Adapting spatiotemporal gait symmetry to functional electrical stimulation during treadmill walking

Seung-Jae Kim; Alex Worthy; Brandom Lee; Setareh Jafari; Olivia Dyke; Jeonghee Cho; Elijah Brown

doi:10.1371/journal.pone.0312285

. 2024 Oct 18;19(10):e0312285. doi: 10.1371/journal.pone.0312285

Adapting spatiotemporal gait symmetry to functional electrical stimulation during treadmill walking

Seung-Jae Kim ^1,^*, Alex Worthy ¹, Brandom Lee ¹, Setareh Jafari ¹, Olivia Dyke ¹, Jeonghee Cho ¹, Elijah Brown ¹

Editor: Kei Masani²

PMCID: PMC11488702 PMID: 39423203

Abstract

Individuals with neurological impairments often exhibit asymmetrical gait patterns. This study explored the potential of using functional electrical stimulation (FES) as a perturbation method during treadmill walking to promote gait symmetry adaptation by investigating whether the FES perturbation could induce gait adaptation concerning spatial and temporal gait symmetry in healthy subjects. In the FES perturbation, both legs received electrical pulses at the same period as the subjects’ initial stride duration, and the temporal gap between the two pulses for each leg was manipulated over a 7-min period. Following this, subjects continued to walk for another 5 minutes without FES. Subjects participated in two trials: implicit and explicit. In the implicit trial, they walked comfortably during FES perturbation without consciously adjusting their gait. In the explicit trial, they voluntarily synchronized their toe-off phase to the stimulation timing. To examine the effects of the FES perturbation, we measured step length and stance time and then analyzed changes in step length and stance time symmetries alongside their subsequent aftereffects. During the explicit trial, subjects adapted their gait patterns to the electrical pulses, resulting in a directional change in stance time (temporal) symmetry, with the left stance becoming shorter than the right. The stance time asymmetry induced by FES perturbation showed a slight residual effect. In the implicit trial, the directional change trend was slightly observed but not statistically significant. No consistent trend in step length (spatial) symmetry changes was observed in either condition, indicating that subjects may adapt their spatial gait patterns independently of their temporal patterns. Our findings suggest that the applied FES perturbation strategy under explicit condition can induce adaptations in subjects’ temporal gait asymmetry, particularly in stance. The implicit condition showed a similar slight trend but was not statistically significant. Further experiments would provide deeper understanding into the mechanism behind subjects’ response to FES perturbations, as well as the long-term effects of these perturbations on the spatial and temporal aspects of gait symmetry.

Introduction

Gait asymmetry frequently follows neurological impairments such as stroke, Parkinson’s disease (PD), or multiple sclerosis (MS) [1, 2]. The achievement of gait symmetry is an important goal in rehabilitation, as it can significantly alleviate issues experienced by many neurologic populations. These issues include reductions in several areas such as walking speed, stability-balance [3, 4], general activity levels, and load-related aspects potentially affecting bone density [5]. Perturbation-based gait training strategies have emerged as effective methods for enhancing and treating gait asymmetry. Rehabilitation robots, for instance, can be integrated into exoskeletons to guide or perturb the patient’s walking patterns, promoting efficient adaptation and correction [6–8]. The split-belt treadmill (SBT), a potent rehabilitation tool, effectively alters patients’ gait patterns through short-term motor adaptation [9, 10], leading to aftereffects following adaptive training [11, 12]. Typically, when subjected to external perturbations during motor training, the nervous system reacts by trying to reduce errors from one movement to the next, showcasing its capacity for rapid adjustment. This critical attribute can be effectively utilized within a rehabilitation program [13].

An alternative approach, quite distinct from utilizing mechanical devices for administering perturbations, involves functional electrical stimulation (FES). FES is a well-established technique used in gait rehabilitation; individuals often pair FES with treadmill or overground walking to activate critical muscles involved in walking or facilitate the reorganization of existing neural circuits by timing the stimulation in sync with the different gait phases [14, 15]. While FES can bring about many other effects on gait rehabilitation, in this study, we explored a novel way to utilize FES to perturb gait to induce gait symmetry adaptation. In our previous study [16], we demonstrated that the recurring sensorimotor stimulation provided by FES during treadmill walking could contribute to implicit changes in the gait cycle period: healthy subjects tended to spontaneously synchronize their gait phase with the timing of brief electrical pulses. Consequently, these synchronized responses resulted in alterations in the gait cycle period, corresponding to changes in pulse frequency.

We extended this idea and developed a hypothesis that skillfully manipulating the timing of electrical pulses applied to both legs could induce asymmetric gait patterns aligned with the gait characteristics synchronized with the external stimulations. To test this hypothesis, we devised an FES-based perturbation paradigm in which the period of electrical pulses applied to both legs is the same, but the time intervals of the two pulses can be adjusted over time: the adjusted time interval of the two pulses within a gait period was regarded as the perturbation level in this study. As the first objective of this study, we investigated whether such a perturbation paradigm utilizing FES could induce changes in spatial and temporal gait patterns while subjects voluntarily synchronized a specific gait phase of both legs with the perturbations (explicit condition). Motor learning includes a form of learning process known as use-dependent plasticity, which involves developing movement biases that favor repeated movement directions [17]. Thus, we hypothesized that the FES perturbation could induce asymmetric gait patterns through this learning process. Meanwhile, motor learning is a result of the combination of explicit (voluntary) and implicit (involuntary) adaptation processes [18]. Implicit adaptation has garnered significant attention in motor rehabilitation due to its potential for enhancing the retention of learned motor patterns from training [19–21]. Therefore, we also investigated whether the FES perturbation could lead to implicit changes in asymmetric gait patterns. To explore this, we also conducted implicit trials where subjects walked comfortably without attempting to compensate for their gait phase with the electrical stimulation. We hypothesized that the FES perturbation could, to some extent, induce asymmetric gait patterns depending on the degree to which an individual spontaneously adjusts their gait in response to FES perturbations. In this context, our study would support the idea that inducing asymmetric gait patterns could lead to gait symmetry among individuals who initially present with asymmetric gait. Therefore, a positive outcome of this study would imply that gait asymmetry adaptation through an FES perturbation paradigm holds promise as a potential method for gait asymmetry rehabilitation programs.

Methods

A. Subjects

Eighteen subjects (21.0 ± 2.8 years) participated in this study. Before obtaining their written informed consent, we provided the subjects with a detailed explanation of the study procedure. Subjects with an irregularity in their walking pattern, such as bow-leggedness, were excluded as this may interfere with our motion sensor’s ability to capture data. The subjects were informed of the physical fatigue they would experience during the experiment and were accustomed to walking on a treadmill. All protocols (065-1617-EXP) were approved by the Institutional Review Board of California Baptist University to ensure that the study adhered to national and international guidelines for research on humans. Additionally, all the researchers gained CITI certifications in Biomedical Researchers and Responsible conduct of research as an additional safeguard in adhering to regulations and protocols of working with subjects in a research environment. The recruitment phase for this study commenced on 02/05/2023 and ended on 08/15/2023.

B. Experimental setup

All experiments were performed on a treadmill (Woodway USA, Waukesha, WI) equipped with supporting handrails to ensure the safety of subjects. All subjects were given an approximate 5-minute preparatory period to adjust to walking on the treadmill. Two motion capturing markers were attached to the back of the subjects’ shoes and tracked by a camera-based motion-capturing system (Optotrak 3D Investigator, Norther Digital Inc. Canada). This system located the positions of the markers and sent the data to a PC in real-time using a program developed with LabVIEW (National Instruments Corp., TX) to measure the subjects’ spatiotemporal gait parameters such as step length, stride period, and stance duration. In this study, the position of the most forward marker was designated as the heel strike position, while the most backward marker position was identified as the toe-off position. We determined the stride period by measuring the interval from one heel-strike to the next, and the stance duration by measuring the interval from a heel-strike to the subsequent toe-off. It is important to note that the actual instance of toe-off occurs slightly after the marker reaches its most backward position. Nonetheless, we adhered to these measurement criteria consistently, prioritizing the assessment of symmetry between the two legs.

In all trials, subjects walked on a treadmill while being hooked up to a commercial electrical stimulator (MOTIONSTIM8, Krauth+Timermann, German), controllable through a computer program. Two 2” x 2” square electrodes, placed approximately 10 cm apart on the calf and the lower ankle, were used to trigger ankle movement by contracting the calf muscle (Fig 1A). Stimulation locations for the calf group included the sural nerve, gastrocnemius, peroneus, or soleus. The electrical stimulator was battery-powered, and a current isolator was used in conjunction with it for added safety. The stimulation threshold of each subject was determined by the magnitude of the current that induced slightly noticeable ankle plantar flexion. The preferred amplitude ranged from 20 mA– 30 mA during the trials. After documenting subjects’ preferred stimulation amplitude and walking speed, an experimental trial ensued where their preferred treadmill speed and amplitude threshold were employed.

Fig 1 — (A) Experimental setup showing a subject’s trial with electrodes placed on the lower legs. (B) Each 16-minute trial consisted of a 4-minute baseline, a 7-minute perturbation, and a 5-minute post-perturbation period. For the perturbation period, the offset time was gradually adjusted to 0, -20, -40, -60, -80, and -100 ms from the initial τ. (C) During the initial FES perturbation period, electrical pulses were delivered to both legs at the same frequency as the initial stride, but the timings of the two pulses were separated by time τ, which signifies the initial time separation between the left toe-off and the subsequent right toe-off. Gradually, the timing interval between the two pulses was decreased by Δτ.

C. Experimental protocol

Experiments were conducted with the following objectives: a) to primarily investigate the impacts of the FES perturbation on spatiotemporal gait symmetry among healthy subjects and b) to explore how the effects varied between the subjects’ explicit and implicit actions during training. Accordingly, all subjects were required to participate in two distinct trials separated by several days: a trial with implicit condition and a trial with explicit condition. The implicit trials were always completed prior to the explicit trials. For the implicit trial, which involved unconscious reaction to FES, subjects were instructed to walk normally and comfortably through the trial. The subjects received no specific instructions, aside from being informed about the periodic electrical stimulation that would occur during the trials. Conversely, the explicit trial required deliberate adjustments, with subjects consciously entraining their gait to the timing of electrical stimulation. Specifically, the subjects were asked to explicitly synchronize the toe-off phase of their gait for both legs with the stimulation.

Each 16-minute trial consisted of three stages: a 4-min baseline period, a 7-min perturbation period, and a 5-min post-perturbation period (Fig 1B). During the baseline period, we measured and calculated the average time (τ) between the left-toe-off and the subsequent right-toe-off phases, as well as the average stride duration from each gait cycle. During the perturbation period, we administered electrical pulses (0.12-second duration, 200 μs biphasic pulses at 90 Hz, 20–25 mA intensity) to both the right and left legs, at the same period of the baseline stride duration. In other words, periodic electrical stimulation was applied to each leg independently, but the stimulations were not delivered simultaneously to both legs; there was a time interval of τ between the stimulations. The time interval between the two electrical pulses delivered to both legs was gradually decreased by the offset time Δτ (Fig 1C). During the initial 60 seconds of the perturbation period, the electrical pulses were applied with zero offset to acclimate subjects to the stimulation. After that, the offset time (Δτ) was gradually adjusted to -20 ms, -40 ms, and -60 ms for 60 seconds each, and -80 ms and -100 ms for 90 seconds, respectively (a 100 ms offset time was approximately 7.5% of the average gait cycle duration in this study). In essence, the separation time between two pulses delivered to both the right and left legs was reduced by Δτ. This manipulation was intended to make the right-toe-off phase occur slightly earlier than in the typical gait cycle, thus inducing gait asymmetry during the perturbation period. Following the perturbation period, electrical stimulation was stopped, and subjects continued to walk for the remaining 5 minutes of the post-perturbation period.

D. Data analysis

The primary measures analyzed in this study were step length and stance duration time. The step length was determined as the distance between the marker on each leg at the heel strike of the leading leg. Specifically, right step length refers to the distance measured at the right heel strike, while left step length refers to the distance measured at the left heel strike. The gait cycle typically consists of two phases: stance and swing. The stance duration was calculated as the percentage of time the foot remained in contact with the ground during the gait cycle (stride time). Right stance duration represents the percentage of time the right foot was in contact with the ground, while left stance duration represents the percentage of time the left foot was in contact with the ground. To evaluate the symmetry of step length and stance duration, a ratio (%) between the measurements of the right and left legs was computed for each gait cycle by using the following formula: 100×(right leg measure–left leg measure)/(0.5×(right leg measure + left leg measure)). For example, a positive step symmetry ratio indicates that the right step length is longer than the left step length, while a negative symmetry ratio indicates that the right step length is shorter than the left step length. In addition, double limb support time is defined by the time in which both feet are in contact with the ground. There are two periods of double support per gait cycle: right double support and left double support. We define right double support as occurring at the end of the right limb’s stance (i.e., the time from left heel strike to right toe-off) and left double support at the end of the left limb’s stance (i.e., the time from right heel strike contact to left toe-off).

For data analysis, the mean and standard deviation (SD) of the symmetry ratios were calculated in successive 30-second intervals to examine the changes in symmetry during the perturbation and post-perturbation periods. The group means and SDs of the step length symmetry and stance duration symmetry were then calculated across all the subjects. To minimize between-subject variability in gait symmetry, the baseline symmetry was used as a reference. The baseline symmetry, which represented the symmetry value measured from the baseline period, was subtracted from the measured symmetry data obtained during all perturbation and post-perturbation periods (including the baseline itself) for each subject.

The primary objective of this study was to investigate the presence of spatiotemporal gait asymmetry induced by the FES perturbation during treadmill walking. We conducted statistical analysis for both the 7-minute perturbation period and the subsequent 5-minute post-perturbation period separately. Paired t-tests were first utilized to determine significant changes in step length and stance duration symmetries, compared to the baseline. These tests allowed us to identify the specific perturbation levels (the offset time) that exhibited significant changes in symmetry. Notably, each perturbation level in our trials lasted either 60 or 90 seconds, and we used the symmetry value obtained from the last 30-second window of each perturbation level. For the post-perturbation period, we assessed only three 30-second epochs (early post-perturbation, middle post-perturbation, late post-perturbation). Additionally, a one-way repeated measures ANOVA was performed to determine how increasing perturbation levels affected changes in step length and stance duration symmetries. All statistical tests were performed at a significance level of p ≤ 0.05, and the p-values are presented in the main text unless depicted in the figures.

Results

Fig 2A illustrates an example of changes in step length and stance duration over time obtained from a subject during the explicit trial. Each data point represents a measurement from each gait cycle. The changes in group mean step length and group mean stance duration across various epochs (30-second intervals) during the explicit trial are shown in Fig 2B. Throughout the perturbation period, as the perturbation level (indicated by the time separation between two electrical pulses sent to the right and left legs) gradually changed, we noticed a slight elongation in the right step length compared to the left. Additionally, the stance duration for the left side decreased compared to the right side. When the stimulation stopped, the relative difference in step length and stance duration changes between the right and left legs appeared to revert to normal, resembling the patterns observed during the baseline period.

In the explicit condition, subjects exhibited a prolonged stance duration on their right leg (or a reduced stance duration on their left side) throughout the perturbation period, leading to a positive asymmetry ratio (Fig 3B). Paired t-test results revealed that the stance symmetries induced during the perturbation period were statistically significant in comparison to the baseline value (p = 0.0024, 0.0305, 0.0012, 0.0003, and 0.00032, respectively for each perturbation epoch). During the post-perturbation period, the stance asymmetry induced by FES perturbation lingered slightly, but no statistical significance was observed except in the 5-min post-epoch (p = 0.0149). These alterations in stance duration asymmetry appeared to influence the spatial gait parameter (step length symmetry) as indicated by the larger variance in step length symmetry during the perturbation period (Fig 3A). Nevertheless, there was no consistent trend in the direction of step length asymmetry changes, nor were there any statistically significant changes in step length symmetry across different epochs except in the 5-min post-epoch (p = 0.0469). The statistical analysis conducting a one-way repeated measure ANOVA with post-hoc pairwise multiple comparisons, focusing solely on the perturbation period of the explicit trial, revealed that different perturbation levels significantly influenced the magnitude of altered stance symmetry (F(4, 68) = 2.51, p ≤ .05). This result suggests a general trend of increasing stance duration asymmetry as perturbation levels increased.

Fig 3 — Explicit group results of step length symmetry (A) and average percent stance duration symmetry (B) averaged across 18 subjects over different epochs. Values equal to 0 represent perfect symmetry. The vertical lines show the standard deviation among subjects for each epoch. The asterisks (*) indicate where the induced symmetry values were shown to be significantly different from the baseline (p<0.05).

To investigate how the subjects modified their gait patterns in response to the FES perturbation, we computed the percent mean time for each leg’s heel strike and toe-off phases. We specifically examined the changes in the right stance and swing times compared to the left leg. Fig 4 illustrates the percent gait stance and swing time plot, with the mean percent time on the x-axis and different epochs vertically along the y-axis. During the perturbation period (Fig 4A), right toe-off and heel-strike times were shifted toward the left. Accordingly, the entire timeline for the right swing and stance was shifted to the left in response to FES perturbations. The shifting right swing and stance times decreased both right and left double support times compared to the baseline as shown in Fig 5A. In the post-perturbation period, the timeline shift seemed to revert toward the baseline, despite a minor residual effect.

Fig 4 — Changes in the percent duration of stance (represented by the solid line) and swing (represented by the dotted line), averaged across 18 subjects under both explicit (A) and implicit (B) conditions. Nine strides represent the stance and swing time obtained from each different epoch. In each epoch, the right stance and swing time are aligned with the left leg; the bottom and top lines represent the left and the right legs, respectively. The percentage times of the toe-off phase, heel strike, and the subsequent toe-off for the right leg were compared to those from the baseline. The asterisks (*) indicate statistically significantly significant differences from the baseline (p<0.05) for the phase timings.

Fig 5 shows the group mean changes in double limb support time for both legs under the explicit (A) and implicit (B) conditions. In the explicit trial, there was a notable decrease in double limb support time during the perturbation period. A statistically significant decrease in double limb support time was observed for both legs, yet no significant differences were detected between the right and left double limb support time (double limb support symmetry). Following the post-adaptation period, the double limb support time rapidly reverted to base levels. In the implicit trial, changes in double limb support time were minimal.

In the implicit trial, subjects did not make conscious actions in response to electrical stimulation. Fig 4B shows the percent gait stance and swing time from the implicit condition. Higher perturbation levels appeared to cause a slight leftward shift in the right swing and stance timeline, but no significant changes were observed. Fig 6A shows the changes in the group mean step length and group mean stance duration for the implicit trial. Throughout the perturbation period, a slight extension in the right stance was observed in juxtaposition to the left stance, but no statistical significance was found. Additionally, subjects did not exhibit any substantial changes in step length. Fig 6B shows the group mean of step symmetry changes and stance duration symmetry changes for the implicit condition. Concerning changes in the step length symmetry, no distinct trend was observed in the alterations of step length symmetry (Fig 6B top). Concerning changes in the stance symmetry, a slight trend toward positive changes in stance symmetry was observed during the perturbation period but not statistically significant, and this general trend vanished once the FES perturbation stopped. Statistical analysis conducted with a one-way repeated measures ANOVA revealed no significant effect of perturbation levels on changes in stance duration symmetry during the adaptation period. Similarly, no significant difference was observed during the post-adaptation period. In terms of step length symmetry, the variability of symmetry significantly increased during the perturbation period, and no substantial directional changes were observed.

Fig 6 — (A) Group data illustrating changes in step length and percent stance duration for implicit trials with vertical bars representing ±SD. Conventions are same as in Fig 2B. (B) Implicit group results of step length symmetry (*top*) and average percent stance duration symmetry (*bottom*) over different epochs, averaged across 18 subjects. The asterisks (*) indicate symmetry values that showed significant differences from the baseline measurement (p<0.05).

Discussion

In this study, we proposed a novel approach to utilizing FES as a perturbation method for altering symmetric gait patterns and evaluated the potential benefits of the FES perturbation by examining the extent of spatiotemporal gait asymmetry adaptation during treadmill walking. The achievement of gait symmetry is one of the primary goals in rehabilitation following neurological conditions. To address gait asymmetry, adaptive locomotor adjustments through motor training are essential. Rehabilitation devices, such as robotic gait orthosis or split-belt treadmills, can facilitate locomotor adjustments. These mechanical devices not only assist subjects in walking but also impart perturbations to their gait. Robotic devices can produce viscous resistance to the leg [22], while split-belt treadmills can modify spatiotemporal gait patterns [11]. These perturbation-based training methods can prompt gait adaptation, which is maintained on a short-term basis, as demonstrated in aftereffects. Gait adaptation can also occur in response to non-mechanical perturbations, such as visual feedback perturbation and electrical stimulation [23, 24].

Our prior study tested the effects of external periodic perturbation using electrical stimulation on gait entrainment (the synchronization of gait cycle duration to the period of electrical stimulation) while walking on a treadmill. We discovered that subjects spontaneously synchronized their gait cycle duration to the period of the electrical stimulation when the stimulation periods were relatively close to the subject’s initial gait period [16]. Remarkably, entrainment was still observed when the stimulation intensity was below the threshold that induced noticeable ankle movements. These observations suggest that periodic afferent signals evoked by FES may contribute to promoting certain features of entrainment, given that spinal neural networks significantly interact with afferent sensory feedback [25, 26]. In this study, we expanded upon this idea, utilizing FES as a perturbation method to induce gait asymmetry adaptation concerning spatiotemporal gait patterns. Perturbation-based training heavily relies on sensory inputs to provoke adaptive responses [27], with the option of using different types of perturbations. For example, visual or auditory cues can be employed as perturbations to engage corresponding sensory information in training. However, we believe that FES offers a simple and cost-effective way to introduce external perturbations during walking. FES not only disrupts gait patterns but also affects the somatosensory pathway, both directly and indirectly, during gait adaptation, leveraging brain plasticity to reshape the neural circuits involved in this process [14, 28]. In our FES perturbation procedure, we applied periodic electrical pulses to both legs, with a controllable time interval between the two pulses sent to each leg. Since no other studies have attempted to use FES in this manner toward inducing asymmetric gait adaptation, we measured the changes in step length and stance duration, and aimed to answer the following questions: (1) Does the use of electrical stimulations to both legs with an offset interval have an effect on alterations in spatiotemporal gait patterns (explicit trial)? and (2) If entrainment is partially a spontaneous phenomenon, does FES-induced perturbation still influence the alteration of spatiotemporal gait patterns even if a subject does not consciously respond to the perturbation (implicit trial)?

Effects of FES-induced perturbations on temporal gait asymmetry adaptation (explicit trial)

In this study, we arranged the implicit trials to always precede the explicit trials to avoid any possible influence or recollection of subjects’ explicit actions on their implicit trials. Here, we first analyzed the outcomes of the explicit trials to comprehend how subjects adapted their gait patterns in response to the FES perturbations. We focused on two adaptive gait parameters: step length and the percentage time in the stance phase. Step length is a spatial gait parameter while percent time in the stance phase (referred to as stance duration) is a temporal measure. During explicit trials, as subjects attempted to synchronize their right and left toe-off phase with the timing of the administered electrical pulse timings, their step length and stance duration changed differently between the right and left leg (Fig 2). As the interval between the right electrical pulse and left electrical pulse decreased (targeting a shorter gap between the left toe-off and the subsequent right toe-off), we observed a decrease in the left stance relative to the right (Fig 2B bottom). Correspondingly, the left swing time became longer than the right swing time (not shown). This resulted in a positive directional change in stance duration symmetry (Fig 3B).

Initially, we thought that the right stance duration would decrease due to the altered timing interval between the two periodic electrical pulses, which was intended to slightly advance the phase of right-toe off. Contrary to our expectations, we observed that the subjects tended to adjust both their left and right gait steps in a complementary manner in response to the perturbation. This compensatory behavior resulted in reduced double limb support time for both legs (Fig 5A), accompanied by a slight decrease in the left stance duration (a corresponding subtle increase in the right stance duration) more than in the opposite leg. The precise mechanism behind why and how subjects adjusted their gait steps in this specific way is still being examined. Fig 3 shows overall changes in gait symmetry relative to the baseline level for the explicit trial (where subjects consciously attempted to entrain their gait with the perturbation). The stance duration symmetry tended toward a positive increase with higher perturbation levels (offset time). Overall, an increase in stance duration asymmetry was observed with higher perturbation levels, except the initial period when the perturbation started. The unexpectedly higher stance duration asymmetry at the lowest perturbation level may be due to subjects initially struggling to align their gait phase with the timing of the perturbations. The adapted stance duration asymmetry returned to symmetry once the perturbation was removed. However, subtle positive asymmetry persisted for up to 5 minutes in the post-perturbation period. These findings demonstrated that the FES perturbation procedure can modify subjects’ temporal gait pattern without necessarily utilizing mechanical devices such as a split-belt treadmill (SBT), which requires physical interaction with the subjects’ walking. Another important observation is the retention trend in the adapted temporal parameter. The positive directional stance duration asymmetry persisted slightly during the post-perturbation period, with only the last epoch showing statistical significance. While this may not provide conclusive evidence, this observation differs from studies using split-belt treadmills. In those studies, stance duration was rapidly changed during adaptation and both legs’ stance time rapidly returned to baseline levels, as did stance time asymmetry [11]. This disparity may be due to differing environmental influences between mechanical-based and the FES-based perturbation approaches. FES perturbation did not involve speed asymmetry, while SBT includes physical speed changes between the right and left legs. Several combinations of other factors, such as psychological and biomechanical factors or afferent sensory signal actions, may influence adaptive behavior differently.

Although stride times for both legs were largely equivalent across all periods, the percentage time in stance, swing, and double limb support changed during the perturbation period. At baseline, stance, swing, and double support times were symmetric for both legs (Fig 4). During the perturbation period, the percent time of right toe-off and right heel-strike (start and end times of the right swing) were slightly advanced, leading to a slight leftward shift of the right swing and consequently right stance time as well relative to those of the left (Fig 4A). This change in right swing and stance times remained consistent throughout all perturbation levels. The shifting right swing and stance times decreased both right and left double support times compared to the baseline (Fig 5A). It was reported that SBT walking induces asymmetry in double limb support time, which is known to proportionally change with the split-belt speed ratio [29]. Although this study observed significant decrease in double limb support times for both legs (Fig 5A), it is important to highlight that no statistically significance differences were found in the double limb support time symmetry during the perturbation period, in contrast to what is typically seen in SBT walking. This implies that physical speed differences between the right and left legs predominantly determine double limb support symmetry, which was not the case with our FES perturbation approach.

Effects of FES-induced perturbations on spatial gait asymmetry adaptation (explicit trial)

Under the explicit condition, the FES perturbation procedure used in this study was primarily oriented toward altering stance and swing symmetry (temporal gait parameter) by entraining toe-off phase with stimulation timing. We anticipated that changes in temporal gait symmetry would inherently influence spatial gait symmetry, such as step length symmetry. However, the change in spatial gait pattern was not as significant as the observed temporal changes. A slight increase in the right step length was noticed at higher perturbation levels (Fig 2B top), but it was not statistically significant. Moreover, despite slight positive directional changes in step length symmetry during the perturbation period (Fig 3A), the large variance inhibited the determination of statistical significance. In summary, the response of step length changes to FES perturbation varied substantially across individuals. This implies that changes in temporal gait patterns are not necessarily tied to changes in spatial gait patterns. Essentially, accommodating temporal gait patterns does not obligate a modification of the spatial gait pattern, or vice versa. Other studies utilizing SBT demonstrated that interlimb coordination can be independently controlled and adjusted in the adult human nervous system without necessarily changing various aspects of intralimb coordination [29, 30]. This suggests that different gait parameters are maintained and adapted through separate processes. Our study’s results are consistent with the prior studies’ findings, indicating that temporal and spatial controls for symmetric gait can be adapted independently.

Effects of FES perturbations under implicit condition

Effective interventions must facilitate efficient motor adaptation and ensure persistent changes (retention) in newly learned motor patterns. Various researchers have proposed that the retention benefit of learning relies on the unconscious or automatic mode within the learning process [19–21]. Therefore, we wanted to understand how FES perturbation affects gait asymmetry changes under implicit conditions. In the implicit trial, subjects walked on a treadmill while receiving electrical pulses but did not consciously alter their gait patterns. We observed a substantial variation in how subjects spontaneously compensated their gait in response to FES perturbation. When examining changes in step length and stance duration, we noticed a slightly reduced left stance duration compared to the right during the perturbation period (Fig 6A bottom), resulting in somewhat positive directional changes in stance duration symmetry (Fig 6B bottom). The degree of asymmetry was significantly smaller than that induced by the subjects’ conscious actions (explicit trial). In the post-perturbation period, there were no signs of aftereffects of the asymmetric stance duration. Regarding the spatial gait pattern changes under the implicit condition, due to large variances across the subjects, we found no significant changes in step length or step length symmetry (Fig 6B top). Additionally, no substantial changes were observed in stance and double support time relative to either leg (Figs 5B and 6).

During implicit trials, we observed that some subjects were unwittingly subjected to perturbation, exhibiting little to no gait entrainment. Others showed substantial entrainment, but most showed only sporadic entrainment throughout the implicit trials. In our earlier study which utilized FES on only one leg, approximately 55% of subjects showed some degree of entrainment [16]. However, the current study showed a lower proportion of subjects showing some degree of entrainment, which could be because FES perturbation was applied to both legs in this study, as opposed to one. It appears more challenging for both legs to spontaneously display entrainment to electrical pulses on each leg than to show entrainment to electrical pulses on a single leg.

We speculate that using a higher stimulation amplitude could have yielded more significant results. However, increasing the amplitude might have more robustly stimulated the muscles and led to greater ankle torque, which was not our intent as a method of inducing gait asymmetry. We maintained minimal stimulation amplitude throughout the implicit trials, as we aimed to understand the extent to which sensory afferent signals caused by FES influence symmetric gait adaptation. If the stimulation intensity needs to be increased to induce significant symmetric gait adaptation spontaneously, this inevitably results in uncomfortable tactile sensations and necessitates incorporation of electrically evoked joint torque as an additional factor in gait adaptation. Another reason for the lack of distinct results under the implicit condition could be that even when entrainment occurred spontaneously in walking, it did not necessarily synchronize with toe-off phases. Some subjects showed entrainment to their heel-strike phases. Consequently, the outcomes exhibited by subjects varied, leading to greater variations in spatiotemporal gait symmetry changes. Under implicit conditions, an experimental protocol designed to accommodate individual differences would likely yield more significant results. Therefore, this suggests the need for further investigation in this area.

Limitations and further direction

The current study represents a pioneering effort to evaluate a novel FES-based perturbation procedure to induce gait asymmetry adaptation during treadmill walking. There are, however, several limitations to consider. First, the stimulation amplitude utilized in this study was confined to a minimum threshold; therefore, the results might be different if varied stimulation intensities were used. For instance, as the stimulation amplitude increases, stronger joint torque follows, which may contribute to inducing asymmetric gait adaptations differently through FES-evoked sensory signals involved in gait control via neural circuits in the spinal cord. Second, the maximum offset time for the perturbation used in this study was capped at 100 ms, which is roughly equivalent to 7.5% of the average gait cycle duration. Should the perturbation become larger, entrainment is unlikely to occur during treadmill walking due to the constraints on walking speed, which is fixed on a treadmill, putting boundaries on gait entrainment. If experiments can be conducted in an over-ground walking setting, the perturbation size could be adjusted more freely, making the effects of FES perturbation more visible. Additionally, due to variations in walking speed and gait styles among the subjects, the range of the offset time (Δτ) did not correspond to the exact percentage time of the gait cycle duration. If gait favorably entrains to a particular percentage of the gait cycle duration, then the offset time should be adjusted based on an exact percentage time of each individual’s gait cycle duration, rather than using an absolute time for more significant results. Third, this study did not explore how subjects’ inherent baseline inherent asymmetry tendencies may affect the directional changes in gait symmetries in response to FES. Although the baseline asymmetry’s statistical significance is negligible, it would be valuable to investigate this further. Another limitation is the short post-FES perturbation observation period, lasting only 5 minutes. To explore the long-term effect, an extended post-perturbation period should be examined to accurately assess any retention effects. These limitations highlight the necessity for further research.

Conclusion

This study investigated the efficacy of FES perturbation-based gait training, which employs periodic electrical pulses to both legs, to cultivate effective gait adaptation in spatial and temporal gait parameters: step length and stance duration. We found that FES perturbation training, where subjects consciously synchronized their gait to the stimulation, induced noticeable asymmetry in stance time that persisted marginally over a 5-minute post-perturbation period. Although not statistically significant, a slight trend of changes in stance time symmetry by FES was observed even without conscious effort, possibly suggesting that the changes in stance time asymmetry include spontaneous components to some extent. The changes in temporal gait symmetry did not correspond well with the changes in step length symmetry. This indicates that temporal and spatial controls for symmetric gait can adapt separately. It is our hope that electrical stimulation can serve as an alternate cost-effective method for gait rehabilitation, helping patients improve their gait asymmetry efficiently by facilitating gait asymmetry adaptation processes during treadmill walking training. Moreover, electrical stimulation has shown potential to enhance muscle strength and stability [31]. Hence, incorporating entrainment through FES may be advantageous in aiding individuals with gait impairments. Comprehensive future research measuring the degree of interaction between the explicit and implicit control of gait is necessary to fully understand the mechanisms at play in the FES-based perturbation approach.

Acknowledgments

Authors would like to thank the support provided by the College of Engineering at California Baptist University.

Data Availability

"data used for analysis" file is available from the google database at the following link: Kim, Seung-Jae (2024). Adapting spatiotemporal gait symmetry to electrical stimulation during treadmill walking [Dataset]. Dryad. https://doi.org/10.5061/dryad.d7wm37q7w.

Funding Statement

The author(s) received no specific funding for this work.

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PLoS One. doi: 10.1371/journal.pone.0312285.r001

Decision Letter 0

Kei Masani

26 Aug 2024

PONE-D-24-11792Adapting spatiotemporal gait symmetry to functional electrical stimulation during treadmill walkingPLOS ONE

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Reviewer #1: General Comments

(1) In general, the gait cycle varies among different subjects, so there should be some variability in gait cycle duration and the rate of stance and swing phases among subjects. In your experimental setup, the offset time of FES perturbation is determined as the absolute time from 0 to -100 ms. If there is some difference in gait cycle duration among subjects, it seems the perturbation timing is applied at different phases for each subject. What percentage is the Δτ of each subject in the gait cycle? Please indicate and discuss the influence of inter-subject variability on actual gait cycle duration and the rate of stance and swing phases.

(2) There is usually a slight gait asymmetry in normal walking, even in young healthy subjects, referred to as the “baseline” in this paper. In fact, in Fig. 2A, a typical subject’s baseline results also seem slightly asymmetrical; the right step length is larger than the left one, and the right stance duration is shorter than the left one, although the statistical significance of this difference is not clear. Such tendencies of gait asymmetry in normal walking may vary among subjects, with some showing the opposite tendency. Please indicate and discuss the influence of baseline asymmetry tendencies of each subject on the main perturbation results.

Specific Comments

(1) In Fig. 2A, the step length scale might be incorrect: (cm) → (mm)?

Reviewer #2: This study by Kim and colleagues investigated whether asymmetric FES could induce asymmetric walking in healthy young adults. The study is innovative and generally robust in their methodology and I commend the authors for that. On the other hand, the interpretation and reporting of the findings could still be refined. Kindly find specific comments below:

Abstract

Line 23: Is the aim of the study to improve or disrupt gait symmetry?

Line 29: Perhaps helpful to mention that the explicit trial was performed in another session.

Line 33: It is important to differentiate between results that are statistically significant and those that are not. The implicit condition failed to consistently induce temporal or spatial adaptation, even with large perturbations, and this should be clearly acknowledged.

Line 34: The right stance became relatively longer. If I look at Figure 2B, it seems like the most significant change in stance duration from baseline, is reduction in the left leg rather than increase in the right leg. The interpretation should be refined and adjusted throughout.

Line 38: Implications should be focused on the explicit response, as the implicit response was rather weak and inconsistent.

Introduction

The focus of the previous study was implicit adaptation to the FES, and here you introduce implicit adaptation to be relevant for rehabilitation. However the subsequent result and discussion section heavily focuses on explicit adaptation, and this seems confusing. Could you introduce why explicit adaptation is given this importance, and what the advantages of using FES for explicit adaptation compared to visual or auditory cues might be?

Methods

Kindly mention that the treadmill was a split-belt treadmill.

FES timing: How functional was the FES? Unclear why the FES was applied at toe-off when the plantar flexors already start working from mid- to terminal stance. Toe-off is when the hip and ankle flexors take over to accelerate the leg through swing phase.

FES – gait synchronization: Once the time period was calculated from the toe-offs, were the toe-offs still used to determine when each stimulation would be given or did the stimulation just occur at a preset rate irrespective of whether the left leg was in toe-off or not? Kindly clarify.

Heel-strike determination: Often heel-strikes occur after the foot achieves its most forward position (which occurs in the air, before putting the foot down on the treadmill). This could impact the parameters of participants who walk with this pattern. Why not use the force plates from the treadmill, or the change in velocity of the markers to determine heel-strikes?

Statistics – were all the outcomes normally distributed and did the models fit the data well?

Statistics Line 202 – Typically, post-hoc t-tests are only performed if there is a significant effect in the repeated measures ANOVA. Otherwise you run into multiple comparison problems.

Results

Figures 3 (Explicit) and 6 (Implict) Asymmetry – the scales on the axis of the figures are different. Kindly harmonize.

Results are rather descriptive – would prefer to start with inferential statistics and then describe those that are significant. Further, there is no need to repeat the description of the figures in the text and in the legend of the figure.

If you want to show a successive increase in asymmetry with larger perturbations, you would need to check the t-tests for pairs of perturbation levels, not by comparing with baseline. And correct for multiple comparisons!

Discussion

The differences in asymmetry between perturbation levels are not discussed. Both for explicit and implicit adaptation, some unexpected responses are seen at low or high perturbation levels.

The reason why post-adaptation changes were only significant in the last 30 seconds is not clear. Were there noticeable changes in their gait pattern following the FES? What was the subjective perception after removing the FES?

What was the amount of perturbation in relation to the baseline time period between heel strikes? Generally, we refer to perturbations as a ratio to baseline parameters – if you can provide information about the size of the ratio between the legs, that might help to interpret how small or large the perturbation was in relation to other studies.

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Reviewer #2: Yes: Nicholas D'Cruz

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PLoS One. 2024 Oct 18;19(10):e0312285. doi: 10.1371/journal.pone.0312285.r002

Author response to Decision Letter 0

1 Sep 2024

Response to Reviewer's Comments

===============================

We would like to thank the reviewers for their valuable comments. The reviewers’ comments are listed below in black, and the authors’ response is blue.

Reviewer #1: General Comments

>>We agreed that the reviewer raised an important point. The gait cycle duration changes with walking speed, so we did not quantitatively analyze the variability in gait cycle duration across all the subjects. However, based on our measurements, the average gait cycle duration was 1339 ± 40 ms, and the offset ∆τ of 0~100 mm then represents roughly 0 to 7.5% of the gait cycle duration. Although the 20 ms offset time increment (roughly 1.5% of gait cycle duration) doesn’t correspond to the same fraction (%) of the gait cycle duration among subjects, the changes in gait asymmetric patterns occurred in response to FES because the subjects synchronized their gait phase with the stimulation timing. In a future study with a more rigorous protocol, we could apply the offset time as a percentage of each individual’s gait cycle duration. We have added this concern as an additional limitation in the Discussion section, which now reads:

“… due to variations in walking speed and gait styles among the subjects, the range of the offset time (∆τ) did not correspond to the exact percentage time of the gait cycle duration across all the subjects. If gait favorably entrains to a particular percentage of the gait cycle duration, then the offset time should be adjusted based on a exact percentage time of each individual’s gait cycle duration, rather than using an absolute time for more significant results”

>>We thank the reviewer for raising this question. Although it would be interesting to quantitatively examine how an individual’s baseline asymmetry tendency affects the directional tendency of changes in gait symmetry in response to FES, we do not believe we would find any significant trends. Our previous experiences indicate that baseline asymmetry tendencies are not consistent even for the same subject (for example, the direction of baseline asymmetry is not consistent for different trials). However, we do not rule out the possible effects of baseline asymmetry on the main results, and a more rigorous study could address this. We have added this point in the Discussion section, which now reads:

“… this study did not explore how subjects’ inherent baseline inherent asymmetry tendencies might affect the directional changes in gait symmetries in response to FES. Although the baseline asymmetry’s statistical significance is negligible, it would be valuable to investigate this further.”

Specific Comments

(1) In Fig. 2A, the step length scale might be incorrect: (cm) → (mm)?

>>We thank the reviewer. We have corrected the typo.

Abstract

Line 23: Is the aim of the study to improve or disrupt gait symmetry?

>>The study aimed to explore the potential of using FES as a perturbation method during walking to promote gait asymmetry adaptation, with the long-term goal of improving gait asymmetry. We have revised the sentence to clarify the objective, which now reads:

“This study explored the potential of using functional electrical stimulation (FES) as a perturbation method during treadmill walking to promote gait symmetry adaptation by investigating whether the FES perturbation paradigm could induce gait symmetry adaptation concerning spatial and temporal gait patterns in healthy subjects”

Line 29: Perhaps helpful to mention that the explicit trial was performed in another session.

>>We have revised the sentence by clearly mentioning two trials (implicit and explicit), which now reads:

“Subjects participated in two trials: implicit and explicit. In the implicit trial, they walked comfortably during FES perturbation without consciously adjusting their gait. In the explicit trial, they voluntarily synchronized their toe-off phase to the stimulation timing.”

>>Although the observed changes in temporal gait symmetry in the implicit trial were not statistically significant over the entire varying perturbation levels (-20 ~ -100 ms), there were partial significant differences compared to the baseline symmetry (Fig. 6B bottom). We are sorry for the confusion, and we agree with the reviewer that the results should be clearly and accurately described in the Abstract. Accordingly, we have revised the sentence, which now reads:

“In this study, during the explicit trial, subjects adapted their gait patterns to the electrical pulses, resulting in a directional change in stance time (temporal) symmetry, with the left stance becoming shorter than the right. The stance time asymmetry induced by FES perturbation showed a slight residual effect. In the implicit trial, the directional change trend was slightly observed but not statistically significant.”

>>We thank the reviewer for bringing up an interesting point. Our original intention was to make the right-toe-off phase occur slightly earlier than usual, so we naturally focused on interpreting the observed change relative to the right side in comparison to the other side. We have revised our interpretation as suggested by the reviewer, throughout the manuscript.

Line 38: Implications should be focused on the explicit response, as the implicit response was rather weak and inconsistent.

>>We have revised the sentence by adding the following statement:

“The implicit condition showed a similar slight trend but was not consistently statistically significant”

Introduction:

>>We appreciate the valuable comments from the reviewer. Initially, we anticipated significant changes in gait symmetries under both explicit and implicit conditions. However, our experimental results showed minimal significant changes in the implicit conditions for various reasons. Instead of reporting only the explicit condition results, we decided to include findings from both conditions, as we believe it is still valuable to document the weak cases given that our study explored a novel method for inducing gait symmetry adaptation through FES.

Following the reviewer’s suggestion, we have revised the Introduction to include statements about the potential use FES for explicit adaptation, etc. The revised text now reads:

“… We investigated whether such a perturbation paradigm utilizing FES could induce changes in spatial and temporal gait patterns as subjects voluntarily synchronized a certain gait phase of both legs with the perturbations (explicit condition). Motor learning includes a form of learning process known as use-dependent plasticity, which involves developing movement biases that favor repeated movement directions (17)…”

>> We have included a statement in the Discussion section that outlines the potential advantages of using FES over visual or auditory cues. The added text now reads:

“Perturbation-based training heavily relies on sensory inputs to provoke adaptive responses (27), with the option of using different types of perturbations. For example, visual or auditory cues can be employed as perturbations to engage corresponding sensory information in training. However, we believe that FES offers a simple and cost-effective way to introduce external perturbations during walking. FES not only disrupts gait patterns but also affects the somatosensory pathway, both directly and indirectly, during gait adaptation, leveraging brain plasticity to reshape the neural circuits involved in this process (14,28).”

Methods:

Kindly mention that the treadmill was a split-belt treadmill.

>>Although this study used a split-belt treadmill, both belts operated at the same speed, functioning like a traditional treadmill. Therefore, we chose not to mention the use of a split-belt treadmill to avoid any potential confusion.

>> The intensity of FES was mild, resulting in only slightly noticeable ankle movement and a tingling sensation. During the explicit trial, subjects were asked to voluntarily synchronize their toe-off phase with the stimulation, as the slight ankle plantarflexion induced by FES was expected to resemble the ankle motion at toe-off. However, there might be some variability in the alignment of the gait phase with the stimulation, with some instances occurring slightly before or after the toe-off phase.

>> The stimulation occurred at a present rate (i.e., at the same interval as the initial stride duration) irrespective of whether the left leg was in toe-off or not. We have provided additional clarification and revised the sentence, which now reads:

“During the perturbation period, we administered electrical pulses (0.12-second duration, 200 µs biphasic pulses at 90 Hz, 20-25 mA intensity) to both the right and left legs, at the same period of the baseline stride duration. In other words, periodic electrical stimulation was applied to each leg independently, but the stimulations were not delivered simultaneously to both legs; there was a time interval of τ between the stimulations.”

>> In this study, we focused on analyzing gait symmetry between the right and left measurements. Although the exact timing of heel-strike may slightly differ between our measurement and others, such as those taken with a force plate, we believe that the symmetry measurement will remain unaffected. We were not able to use force plate, as the instrumental treadmill used in this study was not equipped with force plate.

Statistics – were all the outcomes normally distributed and did the models fit the data well?

>>We tested for normality using the Kolmogorov-Smirnov method (SPSS), and the null hypothesis was not rejected, indicating that the data are approximately normally distributed.

The reviewer may have a different opinion, but regardless of the normality test results, we believe that non-parametric statistical methods are not deemed necessary in this study. Although our sample size is not large enough, it falls within the typical range commonly used in similar studies investigating gait adaptation. Also, the decision against non-parametric analysis is supported by the understanding that non-parametric methods come with their own set of assumptions.

Statistics Line 202 – Typically, post-hoc t-tests are only performed if there is a significant effect in the repeated measures ANOVA. Otherwise you run into multiple comparison problems.

>>We agreed with the reviewer on this point and appreciate this feedback. We revisited our statistical analysis and conducted pairwise comparisons following the ANOVA. The manuscript has been revised accordingly in the Result section.

Results:

Figures 3 (Explicit) and 6 (Implicit) Asymmetry – the scales on the axis of the figures are different. Kindly harmonize.

>>We have revised Figure 6B to match the scale of figure 3.

>>We appreciate the reviewer’s suggestion. We have edited the Results section to make it clearer and more concise by deleting redundant sentences.

>>We understand and appreciate the reviewer’s feedback. For our statistical analysis using ANOVA, we included only the data observed during the perturbation, excluding the baseline data, as our focus was to determine how increasing perturbation levels affect changes in symmetry magnitude. Therefore, we retained the paired t-test analysis comparing with the baseline, primarily to emphasize that the asymmetry observed in the explicit trail resulted from the perturbation.

Discussion:

The differences in asymmetry between perturbation levels are not discussed. Both for explicit and implicit adaptation, some unexpected responses are seen at low or high perturbation levels.

>> The unexpected responses observed at the lowest perturbation level in the explicit condition might be due to subjects initially struggling to align their gait phase with the timing of perturbations. On the other hand, the unexpected responses at the highest perturbation in the implicit condition might result from subjects’ gait phase not being consistently entrained during the perturbation level. We have added a sentence describing the tendency of increasing stance duration symmetry with higher perturbation levels (explicit trial only), which now reads:

“Overall, an increase in stance duration as

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PLoS One. doi: 10.1371/journal.pone.0312285.r003

Decision Letter 1

Kei Masani

25 Sep 2024

PONE-D-24-11792R1Adapting spatiotemporal gait symmetry to functional electrical stimulation during treadmill walkingPLOS ONE

Dear Dr. Kim,

Please address the minor edits suggested by Reviewer 2 to further enhance the clarity of your manuscript.

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Please address the minor edits suggested by Reviewer 2 to further enhance the clarity of your manuscript.

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Reviewers' comments:

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Reviewer #2: All comments have been addressed

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Reviewer #2: Yes

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Reviewer #2: Yes

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Reviewer #2: Yes

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6. Review Comments to the Author

Reviewer #1: (No Response)

Reviewer #2: Thanks for taking on the feedback positively and for adapting the manuscript!

Some small things - I noticed that the abstract in the manuscript submission system is not adapted to reflect the changes made. There is also still some incongruency between the first paragraph of the discussion and the abstract, in regard to whether the perturbation induces gait symmetry or asymmetry adaptations. Apart from these textual edits, I have no concerns that should keep this from being published.

Congratulations and all the best!

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PLoS One. 2024 Oct 18;19(10):e0312285. doi: 10.1371/journal.pone.0312285.r004

Author response to Decision Letter 1

27 Sep 2024

Response to Reviewer's Comments

===============================

We would like to thank the reviewers for their valuable comments.

Reviewer #1: Reviewer #2: Thanks for taking on the feedback positively and for adapting the manuscript!

Some small things - I noticed that the abstract in the manuscript submission system is not adapted to reflect the changes made.

>> Thank you for the information. Honestly, we're unsure why the changes we made didn't reflect in the revised PDF. We hope that this time, the submission system will correctly update the abstract with the revisions.

There is also still some incongruency between the first paragraph of the discussion and the abstract, in regard to whether the perturbation induces gait symmetry or asymmetry adaptations. Apart from these textual edits, I have no concerns that should keep this from being published.

>> We aimed to induce gait asymmetry during training through FES perturbation, ultimately facilitating the adaptation of asymmetric gait patterns. We have revised the first sentence of the Discussion, which now reads:

“In this study, we proposed a novel approach to utilizing FES as a perturbation method for altering symmetric gait patterns and evaluated the potential benefits of the FES perturbation by examining the extent of spatiotemporal gait asymmetry adaptation during treadmill walking.”

Congratulations and all the best!

>> Thank you for taking the time to review our manuscript. We greatly appreciate your feedback, which has helped us make significant improvements.

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PLoS One. doi: 10.1371/journal.pone.0312285.r005

Decision Letter 2

Kei Masani

4 Oct 2024

Adapting spatiotemporal gait symmetry to functional electrical stimulation during treadmill walking

PONE-D-24-11792R2

Dear Dr. Kim,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Kei Masani

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0312285.r006

Acceptance letter

Kei Masani

8 Oct 2024

PONE-D-24-11792R2

PLOS ONE

Dear Dr. Kim,

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

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Data Availability Statement

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PERMALINK

Adapting spatiotemporal gait symmetry to functional electrical stimulation during treadmill walking

Seung-Jae Kim

Alex Worthy

Brandom Lee

Setareh Jafari

Olivia Dyke

Jeonghee Cho

Elijah Brown

Roles

Abstract

Introduction

Methods

A. Subjects

B. Experimental setup

Fig 1.

C. Experimental protocol

D. Data analysis

Results

Fig 2.

Fig 3.

Fig 4.

Fig 5.

Fig 6.

Discussion

Effects of FES-induced perturbations on temporal gait asymmetry adaptation (explicit trial)

Effects of FES-induced perturbations on spatial gait asymmetry adaptation (explicit trial)

Effects of FES perturbations under implicit condition

Limitations and further direction

Conclusion

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

Kei Masani

Roles

Author response to Decision Letter 0

Decision Letter 1

Kei Masani

Roles

Author response to Decision Letter 1

Decision Letter 2

Kei Masani

Roles

Acceptance letter

Kei Masani

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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