceleration during five steps of walking initiation when rhythmic auditory stimuli of the same tempo as comfortable walking were provided before walking.
PARTICIPANTS AND METHODS
For the number of recruits, we conducted a power analysis using G*Power (version 3.1.9.6) prior to the study. We decided to use the corresponding t-test if the data were normally distributed and the Wilcoxon signed-rank test if the data were not normally distributed. The types of power analysis used were “a priori: compute required sample size given α, power, and effect size”, “difference between two dependent means (matched pair)”, and “Wilcoxon signed-rank test (matched pair)”. The effect size dz=0.8, α=0.05, and power (1-β)=0.80. As a result, the minimum sample size required was calculated to be 12 participants. Seventeen right-foot dominant healthy adult volunteers (10 males and 7 females, mean age 23.2 ± 4.9 years, mean height 165.3 ± 10.2 cm) with no orthopedic or neurological abnormalities were enrolled in this study. Previous studies12) on the functions of the dominant and non-dominant feet during movement have reported that the dominant foot performs fine motor skills, while the non-dominant foot performs weight support. In a previous study, Sudo et al.13) found that right-handed participants had a more stable body center of gravity shift in the lateral and forward directions with right-footed walking initiation. The Chapman dominant foot test14) was performed to determine the dominant foot, while participants with scores ranging from 11 to 27 (Right-foot dominant) were recruited. Participants were verbally informed of the purpose of the study and asked to sign a consent form. The study was approved by the Research Ethics Review Committee of Aomori University of Health Sciences (Approval No. 22058).
Participants were instructed to perform 10 steps of indoor-level walking with rhythmic auditory stimulation in two tasks. Participants walked barefoot to reduce variation in walking due to differences in footwear. The walking paths were set at 10 steps at each participant’s step length plus 3-meter deceleration path. As in the studies by MacIntosh et al.8) and Terrier and Dériaz9), the stimulus interval of rhythmic auditory stimuli was set to the participants’ average step time calculated over 10 comfortable walking steps. During the movement tasks, participants were instructed to initiate walking after listening to the 1st auditory stimulus during Task 1, and the 10th auditory stimulus during Task 2. The movement tasks were performed in a random order, and both tasks were performed at least two days apart. Both tasks were performed for two trials each, with 5 minute breaks between trials. The average of two trials was used as the representative value. All the experiments were performed in a quiet environment.
Sound Trigger 2Plus (KISSEICOMTEC, Nagano, Japan) and headphones were used to present auditory rhythmic stimuli to both ears. The stimulus conditions for rhythmic auditory stimulation were set to a sound pressure level of 65 dB SPL, stimulus frequency of 750 Hz, and duration of 25 ms, as in the study by Ito et al15).
The participants were instructed to start walking with their right foot from a standing position for all tasks, and to walk from the starting point to the final point, including the deceleration path. During Task 2, the participants were restricted from moving their limbs in the standing position until the start of walking. All instructions to the participants were given orally using a script, and participants were asked to recite each instruction to check their understanding. The participants were also asked to visually check their compliance with the instructions. In this study, the participants did not perform the practice task in both conditions to prevent habituation to the tempo of rhythmic auditory stimuli. Following the completion of all tasks, participants were instructed to answer “yes” or “no” to the two following questions: 1) “Was it possible to recognize the tempo of the rhythmic auditory stimulus before the start of walking?”; and 2) “Was it possible to synchronize the first step of walking to the first rhythmic auditory stimulus?”. If they answered “no” to the second question, they were further asked if “the onset of the first step of walking preceded or delayed the auditory stimulus”.
The step time and vertical, lateral, and forward/backward trunk accelerations were set as the measurement items. Step time was defined as the time from the initial contact to the left initial contact. For example, the step time between the first and second step is specified as “Step 1–2.” A foot switch, attached to each heel on each side, was used to identify the initial contact. Telemetry electromyographs MQ8 and Vital Recorder2 (KISSEICOMTEC, Nagano, Japan) were used for recording, with a sampling frequency of 1,000 Hz. BIMUTAS-Video (KISSEICOMTEC) used to analyze footswitch contact signals. Referring to the method of Osaka et al.16), trunk acceleration during walking was recorded using an 8-channel compact wireless motion recorder MVP-RF8-HC-2000 (Microstone, Nagano, Japan) attached to the waist of the participant, with the Y-axis in the vertical direction. The sampling frequency of the motion recorder was set to 1,000 Hz. Waveform statistics of trunk acceleration were obtained on a personal computer using Microsoft Excel 365 (Microsoft Japan, Tokyo, Japan). Peak trunk acceleration values in each direction were identified using BIMUTAS II (KISSEICOMTEC). With reference to the studies by Auvinet et al.17) and Menz et al.18), the peak values of trunk acceleration observed before and after heel contact during walking were identified for each step of the 5 step waveforms. Furthermore, in a study by Auvinet et al.17), the lateral trunk accelerations were calculated as absolute values, because of the combination of the left (negative) and right (positive) accelerations. The mean, standard deviation, and coefficient of variation (%) were calculated for the step time and peak trunk accelerations in each direction for the first 5 steps of walking initiation. The coefficient of variation represents the variability of the data and is used as an indicator to assess the risk of falling while walking19). In this study, the coefficient of variation was employed as a measure of walking stability.
The Shapiro–Wilk test was applied to confirm the normality of all data. The step times, peak trunk accelerations in each direction, and coefficients of variation for the five steps of walking initiation were subsequently compared between the two tasks using the Wilcoxon signed-rank test. Step times, lateral and forward peak trunk accelerations for the five steps of walking initiation were compared between the two tasks using the Friedman test. When significant differences were observed, post-hoc multiple comparisons were conducted using the Wilcoxon signed-rank test with Bonferroni correction. Statistical significance was set at p<0.05. All statistical analyses were performed using the SPSS Statistics version 19 (IBM, Armonk, NY, USA).
RESULTS
The step times, peak trunk acceleration values in each direction, and coefficients of variation for the five steps of walking initiation between the two tasks are listed in Table 1. The median step time was 500.8 ms (range: 442.1–532.5 ms) during task 1 and 519.7 ms (range: 476.2–552.7 ms) during Task 2, with a significantly longer time during Task 2 (p<0.05, r=−0.59). The median coefficient of variation was 6.3% (range: 2.6–19.1%) during Task 1 and was significantly longer at 4.4% (range: 1.5–7.7) % during Task 2 (p<0.05, r=−0.61).
Table 1. Median and coefficient of variation at step times and peak trunk acceleration values during Tasks 1 and 2.
| Step times (ms) · Trunk acceleration (m/s2) | Coefficients of variation (%) | |||||
| Task 1 | Task 2 | ES (r) | Task 1 | Task 2 | ES (r) | |
| Step time | 500.8 (442.1–532.5) | 519.7 (476.2–552.7)* | −0.59 | 6.3 (2.6–19.1) | 4.4 (1.5–7.7)* | −0.61 |
| Lateral | 3.1 (1.8–4.5) | 3.1 (2.1–6.6) | −0.45 | 42.4 (17.6–75.0) | 24.2 (7.8–51.3)** | −0.80 |
| Upward | 6.0 (5.1–9.2) | 6.0 (5.1–9.6) | −0.13 | 10.7 (3.6–25.9) | 9.2 (3.1–31.2) | −0.22 |
| Downward | 1.3 (0.8–2.2) | 1.4 (0.7–2.8) | −0.18 | 14.8 (8.9–32.6) | 12.1 (4.3–26.2) | −0.19 |
| Forward | 5.1 (2.6–8.9) | 4.5 (3.0–9.0) | −0.19 | 33.0 (8.0–73.2) | 17.8 (4.7–42.3)** | −0.82 |
| Backward | 3.1 (1.3–5.8) | 3.7 (1.8–7.1) | −0.44 | 7.1 (3.6–13.7) | 7.2 (2.7–16.0) | −0.13 |
Median (Min–Max). **p<0.01, *p<0.05 (Task 1 vs. 2).
The median coefficient of variation of peak lateral trunk acceleration was 42.4% (17.6–75.0%) during Task 1 and 24.2% (range: 7.8–51.3%) during Task 2, which was significantly decreased during Task 2 compared with that during Task 1 (p<0.01, r=−0.80). The median coefficient of variation of the peak forward trunk acceleration was 33.0% (range: 8.0–73.2%) during Task 1 and 17.8% (range: 4.7–42.3%) during Task 2, which was significantly lower during Task 2 than during Task 1 (p<0.01, r=−0.82).
The median step times and peak values of trunk acceleration in the lateral and forward directions for each step of walking initiation 5 steps during Tasks 1 and 2 are shown in Tables 2 and 3, respectively. The median step time of Step 1–2 was 498.5 ms (range: 345.5–599.5 ms) during Task 1, and significantly longer during Task 2 at 573.0 ms (range: 444.5–635.0 ms) (p<0.05, r=−0.51). The median lateral direction trunk acceleration of the first step was 0.5m/s2 (range: 0.1–2.1m/s2) during Task 1, and significantly larger during Task 2 at 1.8m/s2 (range: 0.2–4.1m/s2) (p<0.01, r=−0.73). The median forward direction trunk acceleration of the first step was 3.1m/s2 (0.7–7.5m/s2) during Task 1, and significantly longer during Task 2 at 3.7m/s2 (range: 0.6–8.3m/s2) (p<0.01, r=−0.72).
Table 2. Step times for each step of walking initiation 5 steps during Tasks 1 and 2.
| Task 1 | Task 2 | ES (r) | ||
| Step time (ms) | Step 1–2 | 498.5 (345.5–599.5)* | 573.0 (444.5–635.0) | −0.51 |
| Step 2–3 | 530.0 (440.5–602.0) | 532.5 (510.5–596.0) | −0.04 | |
| Step 3–4 | 530.0 (434.5–607.5) | 523.0 (486.5–555.0) | −0.13 | |
| Step 4–5 | 515.5 (408.0–605.5) | 502.5 (480.0–561.0) | −0.05 | |
Median (Min–Max) *p<0.05 (Task 1 vs. 2).
Table 3. Peak trunk acceleration values in lateral and forward for each step of walking initiation 5 steps during Tasks 1 and 2.
| Task 1 | Task 2 | ES (r) | ||
| Lateral (m/s2) | Step 1 | 0.5 (0.1–2.1)** | 1.8 (0.2–4.1) | −0.73 |
| Step 2 | 3.2 (1.5–6.0) | 3.0 (1.8–5.2) | −0.21 | |
| Step 3 | 2.6 (1.3–4.9) | 3.1 (2.4–5.6) | −0.33 | |
| Step 4 | 4.0 (2.2–6.6) | 3.5 (2.1–5.7) | −0.26 | |
| Step 5 | 3.0 (0.8–5.2) | 3.9 (2.1–5.5) | −0.44 | |
| Forward (m/s2) | Step 1 | 3.1 (0.7–7.5)** | 3.7 (0.6–8.3) | −0.72 |
| Step 2 | 4.0 (2.9–8.7) | 3.9 (2.9–8.7) | −0.01 | |
| Step 3 | 5.7 (2.6–9.7) | 5.0 (2.7–9.6) | −0.40 | |
| Step 4 | 6.2 (2.8–10.0) | 5.7 (3.1–8.3) | −0.27 | |
| Step 5 | 5.3 (2.9–10.7) | 5.2 (2.8–10.9) | −0.21 | |
Median (Min–Max) **p<0.01 (Task 1 vs. 2).
Seventeen participants responded to the question after all tasks were performed, such that walking initiation during Task 1 was delayed until the auditory stimulus (Response rate: 100%). In contrast, 17 participants responded that they were able to initiate walking during Task 2 with tempo perception of a rhythmic auditory stimulus (Response rate: 100%).
DISCUSSION
This study showed that walking during Task 2 extended the step time, while decreasing the coefficient of variation of the step time and the peak values of lateral and forward trunk accelerations. In the participants’ subjective views, all participants were able to initiate walking during Task 2 with tempo perception of the rhythmic auditory stimulus.
We considered the tempo perception of rhythmic auditory stimuli, step time extension, and its coefficient of variation reduction in walking initiation during Task 2. When the rhythmic auditory stimulation was synchronized with movement, movement onset was delayed, as participants could not predict the first auditory stimulus; however, this was promptly remedied7). The participants in this study were instructed to walk in response to rhythmic auditory stimuli. However, during Task 1, as in our previous study10), when the rhythmic auditory stimulation was synchronized with movement, participants were unable to predict the first auditory stimulus, resulting in delayed movement initiation, as observed in simple reaction time tasks. This delay was promptly corrected by motor adjustments made to align subsequent steps with the rhythmic auditory stimuli. Consequently, the step time for Step 1–2 of walking during Task 1 was shorter than the target interval for rhythmic auditory stimulation. A prior study by Kudo et al.20) showed that when the same interval of rhythmic auditory stimuli was listened to three times, movement initiation could be executed accurately for the third auditory stimulus. Fujiwara et al.11) further showed that the standard deviation of the reaction time of the lower limb to rhythmic auditory stimuli decreased after the 10th stimulus, and the movement could be performed with tempo recognition. These results suggest that when healthy adults move with rhythmic auditory stimuli, about 10 auditory stimuli are needed to predict the tempo of the movement. During Task 2, the participants listened to rhythmic auditory stimuli at the target tempo nine times before walking initiation. All participants perceived the tempo of the auditory stimulus before walking initiation, and were able to initiate walking in response to the auditory stimulus during Task 2. In addition, the participants were able to walk at the target tempo after the second step, which extended the step time for Step 1–2. Consequently, the step time for walking initiation in the five steps was prolonged, and the coefficient of variation decreased.
We considered the decreased coefficient of variation of the peak values of lateral trunk acceleration during Task 2. Osaka et al.16) previously showed that walking trunk acceleration measured with a small accelerometer worn on the lower back represents a shift in the body’s center of gravity. Studies by Auvinet et al.17), Menz et al.18), and Neumann21) all showed that lateral trunk acceleration occurs immediately following initial contact, as a preparation for swinging the other lower limb. The participants were delayed in the first step, and needed to step on the lower limb at a faster tempo than comfortable walking during Task 1. The median lateral trunk accelerations for the second and fourth steps were greater than those for the first five steps of walking initiation during Task 1. This result indicates that the second and fourth steps at the start of walking during Task 1 increased the contralateral acceleration or ipsilateral deceleration. The results further showed that the lateral trunk acceleration for the second and fourth steps increased with contralateral acceleration or ipsilateral deceleration during Task 1. In other words, the participants adjusted their body’s center of gravity shift to perform the initial contact in the third and fifth steps, in accordance with the tempo of the rhythmic auditory stimulus. Therefore, the coefficient of variation of peak lateral trunk acceleration increased during Task 1. In contrast, the lateral trunk acceleration in the first step during Task 2 was greater than that during Task 1. The participants perceived the tempo of the auditory stimulus before walking, and were able to ground their first step in time using the rhythmic auditory stimulus. They prepared the initial contact in the second step using the contralateral acceleration or ipsilateral deceleration in the first step. In addition, participants may have performed contralateral acceleration or ipsilateral deceleration in order to walk with rhythmic auditory stimulation after the second step. As a result, the coefficient of variation of lateral trunk acceleration decreased during Task 2.
Subsequently, we considered the decreased coefficient of variation of the peak value of forward trunk acceleration during Task 2. Sato et al.22) showed that when the step time of walking is short, the forward shift of the center of pressure is accelerated, and the forward component of the ground reaction force is increased. Auvinet et al.17) further showed that forward trunk acceleration is a propulsive force during walking that reaches a maximum value immediately prior to initial contact. Participants were required to correct errors between the rhythmic auditory stimulus and the initial walking contact during Task 1. Additionally, they were required to step forward with their lower limbs for a shorter time than the comfortable walking initiation. Our previous study10) similarly showed that normal participants could correct the first-step delay by rapid forward acceleration during the four steps of walking initiation with rhythmic auditory stimulation at the same tempo as the step time for comfortable walking. It is possible that the coefficient of variation of the forward trunk acceleration increased during Task 1 of this study, which also required a sudden forward shift of the body’s center of gravity after the second step to correct the delay in the first step. However, similar to the lateral trunk acceleration, the forward trunk acceleration in the first step was larger during Task 2 than during Task 1. We considered that the participants perceived the tempo of the rhythmic auditory stimulus before walking, and that the forward acceleration in the first step prepared them for initial contact in the second step. In addition, it is possible that forward acceleration achieves the purpose of walking with rhythmic auditory stimulation even after the second step. As a result, the coefficient of variation of forward trunk acceleration decreased during Task 2.
The results of this study showed that when healthy participants listened to rhythmic auditory stimuli 10 times prior walking, the variability in step time and lateral and forward trunk accelerations of the five steps of walking initiation was decreased. The coefficient of variation represents the variability of the data and is often employed as an indicator to assess the risk of falling while walking or as a measure of walking stability19). The decreased variability in step time and trunk acceleration in Task 2 suggests that rhythmic auditory stimulation improves the stability of the tempo of the five steps of walking initiation in healthy adults. In particular, we considered that the 75 ms step time extension for step 1–2 during Task 2 might contribute to improved walking stability, such as stance time extension of the first step and step width expansion of the second step of walking initiation.
The limitations of this study are that it was not possible to show the number and quality of auditory stimuli required to decrease the variability of the parameters and changes in joint movements during the five steps of walking initiation. In addition, due to the small sample size, the effects of gender differences on step time and trunk acceleration for walking could not be examined. While the stimulus parameters used in this study were effective for the adult participants, older adults with age-related hearing loss or central auditory processing deficits may require adjustments in stimulus intensity or frequency. Future studies should explore parameter optimization for older populations to enhance the generalizability of those findings.
Conflict of interest
The author, their immediate family, and any research foundation with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article. We have not received any funding related to the subject matter of this article.
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