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Influence of Treadmill Speed and Perturbation Intensity on Selection of Balancing Strategies during Slow Walking Perturbed in the Frontal Plane

Influence of Treadmill Speed and Perturbation Intensity on Selection of Balancing Strategies... Hindawi Applied Bionics and Biomechanics Volume 2019, Article ID 1046459, 14 pages https://doi.org/10.1155/2019/1046459 Research Article Influence of Treadmill Speed and Perturbation Intensity on Selection of Balancing Strategies during Slow Walking Perturbed in the Frontal Plane Zlatko Matjačić , Matjaž Zadravec, and Andrej Olenšek University Rehabilitation Institute, Republic of Slovenia, Linhartova 51, SI-1000 Ljubljana, Slovenia Correspondence should be addressed to Zlatko Matjačić; zlatko.matjacic@ir-rs.si Received 22 February 2019; Revised 8 May 2019; Accepted 16 May 2019; Published 2 June 2019 Academic Editor: Craig P. McGowan Copyright © 2019 Zlatko Matjačić et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Background. Common understanding is that adequate foot placement (stepping strategy) is crucial in maintaining stability during walking at normal speed. The aim of this study was to investigate strategies that humans use to cope with lateral perturbations during very slow walking. Methods. Ten healthy individuals underwent an experimental protocol whereby a set of perturbations directed inward (medially to a stance leg) and outward (laterally to a stance leg) of three intensities (F =5%, F =10%, and 1 2 F =15% of body weight), applied at three instances of a stance phase, were delivered in random order to the pelvis using a balance assessment robot while walking on a treadmill at three walking speeds (S =0 4, S =0 6, and S =0 8 m/s). We 1 2 3 analyzed the peak center of mass displacements; step length, step width, and step times; and the lateral component of ground reaction force for perturbations that were delivered at the beginning of the gait cycle. Results. Responses after inward perturbations were similar at all tested speeds and consistently employed stepping strategy that was further facilitated by a shortened stance. Wider and shorter steps were applied with increased perturbation intensity. Responses following outward perturbations were more complex. At S , hip strategy (impulse-like increase of mediolateral ground reaction force) augmented with ankle strategy (mediolateral shift of the center of pressure) mainly contributed to responses already during the stance phase. The stance duration was significantly longer for all perturbation intensities. At S , the relative share of hip strategy was reduced while with increased perturbation intensity, stepping strategy was gradually added. The stance duration was significantly longer for F and F .At S , stepping strategy was mainly used while the duration of stance was similar to 1 2 3 the one in unperturbed walking. Responses following both inward and outward perturbations at all speeds were characterized by temporary slowing down movement in a sagittal plane that was more pronounced with increased perturbation intensity. Conclusions. This study provides novel insights into balancing strategies used at slower walking speeds which may be more relevant to understand the challenges of gait stability following perturbations in the frontal plane in clinical populations. 1. Introduction Likewise, following a perturbation that may be imposed by various perturbation modalities, for example, (i) as a push An essential component of bipedal walking is maintenance of at the waist level, mimicking a sudden bump into another dynamic balance, particularly in the frontal plane [1]. The person in a crowd [4–7], (ii) as a movement of the support main mechanism used in normal unperturbed human walk- surface, mimicking a slip [8], and (iii) as a pull on the foot ing has been explained through the inverted pendulum of the swinging leg, mimicking a trip [9], the main balancing model and is related to adequate placement of the swinging strategy used was related to the placement of the swinging limb onto a new stance location [2]. This changes the base limb onto an adequate location [3, 10, 11]. Stepping was of support (BOS) and provides appropriate development of additionally augmented by the “ankle strategy,” which is the lateral component of ground reaction force to ensure sta- related to the activity of ankle musculature to displace the ble side-to-side movement of the center of mass (COM) [3]. center of pressure (COP) under the stance leg in the direction 2 Applied Bionics and Biomechanics the interplay of strategies that humans use to cope with the of the action of perturbation [12, 13]. Additionally, for per- turbations acting in the inward direction (medially relative consequences of an unexpected lateral perturbation. to the stance leg in case of perturbing pushes to the waist), the swing time was shortened to facilitate earlier application 2. Methods of balance correction in the next step [4, 6]. However, for the perturbations acting in the outward direction (laterally 2.1. Subjects. Ten healthy males without known history of relative to the stance leg in case of perturbing pushes to the neuromuscular or orthopedic problems (age: 31 ± 5 years, waist), shortening of the swing phase has not been observed height: 180 ± 3 9cm, and mass: 78 7±6 5kg) participated [4, 6]. Several studies have also pointed out that in sessions in this study after signing informed consent forms. The sub- where perturbations in the frontal plane were delivered sub- jects represent a sample of convenience. The study was jects adopted wider stepping as an additional stabilizing mea- approved by the Slovenian National Ethics Committee. sure, compared to sessions without perturbations [14, 15]. The above referenced studies examined dynamic reactions 2.2. Instrumentation. Figure 1 shows the experimental envi- to perturbations that were imposed during walking in a range ronment, which consisted of a balance assessment robot of speeds that are normally used (0.8–1.2 m/s). and an instrumented treadmill (BART). Here, only a brief Various diseases or injuries to the central nervous sys- description of the experimental setup is given, as a more tem (CNS) result in substantially reduced motor capabilities detailed description is provided elsewhere [6, 7]. The BART in clinical cases. For example, after completion of clinical interfaces with the pelvis of a walking participant with six rehabilitation, the majority of stroke survivors walk with degrees of freedom (DOF). Five of the DOFs (translation speeds that range from 0.4 to 0.8 m/s [16]. Our knowledge of the pelvis in the sagittal, lateral, and vertical directions; of balancing mechanisms used following perturbations at pelvic rotation; and pelvic list) are actuated and admit- these lower speeds of walking is scarce. One consequence tance-controlled, providing transparent haptic interaction of slower walking is that swing times are longer. Thus, for with negligible power transfer [7]. The sixth DOF (pelvic example, if a perturbation is imposed during a double sup- tilt) is passive. The BAR-TM is capable of delivering pertur- port phase, which would resemble a situation of a slip on bations in the forward/backward and left/right directions. the floor [8], it may be the case that a corrective action com- In this study, we only considered inward and outward ing from a wider/narrower next step, which inevitably acts perturbations delivered in the frontal plane as depicted in with considerable delay against the induced instability [4], Figure 1. would not be sufficient to successfully correct for the pertur- COM movement was estimated from the translational bation. Thus, corrective actions may be required to start movement of the subjects’ pelvis and assessed from the already during the stance phase. Apart from using ankle movement of the BAR-TM, similarly as in our previous strategy under the stance leg that can act fast against pertur- studies [7, 18]. Recordings of the ground reaction force bation but has limited stabilizing effect due to a narrow foot (GRF) and COP in the transversal plane during walking width [4, 13], additional strategy related to counter-rotation were obtained by means of four force transducers of body segments, termed as “inertial strategy” [12], which is (K3D120, ME Systeme GmbH) placed underneath the tread- frequently used during one-leg standing [17], may be uti- mill. Spatiotemporal data were assessed by means of an lized during slow walking. The most notable example of OptiTrack camera (NaturalPoint Inc.). Passive reflective inertial strategy is related to the pelvis and trunk rotation markers were placed on the participants’ feet (on the medial and has been termed as “hip strategy” [12, 17]. In our previ- malleoli and the first and fourth metatarsal joints) [7, 18]. ous work with a selected neurologically intact subject walk- Sampling frequency for the kinematic and kinetic data was ing at the speed of 0.4 m/s, we observed that an important 50 Hz which is considered to be adequate for this type of contribution to the balancing response after an outward per- study [20]. turbing push was a hip strategy related to the activity of hip abductors of the stance leg [18]. Vlutters et al. [19] have also 2.3. Experimental Protocol. The experimental protocol is observed important activity of the gluteus medius muscle of shown schematically in Figure 2. First, subjects walked at a the stance leg following outward pushes at walking speed of treadmill speed set to 0.4 m/s for a period of three minute- 0.6 m/s. On the other hand, studies from Hof et al. [4] and s—unperturbed walking session. This was followed by a Vlutters et al. [19] where pelvis perturbations of similar period of around half an hour of perturbed walking—per- intensity were applied in the frontal plane at walking speed turbed walking session. These two experimental blocks were of 1.2 m/s have not observed use of hip strategy. This indi- then repeated for treadmill speeds of 0.6 m/s and 0.8 m/s. The cates that walking speed may have a considerable influence whole protocol was done in a single day and took around 2 on the selection of a suitable balancing strategy or a synergy hours. Perturbations were delivered with a randomly varied of balancing strategies following perturbations applied in the pause that ranged from six to eight seconds in order to avoid frontal plane. predictability of the perturbation occurrence. Four perturba- The aim of this study was to systematically investigate the tion directions (outward RR and LL and inward RL and LR), kinematics and kinetics of reactive dynamic balancing at var- three perturbation onsets (at 0%, 30%, and 60% of the stance ious speeds of slower walking and at various intensities of phase of a gait cycle), and three perturbation amplitudes (5%, inward- and outward-directed perturbing pushes applied at 10%, and 15% of body weight) were varied. Each combina- the waist at the beginning of the stance phase, to elucidate tion of perturbation parameters was repeated seven times. Applied Bionics and Biomechanics 3 RR RL LL LR AP ML (a) (b) Figure 1: Photo of a subject walking on an instrumented treadmill while being embraced by the BAR-TM perturbing device; projection on the wall shows the middle of the BAR-TM working space as well as the current position and orientation of the pelvis in a transverse plane—the subjects were instructed to return to the middle of the BAR-TM working space after they rejected perturbation (a). Top view illustration of perturbation directions: outward RR: perturbation to the right triggered at right-foot contact; inward RL: perturbation to the left triggered at right-foot contact; outward LL: perturbation to the left triggered at left-foot contact; inward LR: perturbation to the right triggered at left-foot contact (b). Unperturbed Perturbed Unperturbed Perturbed Unperturbed Perturbed walking walking walking walking walking walking 252 random perturbations 252 random perturbations 252 random perturbations (3 min) Rest (3 min) (3 min) Rest (30 min) (30 min) (30 min) (5 min) (3 min) S = 0.4 m/s S = 0.6 m/s S = 0.8 m/s 1 2 3 Figure 2: Schematic diagram of the experimental protocol. This yielded a total of 252 perturbing pushes at each walking seven repetitions. We also averaged spatiotemporal parame- speed that were block-randomized. Perturbations took the ters for unperturbed walking in unperturbed walking sessions and unperturbed walking (the periods between the complete form of a force impulse lasting 150 ms [6, 7, 18]. Prior to this study, all subjects visited our laboratory where they practiced recoveries from previous perturbation until the onset of the unperturbed and perturbed walking on the BAR-TM system next perturbation) in the perturbed walking sessions at each tested treadmill speed. for approximately half an hour. Although we assessed postural responses at three levels of 2.4. Measurements and Data Analysis. The COM, COP, and perturbation onset, we included in further analysis only per- GRF were first segmented into strides with the gait cycle turbations that commenced at 0% of a gait cycle. defined as the period between two consecutive left (for LL The following data were used as outcome measures: step and LR responses) or right (for RR and RL responses) heel lengths, step widths, and step times for perturbed (we strikes, as detected from COP and COP signals. Two full analyzed the first step after the perturbation onset which ML AP gait cycles, half of a cycle prior to and one and a half cycles determines the “stepping” response) and unperturbed exper- after the onset of perturbation, were analyzed. Spatiotem- imental conditions; peak displacements of COM within the poral responses were investigated in terms of step length, first stride (from 0% to 100% of the gait cycle) in sagittal step width, and step time where left (right) step length (COM ) and frontal planes (COM ); and integral AP peak ML peak was taken to be the anterio-posterior distance between of the lateral component of GRF (GRF ) for the ML impulse ankle markers at the moment of left (right) foot strike period of the first stance phase (from 0% to approx. 50% while left (right) step width was defined as the mediolat- of a gait cycle) (“in-stance response”) and for the period eral distance between the same markers. Step times were of the second stance phase (from approx. 50% to 100% of a gait cycle) (“stepping response”). Thus, the “in-stance defined as the time elapsed between two consecutive left (right) and right (left) foot strikes. In each combination response” period encompassed the balancing activity prior of perturbation parameters, COM, COP, and GRF trajec- to the first step after the onset of perturbation, while the tories and spatiotemporal parameters were averaged across “stepping response” period encompassed the balancing 4 Applied Bionics and Biomechanics activity between the first and the second steps after the At a walking speed of 0.6 m/s, we can observe increased onset of perturbation. Since GRF determines the acceler- lateral displacement of COP in the “in-stance” period ML ML ation of COM , the GRF provides a measure of while the impulse-like rise in GRF in the first half of the ML ML impulse ML the overall balancing activity in both “in-stance” and “step- “in-stance” period was smaller in comparison to those at ping” periods of balance responses. walking speed 0.4 m/s. Medial displacement of COP and ML related decrease in GRF were observed in the “stepping” ML period for the perturbation intensity of 15%. 2.5. Statistical Analysis. For unperturbed walking, a two-way At a walking speed of 0.8 m/s, increased lateral displace- repeated measures analysis of variance (rmANOVA) was ment of COP in the “in-stance” period was observed while ML used to test for the main effects and interactions on step the impulse-like rise in the GRF in the first half of the “in- ML length, step width, and step time between walking speed (3 stance” period was not present. In the second half of the same levels: 0.4, 0.6, and 0.8 m/s) and walking condition (2 levels: period, there was a gradual decrease of GRF with increas- ML unperturbed walking during unperturbed walking sessions ing perturbation intensity followed by a progressively larger and unperturbed walking during perturbed walking ses- medial displacement of COP and related decrease in ML sions). When a significant main effect or interaction was GRF in the “stepping” period. ML found, we performed post hoc pairwise comparisons for each of the walking speeds separately. A significance level of 0.05 (2) Sagittal Plane. At walking speed of 0.4 m/s, COP was AP was used. displaced increasingly forward in the first half of the stance For perturbed walking, a two-way rmANOVA was with increasing intensity of perturbation while GRF AP used to test for the main effects and interactions on step showed increased braking action that decelerated COM AP length, step width, step time, COM , COM , ML peak AP peak in relation to unperturbed walking. Slowing down of COM AP and GRF between walking speed (3 levels: 0.4, 0.6, ML impulse and associated changes in COP were progressively smaller AP and 0.8 m/s) and perturbation amplitude (4 levels: 0% at walking speeds of 0.6 m/s and 0.8 m/s compared to those (unperturbed strides from perturbed sessions), 5%, 10%, observed at the speed of 0.4 m/s. and 15% of body weight). When a significant main effect or interaction was found, we performed post hoc pairwise com- 3.1.2. Inward Perturbations. Figure 4 shows COP, COM, and parisons versus unperturbed walking for each of the walking GRF responses to inward perturbations (RL) for all three speeds separately. A significance level of 0.05 was used, and a tested walking speeds and for all three tested perturbation Bonferroni correction was applied to correct for multiple intensities for a representative subject. The responses look comparisons (0.016). similar across the tested walking speeds. (1) Frontal Plane. In the “in-stance” period, no noticeable 3. Results difference can be observed in COP , COM , and GRF ML ML ML The results for pushes RR (outward perturbation) and RL in relation to unperturbed walking except for a shortened (inward perturbation) are presented in this section. The duration of the stance phase. The dominant balancing effects of pushes to both outward directions (LL and RR) response can be observed in the “stepping” period where were comparable. Likewise, the effects of pushes to both depending on the perturbation intensity COP was shifted ML inward directions (LR and RL) were comparable. laterally which was accompanied with a progressively increased GRF . ML 3.1. Dynamic Balancing Responses following Perturbations (2) Sagittal Plane. In the second part of the “in-stance” 3.1.1. Outward Perturbations. Figure 3 shows COP, COM, period, a shortened posterior displacement of COP can AP and GRF responses to outward perturbations (RR) for all be observed. Consequently, GRF was also reduced thus AP three tested walking speeds and for all three tested perturba- slowing down movement of COM . Throughout the “step- AP tion intensities for a representative subject. ping” period, a smaller anterior displacement of COP can AP be seen with accompanying reduction of GRF which AP (1) Frontal Plane. At a walking speed of 0.4 m/s, we can enabled COM to catch up with the relative position of AP observe increased lateral displacement of COP in the “in- COM on the treadmill that the subject assumed before ML AP stance” period of the response (from 0% to approx. 50% of the action of perturbation. a gait cycle) in relation to unperturbed walking. An impulse-like rise in the GRF can be seen in the first half 3.2. Peak COM Displacements. Figure 5 shows peak excur- ML of the stance that is similar for all three intensities and acts sions of COM and COM for both outward (RR) and ML AP in the direction opposite to the perturbation. Perturbation inward (RL) perturbations. COM following out- ML peak was fully contained during the “in-stance” period for pertur- ward perturbation was significantly affected by the speed bation intensities of 5% and 10% while following a perturba- of walking (F 2, 18 =10 015, p =0 001), the perturbation tion intensity of 15%, there was medial displacement of intensity (F 3, 27 = 274 194, p <0 001), and their interac- COP and related decrease in GRF in the “stepping tion (F 6, 54 =9 790, p <0 001). Post hoc analysis has ML ML period” (from approx. 50% to approx. 100% of a gait cycle) shown significantly larger peak COM displacements ML that finally contained the instability. for all intensities and at all speeds in comparison to Applied Bionics and Biomechanics 5 S = 0.4 m/s S = 0.6 m/s S = 0.8 m/s 1 2 3 200 200 200 100 100 100 00 0 −100 −100 −100 −200 −200 −200 COP COM 100 100 100 50 50 50 0 0 0 −50 −50 −50 −100 −100 −100 200 200 200 100 100 100 0 0 0 −100 −100 −100 −200 −200 −200 Time (s) Time (s) Time (s) −0.5 0 0.5 1 1.5 2 2.5 −0.5 0 0.5 1 1.5 2 2.5 −0.5 0 0.5 1 1.5 100 100 100 50 50 50 0 0 0 −50 −50 −50 −100 −100 −100 −50 050 100 150 −50 0 50 100 150 −50 0 50 100 150 % gait cycle % gait cycle % gait cycle AP In-stance Stepping RR ML Perturbation interval F = 10% BW Unperturbed gait F = 15% BW F = 5% BW Figure 3: Kinematics and kinetics of balancing responses following outward RR perturbation assessed in a representative subject. The first row shows the trajectories of COP (solid lines) and COM (dotted lines), while the second row shows GRF trajectories. The third ML ML ML row shows COP (solid lines) and COM (dotted lines) trajectories, while the fourth row shows GRF trajectories. Each graph AP AP AP contains responses to all three perturbation intensities along with the trajectories assessed during the unperturbed walking sessions. The left, middle, and right columns show the balancing responses at speeds S , S , and S , respectively. Half a stride prior to and one and a half 1 2 3 strides following the perturbation commencement are shown. A stride is defined as the period between two consecutive right-foot contacts. The trajectories displayed show mean values of seven balancing responses. p =0 unperturbed walking. COM following outward per- 352). Post hoc analysis has shown significantly larger AP peak turbation was significantly affected by the speed of walking peak COM displacements for majority of intensities at all ML (F 2, 18 =69 523, p <0 001), the perturbation intensity speeds in comparison to unperturbed walking. (F 3, 27 =88 255, p <0 001), and their interaction (F 6, 54 =5 551, p <0 001). Post hoc analysis has shown 3.3. Spatiotemporal Parameters. Figure 6 shows spatiotempo- significantly larger peak COM displacements for all inten- ral parameters for unperturbed walking during the unper- AP sities and at all speeds in comparison to unperturbed walk- turbed walking sessions (UWS) and for unperturbed ing. COM following inward perturbation was walking during the perturbed walking sessions (PWS). Step ML peak significantly affected by the intensity of perturbation lengths and step times were significantly affected only by (F 3, 27 =53 150, p <0 001) and interaction between inten- the walking speed (step length F 2, 18 =354 221, p <0 001; sity and speed (F 6, 54 =3 556, p =0 005) but not by the step time F 2, 18 = 238 195, p <0 001) but not by the walk- speed of walking (F 2, 18 =3 088, p =0 070). Post hoc anal- ing condition (step length F 1, 9 =3 089, p =0 113; step ysis has shown significantly larger peak COM displace- time F 1, 9 =4 822, p =0 056) nor the interaction between ML ments for all intensities and at all speeds in comparison to the walking condition and the walking speed (step length unperturbed walking. COM following inward pertur- F 2, 18 =1 304, p =0 296; step time F 2, 18 =2 866, p = AP peak bation was significantly affected only by the perturbation 0 083). Step lengths increased with increased walking speed intensity (F 3, 27 =18 892, p <0 001) but not by the walk- while the step times decreased with increased walking ing speed (F 2, 18 =1 620, p =0 225) nor the interaction speed. Step widths were significantly affected by walking between the intensity and walking speed (F 6, 54 =1 140, speed (F 2, 18 =4 996, p =0 019) and walking condition GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML 6 Applied Bionics and Biomechanics S = 0.4 m/s S = 0.6 m/s S = 0.8 m/s 1 2 3 200 200 200 100 100 100 00 0 −100 −100 −100 −200 −200 −200 COP COM 100 100 100 50 50 50 0 0 0 −50 −50 −50 −100 −100 −100 200 200 200 100 100 100 0 0 0 −100 −100 −100 −200 −200 −200 Time (s) Time (s) Time (s) −0.5 0 0.5 1 1.5 2 2.5 −0.5 0 0.5 1 1.5 2 2.5 −0.5 0 0.5 1 1.5 100 100 100 50 50 50 0 0 0 −50 −50 −50 −100 −100 −100 −50 050 100 150 −50 0 50 100 150 −50 0 50 100 150 % gait cycle % gait cycle % gait cycle AP RL In-stance Stepping ML Perturbation interval F = 10% BW Unperturbed gait F = 15% BW F = 5% BW Figure 4: Kinematics and kinetics of balancing responses following inward RL perturbation assessed in a representative subject. The first row shows the trajectories of COP (solid lines) and COM (dotted lines), while the second row shows GRF trajectories. The third row ML ML ML shows COP (solid lines) and COM (dotted lines) trajectories, while the fourth row shows GRF trajectories. Each graph contains AP AP AP responses to all three perturbation intensities along with the trajectories assessed during the unperturbed walking sessions. The left, middle, and right columns show the balancing responses at speeds S , S , and S , respectively. Half a stride prior to and one and a half 1 2 3 strides following the perturbation commencement are shown. A stride is defined as the period between two consecutive right-foot contacts. The trajectories displayed show mean values of seven balancing responses. 5% and 10% while at 0.8 m/s, significantly shorter steps were (F 1, 9 =70 489, p <0 001) but not by interaction of the two (F 2, 18 =0 830, p =0 452). Post hoc analysis has made at a perturbation intensity of 15% in comparison to shown that the difference between step widths of unper- unperturbed walking. Post hoc analysis further revealed that turbed walking during unperturbed walking sessions and step widths at a walking speed of 0.4 m/s were not statisti- during perturbed walking sessions was on average 4 cm. cally different; at the walking speed of 0.6 m/s, step width at the strongest perturbation was significantly smaller in Figure 7 shows spatiotemporal parameters for perturbed walking following outward (RR) and inward (RL) perturba- comparison to unperturbed walking while at a walking tions. Step lengths, step widths, and step times following out- speed of 0.8 m/s, step widths for all intensities were signifi- ward perturbation were significantly affected by the walking cantly smaller in comparison to unperturbed walking. Post speed (step length F 2, 18 =38 259, p <0 001; step width hoc analysis for step times has shown significantly longer steps at 0.4 m/s for all intensities in comparison to unper- F 2, 18 =8 869, p =0 002; and step time F 2, 18 = 153 168, p <0 001), by intensity (step length F 3, 27 = turbed walking; at 0.6 m/s, this was the case for intensities 6 721, p =0 002; step width F 3, 27 =51 945, p <0 001; of 5% and 10% while at 0.8 m/s, the step time for an inten- and step time F 3, 27 =12 214, p <0 001), and by interac- sity of 10% was significantly longer in comparison to unper- tion of both factors (step length F 6, 54 =5 407, p <0 001; turbed walking. step width F 6, 54 =12 023, p <0 001; and step time F 6, Step lengths and step times following inward perturba- 54 =13 333, p <0 001). Post hoc analysis showed no signif- tion were significantly affected by the walking speed (step icant differences in step lengths at 0.4 m/s; at 0.6 m/s, signifi- length F 2, 18 =43 703, p <0 001; step time F 2, 18 = cantly longer steps were taken at perturbation intensities of 75 724, p <0 001) but not the step width (F 2, 18 =3 085, GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML Applied Bionics and Biomechanics 7 Speed: p = 0.001 Force: p < 0.001 Interaction: p < 0.001 150 0 ⁎ ⁎ 100 −50 50 −100 Speed: p < 0.001 Force: p < 0.001 Interaction: p = 0.001 0 −150 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) (a) 0 0 −50 −50 Speed: p < 0.225 Force: p < 0.001 Interaction: p = 0.352 −100 −100 Speed: p = 0.07 Force: p < 0.001 Interaction: p = 0.005 −150 −150 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) (b) Unperturbed gait F = 10% BW F = 5% BW F = 15% BW 1 3 Figure 5: Group average (±standard deviation) of peak COM and COM excursions across the three walking speeds during unperturbed ML AP walking and perturbed walking is shown for outward RR (a) and inward RL (b) perturbations along with the p values of 2-way rmANOVA. Asterisks ( ) indicate significant difference from unperturbed walking in Bonferroni post hoc pairwise comparisons (p <0 016). p =0 071). On the other hand, perturbation intensity had Post hoc analysis has shown a decrease of step lengths significant effect on step length, step width, and step time and step times and an increase of step widths with (step length F 3, 27 = 195 329, p <0 001; step width F 3, increased intensity at all tested speeds in comparison to 27 =31 060, p <0 001; and step time F 3, 27 = 361 699, unperturbed walking. p <0 001). Only step width and step time were signifi- cantly affected by interaction of both factors (step width 3.4. Lateral GRF Impulses. Figure 8 shows the integral of F 6, 54 =2 758, p =0 021; step time F 6, 54 =44 580, p < GRF over the “in-stance” and “stepping” periods of ML 0 001) and not the step length (F 6, 54 =1 103, p =0 373). dynamic responses following outward (RR) and inward RL RR COM (mm) COM (mm) ML peak ML peak COM (mm) COM (mm) AP peak AP peak 8 Applied Bionics and Biomechanics Speed: p < 0.001 Speed: p = 0.019 Speed: p < 0.001 Walking conditions: p = 0.113 Walking conditions: p < 0.001 Walking conditions: p = 0.056 Interaction: p = 0.296 Interaction: p = 0.452 Interaction: p = 0.083 600 250 1.2 ⁎ ⁎ 500 1 400 0.8 300 0.6 200 0.4 100 0.2 0 0 0 0.4 0.6 0.8 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) Walking speed (m/s) UWS PWS Figure 6: Group average (±standard deviation) of step lengths, step widths, and step times across the three walking speeds during unperturbed walking in unperturbed walking session (UWS) and during unperturbed walking in perturbed walking sessions (PWS) is shown along with the p values of 2-way rmANOVA. Asterisks ( ) indicate significant difference from unperturbed walking in post hoc pairwise comparisons (p <0 05). (RL) perturbations. GRF following outward per- for the “stepping” period at speeds of 0.4 m/s and 0.6 m/s ML impulse turbation was significantly affected by the walking speed showed significantly higher values of GRF for inten- ML impulse (“in-stance” F 2, 18 =37 079, p <0 001; “stepping” F 2, sities of 10% and 15% while at 0.8 m/s, significantly higher 18 =82 463, p <0 001), by intensity (“in-stance” F 3, 27 = values were observed for all intensities in comparison to 26 849, p <0 001; “stepping” F 3, 27 =87 569, p <0 001), unperturbed walking. and by interaction of both factors (“in-stance” F 6, 54 = 10 037, p <0 001; “stepping” F 6, 54 =24 318, p <0 001) 4. Discussion during both periods. Post hoc analysis for the “in-stance” period has shown significant increases for intensities of 5% The main aim of this study was to investigate how slower and 10% at a walking speed of 0.4 m/s while GRF walking speeds and various intensities of perturbing pushes ML impulse value at an intensity of 15% was not significantly different delivered at the heel strike influence the selection of dynamic from unperturbed walking. At 0.6 m/s, GRF values balancing responses. ML impulse at intensities of 5% and 10% were significantly increased Responses after inward perturbations were similar at all while GRF value at an intensity of 15% was signifi- tested speeds and consistently employed a predominantly ML impulse cantly decreased in comparison to unperturbed walking. At stepping strategy facilitated by a shortened stance. Wider 0.8 m/s, only GRF value at an intensity of 5% was steps and shorter stances were applied with increasing per- ML impulse significantly increased while GRF turbation strengths. The role of hip/inertial balancing strate- values at intensi- ML impulse ties of 10% and 15% were significantly decreased. Post hoc gies was not observed. These observations are well in line analysis for the “stepping” period has shown no statistically with the observations of other studies which were mostly per- significant differences among intensity factors at a walking formed at higher walking speeds [4, 5, 7, 11]. speed of 0.4 m/s. At walking speeds 0.6 m/s and 0.8 m/s, the On the contrary, when subjects were faced with outward perturbations, additional inertial balancing strategies were GRF shows increasingly smaller values with increas- ML impulse ing intensity of perturbation in comparison to unperturbed used. The predominant inertial strategy associated with the walking. counter-rotation of body segments changing GRF is the hip Following inward perturbation, GRF was signif- strategy [12, 17, 21]. Depending on the walking speed and ML impulse icantly affected in both periods by the perturbation intensity perturbation intensity, the relative contribution of individual balancing strategy also varied. At the slowest walking speed, (“in-stance” F 3, 27 =53 116, p <0 001; “stepping” F 3, 27 =28 598, p <0 001) and by interaction of both factors we consistently observed a significant contribution of hip (“in-stance” F 6, 54 =4 832, p =0 001; “stepping” F 6, 54 strategy in the first half of the “in-stance” period. The hip =7 391, p <0 001) but was not significantly affected by strategy was augmented with an ankle strategy, displacing walking speed (“in-stance” F 2, 18 =1 289, p =0 300; “step- the COP in the lateral direction away from the direction of ping” F 2, 18 =1 319, p =0 292). Post hoc analysis for the perturbation [13]. The stance duration was significantly lon- “in-stance” period at all speeds showed increasingly smaller ger for all perturbation intensities. At medium walking speed, values of GRF with increasing intensity of perturba- the hip strategy augmented with an ankle strategy was suffi- ML impulse tion in comparison to unperturbed walking. Post hoc analysis cient at the weakest perturbation magnitude while a stepping Step length (mm) Step width (mm) Step time (s) Applied Bionics and Biomechanics 9 Speed: p < 0.001 Speed: p < 0.001 Speed: p < 0.001 Force: p = 0.002 Force: p = 0.002 Force: p < 0.001 Interaction: p < 0.001 Interaction: p < 0.001 Interaction: p < 0.001 600 300 1.5 500 250 400 400 1 300 150 200 100 0.5 100 50 0 0 0 0.4 0.6 0.8 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) Walking speed (m/s) (a) Speed: p < 0.001 Speed: p = 0.071 Speed: p < 0.001 Force: p < 0.001 Force: p < 0.001 Force: p < 0.001 Interaction: p = 0.373 Interaction: p = 0.021 Interaction: p < 0.001 600 300 1.5 ⁎ ⁎ ⁎ ⁎ 500 ⁎ 400 1 200 150 ⁎ ⁎ ⁎ 100 ⁎ 100 0.5 −100 0 0 −200 0.4 0.6 0.8 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) Walking speed (m/s) (b) Unperturbed gait F = 10% BW F = 5% BW F = 15% BW Figure 7: Group average (±standard deviation) of step lengths, step widths, and step times across the three walking speeds during unperturbed walking and perturbed walking is shown for outward RR (a) and inward RL (b) perturbations along with the p values of 2- way rmANOVA. Asterisks ( ) indicate significant difference from unperturbed walking in Bonferroni post hoc pairwise comparisons (p <0 016). strategy was gradually added with increasing perturbation 4.1. Synergy of Balancing Strategies following Outward intensity. At the highest walking speed, stepping was the Perturbations. This study provides an important insight into main strategy used to counteract the effects of perturbation the balancing strategies used at walking speeds that are well while the duration of stance was similar to those in unper- below those normally used and which may be more relevant turbed walking. for understanding the challenges of gait stability following RL RR Step length (mm) Step length (mm) Step widthh (mm) Step widthh (mm) Step time (s) Step time (s) 10 Applied Bionics and Biomechanics In-stance Stepping 60 60 40 40 Speed: p < 0.001 Force: p < 0.001 Interaction: p < 0.001 20 20 0 0 −20 −20 ⁎ Speed: p < 0.001 Force: p < 0.001 −40 −40 Interaction: p < 0.001 −60 −60 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) (a) 60 60 ⁎ ⁎ 40 40 Speed: p < 0.001 Force: p < 0.001 Interaction: p < 0.001 20 20 0 0 −20 −20 ⁎ ⁎ ⁎ ⁎ −40 −40 Speed: p < 0.001 Force: p < 0.001 Interaction: p < 0.001 −60 −60 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) (b) Unperturbed gait F = 10% BW F = 5% BW F = 15% BW 1 3 Figure 8: Group average (±standard deviation) of integrals of GRF over the “in-stance” and “stepping” periods across the three walking ML speeds during unperturbed walking and perturbed walking is shown for outward RR (a) and inward RL (b) perturbations along with the p values of 2-way rmANOVA. Asterisks ( ) indicate significant difference from unperturbed walking in Bonferroni post hoc pairwise comparisons (p <0 016). perturbations in the frontal plane in clinical populations. opinion that control of human gait is predominantly This study complements the existing body of knowledge on achieved through foot placement [3–5, 7, 10]. Stepping strat- the organization of balancing responses during walking fol- egy may well be the primary and energetically wise optimal lowing perturbations acting in the frontal plane. The results coping option following perturbations at normal speeds of of this study to some extent challenge the currently accepted walking; however, the inherent time-delay associated with RR RR GRF (Ns) GRF (Ns) ML impulse ML impulse GRF (Ns) GRF (Ns) ML impulse ML impulse Applied Bionics and Biomechanics 11 swing time needed for a stepping strategy to start acting ing an outward perturbation at low walking speed in more against a perturbation after an outward perturbation is recip- details. rocal to the walking speed. This becomes critical at lower 4.2. Shortening and Prolongation of the Stance Duration as a speeds of walking in particular when the perturbation is Balancing Strategy. It was shown that humans while walking applied in early stance thus maximizing the time for instabil- at normal speeds and when subjected to larger perturbations ity to develop. Wang and Srinivasan [22] have indicated that of inward direction react more quickly by shortening their as much as 80% of the variance in deviations of foot place- stance duration so that the next step which is also a corrective ment from the average during unperturbed walking at speeds step is made earlier [4, 11]. Our results show that this is also ranging from 1 to 1.4 m/s could be explained by deviations the case for lower speeds. from the average in pelvis position and speed at midstance. However, when reacting to outward perturbations at Vlutters et al. [23] have also shown a similar correlation for lower speeds, the stance phase was in most cases substantially perturbed walking at speed of 1.2 m/s. However, a study from prolonged, thus prolonging utilization of the “in-stance” hip Stimpson et al. [24] that examined step-by-step control of strategy resulting in an increase of GRF in the first half of ML step width during unperturbed walking at speeds ranging the stance that acted in the direction opposite to the move- from 0.2 to 1.2 m/s has shown that the strength of the rela- ment of COM. tionship between the step width and pelvis mechanics is sig- nificantly reduced at lower speeds. These findings imply that 4.3. Braking of the Movement in the Plane of Progression as a utilization of adequate foot placement (stepping strategy) as Balancing Strategy. Both types of perturbation lead to tempo- the main strategy to maintain dynamic stability in the frontal rary slowing down of progression in the sagittal plane, which plane depends substantially on walking speed. Therefore, was more pronounced for outward perturbations at lower during very slow walking, which is characteristic for clinical speeds and stronger perturbations. Similar results were also populations, other balancing mechanisms, primarily the observed in the studies of Hof et al. [4, 11, 13], however, at inertial strategy in a form of hip strategy, which are consid- higher walking speeds. It seems that slowing down of the ered to have a limited control ability to counteract pertur- movement in the plane of progression following perturbation bations applied in the frontal plane during walking at acting in the frontal plane is related to stiffening of the ankle normally used speeds [2], should be employed earlier in [13] and also knee and hip joints [19] of the stance leg. the stance to impede the development of instability and thus decisively contribute to successful correction of an out- 4.4. Widening of Steps as a General Strategy to Increase ward perturbation. Stability when Faced with the Prospect of a Period of Previous studies have shown that mediolateral ankle Perturbations. Several studies have identified a common pre- strategy is employed following an outward push regardless cautionary strategy of widening steps when faced with pro- of walking speed and intensity of perturbation [4, 5, 13] spective perturbations [14, 15]. The results of our study probably because it can, according to the inverted pendulum show that the subjects consistently adopted wider steps dur- model, act fast against the developing instability by increas- ing perturbed walking sessions. In our opinion, this further ing GRF in the direction opposite to the action of a pertur- ML stresses the importance of utilizing the hip balancing strate- bation. This is also what we observed in this study. No gies in the first half of the stance at the lowest speed of walk- visually noticeable movement of the trunk or the arms was ing as seen in this study, since in a real-life situation, the observed following perturbations in our study, which is con- occurrence of perturbation cannot be expected in advance. sistent with observations from other studies using similar Therefore, the narrower stepping that is normally exercised perturbation intensities and at walking speeds of 1.2 m/s [4] during walking would facilitate an even larger destabilizing and 0.6 m/s [5]. However, the observed impulse-like increase effect of a perturbation applied in the frontal plane as com- of GRF immediately after the perturbation commence- ML pared to walking with adopted wider stepping. ment at low walking speed is not consistent with the inverted pendulum model [1, 12] and implies movement of other 4.5. Relevance of COM-Based Pushes to Real-Life Situations. body segments. Balancing activity during the “in-stance” Hof and Duysens [13] compared the results of ankle muscle activity responses obtained in their study, where the pushes period following the commencement of outward perturba- tion seems to be similar to balancing while standing on one at the level of COM were applied, to the ankle muscle activity leg [12, 17] where visually notable counter-rotation of body obtained in studies that used walking surface translations as a segments resulting in an increase of GRF that acts in the source of perturbation. They concluded that the lateral trans- ML opposite direction of the COM movement is readily used lation of the floor is comparable to inward (medial) perturba- ML tion at the level of the waist while the medial translation of to maintain balance. Our recent study [18] and the study from Vlutters et al. [19] have shown pronounced activity of the floor is similar to outward (lateral) perturbation at the hip abductors of the stance leg following an outward pertur- waist level. Oddsson et al. [8] applied surface translations bation which seems to be the cause of the observed impulse- and observed that lateral translation of the standing foot dur- like increase in GRF constituting a hip strategy. Since this ing the midstance caused the upcoming step to be wider ML GRF impulse was rather small, it has limited capacity to while a medially directed translation caused the upcoming ML substantially move the relatively heavy trunk. Future studies step to be narrower. This is also in agreement with the notion should explore the neuromechanics of the “in-stance” balan- of Hof and Duysens [13] with respect to the similarity of sur- cing responses (consisting of ankle and hip strategies) follow- face translation-based and waist push-based perturbations. 12 Applied Bionics and Biomechanics viduals with gait pathology. Able-bodied and neurologically 4.6. Methodological Considerations and Study Limitations. We limited our analysis to single perturbation timing. impaired subjects have in general different repertoires of The instant of perturbation commencement at the begin- available muscle actions to react to unexpected mechanical perturbations. Balancing responses as assessed in able- ning of the stance was selected because this particular tim- ing gives the perturbation opportunity to develop instability bodied subjects can be regarded as optimal solution for a for the longest period until the leg in swing can enter given speed of walking and a given perturbation strength. stance onto a new location. For example, Oddsson et al. In this study, we found differences in a way how the able- [8] have applied perturbations during the midstance and bodied population reacts to perturbations of the same inten- sity at different speeds of walking. A significant balancing not at the beginning of the stance phase when one would normally expect a real slip to occur. They did that in order activity must commence already during the “in-stance to avoid possible tripping which is clearly associated with period,” which is not the case for higher walking speeds. the stepping response following an outward perturbation. This implies that at low speed of walking, the task of balan- Therefore, a perturbation applied at the beginning of the cing for neurologically impaired will be substantially the same as for able-bodied, and if they will not react appropri- stance seems to be the most challenging to cope with. Additionally, at this perturbation timing, the responses ately already in the “in-stance period,” this will have conse- throughout the varied speeds and intensities finished at quences for subsequent phases of response. Therefore, the end of the next step (within one stride—0–100% of understanding balancing responses in able-bodied individ- a gait cycle). This enabled consistent treatment of all uals at speeds that are similar to those used by neurologi- cally impaired individuals enables us to better understand responses. However, from a methodological point of view, the inclusion of two additional instances of perturbation what the task at hand is for neurologically impaired when occurrence (at 30% and 60% of stance) increased the subjected to mechanical perturbation. level of unpredictability which increases the strength of our findings. 5. Conclusion The largest perturbation intensity used in this study was 15% of body weight which was also the value used in our pre- vious study [7]. At this perturbation intensity, no noticeable In conclusion, our findings reveal reactive dynamic balancing trunk movement or arm movement was observed; however, responses following perturbations delivered at the waist at at the lowest treadmill speed, a perturbation of 15% elicited very slow walking speeds. The responses to inward perturba- responses in some subjects that, beside hip strategy, also tions predominantly consist of a stepping strategy at all required utilization of stance foot repositioning through walking speeds and all tested perturbation intensities. The pivoting on the toes and heel which has also been shown in responses to outward perturbations are highly dependent our previous study [14]. This response indicates that if we on the walking speed and perturbation intensity. Our inter- increased the perturbation magnitude even further, addi- pretation is that at the slowest speed and lowest intensity, tional balancing strategies such as trunk rotation, rapid arm the hip strategy is dominant while at the greatest speed and leg movements, and possibly also hopping on the stance and highest intensity, the stepping strategy dominates. leg could be employed, possibly resulting in inconsistent and Between these two extremes, a synergy of both strategies is variable within-subject responses. used with the relative share of each strategy depending on The balance assessment robot was controlled such that the walking speed and perturbation intensity. Further stud- the interaction forces between the walking subject and pelvis ies should explore in more details the neuromechanics of link were as low as possible. We have assessed the peak the “in-stance” balancing responses (consisting of ankle interaction forces in a previous study and found that the and hip strategies) following an outward perturbation at influence of these forces on COP and GRF in sagittal and low walking speeds. frontal planes as well as on EMGs of major lower limb mus- The results related to balancing responses following out- cles during unperturbed walking had negligible effects in the ward perturbations have implications for the development of range of walking speed from 0.4 to 0.8 m/s [25]. In another a screening method which could identify potential fallers study, we have demonstrated that the interaction between among either elderly or neurologically impaired populations. the balance assessment robot and the pelvis of a walking Inability to generate an adequate “in-stance” response at subject is purely passive; thus, the interaction forces can be slower speeds of walking could be an indication of dimin- perceived as reflected inertia which was estimated for the ished balancing abilities. The results of this study may also balance assessment robot to be below 5 kg at walking speed be very relevant to the developers of control approaches of 0.85 m/s [7]. This is below a value of 6 kg identified in applied in robot exoskeletons that are used to support walk- the study of Meuleman et al. [26] that can be added to the ing and balance functions. pelvis without significantly affecting the gait. Therefore, we may conclude that the interaction forces between the bal- ance assessment robot and the walking subject had minimal Data Availability influence on the dynamic balancing responses observed in this study. The datasets used and/or analyzed during the current study A valid question one can pose is how relevant may be are available from the corresponding author on request for the balancing responses assessed in healthy people to indi- reasonable use. Applied Bionics and Biomechanics 13 [8] L. I. E. Oddsson, C. Wall III, M. D. McPartland, D. E. Krebs, Ethical Approval and C. A. Tucker, “Recovery from perturbations during paced Ethical approval for this study was obtained from Republic walking,” Gait & Posture, vol. 19, no. 1, pp. 24–34, 2004. of Slovenia National Medical Ethics Committee, decision [9] Z. Potocanac, M. Pijnappels, S. Verschueren, J. van Dieën, and number 80/03/15. J. Duysens, “Two-stage muscle activity responses in decisions about leg movement adjustments during trip recovery,” Jour- nal of Neurophysiology, vol. 115, no. 1, pp. 143–156, 2016. Consent [10] B. L. Rankin, S. K. Buffo, and J. C. Dean, “A neuromechanical strategy for mediolateral foot placement in walking humans,” Participants gave consent to use and publish data in such Journal of Neurophysiology, vol. 112, no. 2, pp. 374–383, 2014. way that anonymity is assured. All participants gave signed, [11] A. L. Hof and J. Duysens, “Responses of human hip abductor written, informed consent. muscles to lateral balance perturbations during walking,” Experimental Brain Research, vol. 230, no. 3, pp. 301–310, Conflicts of Interest [12] A. L. Hof, “The equations of motion for a standing human The authors declare that they have no competing interests. reveal three mechanisms for balance,” Journal of Biomechan- ics, vol. 40, no. 2, pp. 451–457, 2007. Authors’ Contributions [13] A. L. Hof and J. Duysens, “Responses of human ankle muscles to mediolateral balance perturbations during walking,” ZM conceived the draft structure and wrote the final version Human Movement Science, vol. 57, pp. 69–82, 2018. of the paper. MZ and AO critically revised the draft paper [14] L. Hak, H. Houdijk, F. Steenbrink et al., “Speeding up or slow- and contributed to all sections. ZM, MZ, and AO all contrib- ing down?: gait adaptations to preserve gait stability in uted substantially to the analysis of the data. MZ did most of response to balance perturbations,” Gait & Posture, vol. 36, the data processing and prepared the figures. All authors read no. 2, pp. 260–264, 2012. and approved the final manuscript. [15] H. E. Stokes, J. D. Thompson, and J. R. Franz, “The neuromus- cular origins of kinematic variability during perturbed walk- ing,” Scientific Reports, vol. 7, no. 1, p. 808, 2017. Acknowledgments [16] B. Raja, R. R. Neptune, and S. A. Kautz, “Quantifiable patterns This research was supported by the Slovenian Research of limb loading and unloading during hemiparetic gait: rela- Agency under research project J2-8172 and research pro- tion to kinetic and kinematic parameters,” The Journal of Rehabilitation Research and Development, vol. 49, no. 9, gram number P2-0228. pp. 1293–1304, 2012. [17] E. Otten, “Balancing on a narrow ridge: biomechanics and References control,” Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, vol. 354, no. 1385, [1] C. D. MacKinnon and D. A. Winter, “Control of whole body pp. 869–875, 1999. balance in the frontal plane during human walking,” Journal [18] Z. Matjačić, M. Zadravec, and A. Olenšek, “Feasibility of of Biomechanics, vol. 26, no. 6, pp. 633–644, 1993. robot-based perturbed-balance training during treadmill walk- [2] C. E. Bauby and A. D. 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Haran, “Interpretation of postural control may change pp. 2655–2664, 2010. due to data processing techniques,” Gait & Posture, vol. 41, [5] M. Vlutters, E. H. F. van Asseldonk, and H. van der Kooij, no. 2, pp. 731–735, 2015. “Center of mass velocity based predictions in balance recovery [21] R. R. Holt, D. Simpson, J. R. Jenner, S. G. B. Kirker, and A. M. following pelvis perturbations during human walking,” The Wing, “Ground reaction force after a sideways push as a mea- Journal of Experimental Biology, vol. 219, no. 10, pp. 1514– sure of balance in recovery from stroke,” Clinical Rehabilita- 1523, 2016. tion, vol. 14, no. 1, pp. 88–95, 2000. [6] A. Olenšek, M. Zadravec, and Z. Matjačić, “A novel robot for [22] Y. Wang and M. Srinivasan, “Stepping in the direction of the imposing perturbations during overground walking: mecha- nism, control and normative stepping responses,” Journal of fall: the next foot placement can be predicted from current upper body state in steady-state walking,” Biology Letters, Neuroengineering and Rehabilitation, vol. 13, no. 1, p. 55, 2016. vol. 10, no. 9, article 20140405, 2014. [7] Z. Matjačić, M. Zadravec, and A. Olenšek, “An effective balan- [23] M. Vlutters, E. H. F. van Asseldonk, and H. van der Kooij, cing response to lateral perturbations at pelvis level during “Foot placement modulation diminishes for perturbations slow walking requires control in all three planes of motion,” near foot contact,” Frontiers in Bioengineering and Biotechno- Journal of Biomechanics, vol. 60, pp. 79–90, 2017. logy, vol. 6, p. 48, 2018. 14 Applied Bionics and Biomechanics [24] K. H. Stimpson, L. N. Heitkamp, J. S. Horne, and J. C. 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Influence of Treadmill Speed and Perturbation Intensity on Selection of Balancing Strategies during Slow Walking Perturbed in the Frontal Plane

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Copyright © 2019 Zlatko Matjačić et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Hindawi Applied Bionics and Biomechanics Volume 2019, Article ID 1046459, 14 pages https://doi.org/10.1155/2019/1046459 Research Article Influence of Treadmill Speed and Perturbation Intensity on Selection of Balancing Strategies during Slow Walking Perturbed in the Frontal Plane Zlatko Matjačić , Matjaž Zadravec, and Andrej Olenšek University Rehabilitation Institute, Republic of Slovenia, Linhartova 51, SI-1000 Ljubljana, Slovenia Correspondence should be addressed to Zlatko Matjačić; zlatko.matjacic@ir-rs.si Received 22 February 2019; Revised 8 May 2019; Accepted 16 May 2019; Published 2 June 2019 Academic Editor: Craig P. McGowan Copyright © 2019 Zlatko Matjačić et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Background. Common understanding is that adequate foot placement (stepping strategy) is crucial in maintaining stability during walking at normal speed. The aim of this study was to investigate strategies that humans use to cope with lateral perturbations during very slow walking. Methods. Ten healthy individuals underwent an experimental protocol whereby a set of perturbations directed inward (medially to a stance leg) and outward (laterally to a stance leg) of three intensities (F =5%, F =10%, and 1 2 F =15% of body weight), applied at three instances of a stance phase, were delivered in random order to the pelvis using a balance assessment robot while walking on a treadmill at three walking speeds (S =0 4, S =0 6, and S =0 8 m/s). We 1 2 3 analyzed the peak center of mass displacements; step length, step width, and step times; and the lateral component of ground reaction force for perturbations that were delivered at the beginning of the gait cycle. Results. Responses after inward perturbations were similar at all tested speeds and consistently employed stepping strategy that was further facilitated by a shortened stance. Wider and shorter steps were applied with increased perturbation intensity. Responses following outward perturbations were more complex. At S , hip strategy (impulse-like increase of mediolateral ground reaction force) augmented with ankle strategy (mediolateral shift of the center of pressure) mainly contributed to responses already during the stance phase. The stance duration was significantly longer for all perturbation intensities. At S , the relative share of hip strategy was reduced while with increased perturbation intensity, stepping strategy was gradually added. The stance duration was significantly longer for F and F .At S , stepping strategy was mainly used while the duration of stance was similar to 1 2 3 the one in unperturbed walking. Responses following both inward and outward perturbations at all speeds were characterized by temporary slowing down movement in a sagittal plane that was more pronounced with increased perturbation intensity. Conclusions. This study provides novel insights into balancing strategies used at slower walking speeds which may be more relevant to understand the challenges of gait stability following perturbations in the frontal plane in clinical populations. 1. Introduction Likewise, following a perturbation that may be imposed by various perturbation modalities, for example, (i) as a push An essential component of bipedal walking is maintenance of at the waist level, mimicking a sudden bump into another dynamic balance, particularly in the frontal plane [1]. The person in a crowd [4–7], (ii) as a movement of the support main mechanism used in normal unperturbed human walk- surface, mimicking a slip [8], and (iii) as a pull on the foot ing has been explained through the inverted pendulum of the swinging leg, mimicking a trip [9], the main balancing model and is related to adequate placement of the swinging strategy used was related to the placement of the swinging limb onto a new stance location [2]. This changes the base limb onto an adequate location [3, 10, 11]. Stepping was of support (BOS) and provides appropriate development of additionally augmented by the “ankle strategy,” which is the lateral component of ground reaction force to ensure sta- related to the activity of ankle musculature to displace the ble side-to-side movement of the center of mass (COM) [3]. center of pressure (COP) under the stance leg in the direction 2 Applied Bionics and Biomechanics the interplay of strategies that humans use to cope with the of the action of perturbation [12, 13]. Additionally, for per- turbations acting in the inward direction (medially relative consequences of an unexpected lateral perturbation. to the stance leg in case of perturbing pushes to the waist), the swing time was shortened to facilitate earlier application 2. Methods of balance correction in the next step [4, 6]. However, for the perturbations acting in the outward direction (laterally 2.1. Subjects. Ten healthy males without known history of relative to the stance leg in case of perturbing pushes to the neuromuscular or orthopedic problems (age: 31 ± 5 years, waist), shortening of the swing phase has not been observed height: 180 ± 3 9cm, and mass: 78 7±6 5kg) participated [4, 6]. Several studies have also pointed out that in sessions in this study after signing informed consent forms. The sub- where perturbations in the frontal plane were delivered sub- jects represent a sample of convenience. The study was jects adopted wider stepping as an additional stabilizing mea- approved by the Slovenian National Ethics Committee. sure, compared to sessions without perturbations [14, 15]. The above referenced studies examined dynamic reactions 2.2. Instrumentation. Figure 1 shows the experimental envi- to perturbations that were imposed during walking in a range ronment, which consisted of a balance assessment robot of speeds that are normally used (0.8–1.2 m/s). and an instrumented treadmill (BART). Here, only a brief Various diseases or injuries to the central nervous sys- description of the experimental setup is given, as a more tem (CNS) result in substantially reduced motor capabilities detailed description is provided elsewhere [6, 7]. The BART in clinical cases. For example, after completion of clinical interfaces with the pelvis of a walking participant with six rehabilitation, the majority of stroke survivors walk with degrees of freedom (DOF). Five of the DOFs (translation speeds that range from 0.4 to 0.8 m/s [16]. Our knowledge of the pelvis in the sagittal, lateral, and vertical directions; of balancing mechanisms used following perturbations at pelvic rotation; and pelvic list) are actuated and admit- these lower speeds of walking is scarce. One consequence tance-controlled, providing transparent haptic interaction of slower walking is that swing times are longer. Thus, for with negligible power transfer [7]. The sixth DOF (pelvic example, if a perturbation is imposed during a double sup- tilt) is passive. The BAR-TM is capable of delivering pertur- port phase, which would resemble a situation of a slip on bations in the forward/backward and left/right directions. the floor [8], it may be the case that a corrective action com- In this study, we only considered inward and outward ing from a wider/narrower next step, which inevitably acts perturbations delivered in the frontal plane as depicted in with considerable delay against the induced instability [4], Figure 1. would not be sufficient to successfully correct for the pertur- COM movement was estimated from the translational bation. Thus, corrective actions may be required to start movement of the subjects’ pelvis and assessed from the already during the stance phase. Apart from using ankle movement of the BAR-TM, similarly as in our previous strategy under the stance leg that can act fast against pertur- studies [7, 18]. Recordings of the ground reaction force bation but has limited stabilizing effect due to a narrow foot (GRF) and COP in the transversal plane during walking width [4, 13], additional strategy related to counter-rotation were obtained by means of four force transducers of body segments, termed as “inertial strategy” [12], which is (K3D120, ME Systeme GmbH) placed underneath the tread- frequently used during one-leg standing [17], may be uti- mill. Spatiotemporal data were assessed by means of an lized during slow walking. The most notable example of OptiTrack camera (NaturalPoint Inc.). Passive reflective inertial strategy is related to the pelvis and trunk rotation markers were placed on the participants’ feet (on the medial and has been termed as “hip strategy” [12, 17]. In our previ- malleoli and the first and fourth metatarsal joints) [7, 18]. ous work with a selected neurologically intact subject walk- Sampling frequency for the kinematic and kinetic data was ing at the speed of 0.4 m/s, we observed that an important 50 Hz which is considered to be adequate for this type of contribution to the balancing response after an outward per- study [20]. turbing push was a hip strategy related to the activity of hip abductors of the stance leg [18]. Vlutters et al. [19] have also 2.3. Experimental Protocol. The experimental protocol is observed important activity of the gluteus medius muscle of shown schematically in Figure 2. First, subjects walked at a the stance leg following outward pushes at walking speed of treadmill speed set to 0.4 m/s for a period of three minute- 0.6 m/s. On the other hand, studies from Hof et al. [4] and s—unperturbed walking session. This was followed by a Vlutters et al. [19] where pelvis perturbations of similar period of around half an hour of perturbed walking—per- intensity were applied in the frontal plane at walking speed turbed walking session. These two experimental blocks were of 1.2 m/s have not observed use of hip strategy. This indi- then repeated for treadmill speeds of 0.6 m/s and 0.8 m/s. The cates that walking speed may have a considerable influence whole protocol was done in a single day and took around 2 on the selection of a suitable balancing strategy or a synergy hours. Perturbations were delivered with a randomly varied of balancing strategies following perturbations applied in the pause that ranged from six to eight seconds in order to avoid frontal plane. predictability of the perturbation occurrence. Four perturba- The aim of this study was to systematically investigate the tion directions (outward RR and LL and inward RL and LR), kinematics and kinetics of reactive dynamic balancing at var- three perturbation onsets (at 0%, 30%, and 60% of the stance ious speeds of slower walking and at various intensities of phase of a gait cycle), and three perturbation amplitudes (5%, inward- and outward-directed perturbing pushes applied at 10%, and 15% of body weight) were varied. Each combina- the waist at the beginning of the stance phase, to elucidate tion of perturbation parameters was repeated seven times. Applied Bionics and Biomechanics 3 RR RL LL LR AP ML (a) (b) Figure 1: Photo of a subject walking on an instrumented treadmill while being embraced by the BAR-TM perturbing device; projection on the wall shows the middle of the BAR-TM working space as well as the current position and orientation of the pelvis in a transverse plane—the subjects were instructed to return to the middle of the BAR-TM working space after they rejected perturbation (a). Top view illustration of perturbation directions: outward RR: perturbation to the right triggered at right-foot contact; inward RL: perturbation to the left triggered at right-foot contact; outward LL: perturbation to the left triggered at left-foot contact; inward LR: perturbation to the right triggered at left-foot contact (b). Unperturbed Perturbed Unperturbed Perturbed Unperturbed Perturbed walking walking walking walking walking walking 252 random perturbations 252 random perturbations 252 random perturbations (3 min) Rest (3 min) (3 min) Rest (30 min) (30 min) (30 min) (5 min) (3 min) S = 0.4 m/s S = 0.6 m/s S = 0.8 m/s 1 2 3 Figure 2: Schematic diagram of the experimental protocol. This yielded a total of 252 perturbing pushes at each walking seven repetitions. We also averaged spatiotemporal parame- speed that were block-randomized. Perturbations took the ters for unperturbed walking in unperturbed walking sessions and unperturbed walking (the periods between the complete form of a force impulse lasting 150 ms [6, 7, 18]. Prior to this study, all subjects visited our laboratory where they practiced recoveries from previous perturbation until the onset of the unperturbed and perturbed walking on the BAR-TM system next perturbation) in the perturbed walking sessions at each tested treadmill speed. for approximately half an hour. Although we assessed postural responses at three levels of 2.4. Measurements and Data Analysis. The COM, COP, and perturbation onset, we included in further analysis only per- GRF were first segmented into strides with the gait cycle turbations that commenced at 0% of a gait cycle. defined as the period between two consecutive left (for LL The following data were used as outcome measures: step and LR responses) or right (for RR and RL responses) heel lengths, step widths, and step times for perturbed (we strikes, as detected from COP and COP signals. Two full analyzed the first step after the perturbation onset which ML AP gait cycles, half of a cycle prior to and one and a half cycles determines the “stepping” response) and unperturbed exper- after the onset of perturbation, were analyzed. Spatiotem- imental conditions; peak displacements of COM within the poral responses were investigated in terms of step length, first stride (from 0% to 100% of the gait cycle) in sagittal step width, and step time where left (right) step length (COM ) and frontal planes (COM ); and integral AP peak ML peak was taken to be the anterio-posterior distance between of the lateral component of GRF (GRF ) for the ML impulse ankle markers at the moment of left (right) foot strike period of the first stance phase (from 0% to approx. 50% while left (right) step width was defined as the mediolat- of a gait cycle) (“in-stance response”) and for the period eral distance between the same markers. Step times were of the second stance phase (from approx. 50% to 100% of a gait cycle) (“stepping response”). Thus, the “in-stance defined as the time elapsed between two consecutive left (right) and right (left) foot strikes. In each combination response” period encompassed the balancing activity prior of perturbation parameters, COM, COP, and GRF trajec- to the first step after the onset of perturbation, while the tories and spatiotemporal parameters were averaged across “stepping response” period encompassed the balancing 4 Applied Bionics and Biomechanics activity between the first and the second steps after the At a walking speed of 0.6 m/s, we can observe increased onset of perturbation. Since GRF determines the acceler- lateral displacement of COP in the “in-stance” period ML ML ation of COM , the GRF provides a measure of while the impulse-like rise in GRF in the first half of the ML ML impulse ML the overall balancing activity in both “in-stance” and “step- “in-stance” period was smaller in comparison to those at ping” periods of balance responses. walking speed 0.4 m/s. Medial displacement of COP and ML related decrease in GRF were observed in the “stepping” ML period for the perturbation intensity of 15%. 2.5. Statistical Analysis. For unperturbed walking, a two-way At a walking speed of 0.8 m/s, increased lateral displace- repeated measures analysis of variance (rmANOVA) was ment of COP in the “in-stance” period was observed while ML used to test for the main effects and interactions on step the impulse-like rise in the GRF in the first half of the “in- ML length, step width, and step time between walking speed (3 stance” period was not present. In the second half of the same levels: 0.4, 0.6, and 0.8 m/s) and walking condition (2 levels: period, there was a gradual decrease of GRF with increas- ML unperturbed walking during unperturbed walking sessions ing perturbation intensity followed by a progressively larger and unperturbed walking during perturbed walking ses- medial displacement of COP and related decrease in ML sions). When a significant main effect or interaction was GRF in the “stepping” period. ML found, we performed post hoc pairwise comparisons for each of the walking speeds separately. A significance level of 0.05 (2) Sagittal Plane. At walking speed of 0.4 m/s, COP was AP was used. displaced increasingly forward in the first half of the stance For perturbed walking, a two-way rmANOVA was with increasing intensity of perturbation while GRF AP used to test for the main effects and interactions on step showed increased braking action that decelerated COM AP length, step width, step time, COM , COM , ML peak AP peak in relation to unperturbed walking. Slowing down of COM AP and GRF between walking speed (3 levels: 0.4, 0.6, ML impulse and associated changes in COP were progressively smaller AP and 0.8 m/s) and perturbation amplitude (4 levels: 0% at walking speeds of 0.6 m/s and 0.8 m/s compared to those (unperturbed strides from perturbed sessions), 5%, 10%, observed at the speed of 0.4 m/s. and 15% of body weight). When a significant main effect or interaction was found, we performed post hoc pairwise com- 3.1.2. Inward Perturbations. Figure 4 shows COP, COM, and parisons versus unperturbed walking for each of the walking GRF responses to inward perturbations (RL) for all three speeds separately. A significance level of 0.05 was used, and a tested walking speeds and for all three tested perturbation Bonferroni correction was applied to correct for multiple intensities for a representative subject. The responses look comparisons (0.016). similar across the tested walking speeds. (1) Frontal Plane. In the “in-stance” period, no noticeable 3. Results difference can be observed in COP , COM , and GRF ML ML ML The results for pushes RR (outward perturbation) and RL in relation to unperturbed walking except for a shortened (inward perturbation) are presented in this section. The duration of the stance phase. The dominant balancing effects of pushes to both outward directions (LL and RR) response can be observed in the “stepping” period where were comparable. Likewise, the effects of pushes to both depending on the perturbation intensity COP was shifted ML inward directions (LR and RL) were comparable. laterally which was accompanied with a progressively increased GRF . ML 3.1. Dynamic Balancing Responses following Perturbations (2) Sagittal Plane. In the second part of the “in-stance” 3.1.1. Outward Perturbations. Figure 3 shows COP, COM, period, a shortened posterior displacement of COP can AP and GRF responses to outward perturbations (RR) for all be observed. Consequently, GRF was also reduced thus AP three tested walking speeds and for all three tested perturba- slowing down movement of COM . Throughout the “step- AP tion intensities for a representative subject. ping” period, a smaller anterior displacement of COP can AP be seen with accompanying reduction of GRF which AP (1) Frontal Plane. At a walking speed of 0.4 m/s, we can enabled COM to catch up with the relative position of AP observe increased lateral displacement of COP in the “in- COM on the treadmill that the subject assumed before ML AP stance” period of the response (from 0% to approx. 50% of the action of perturbation. a gait cycle) in relation to unperturbed walking. An impulse-like rise in the GRF can be seen in the first half 3.2. Peak COM Displacements. Figure 5 shows peak excur- ML of the stance that is similar for all three intensities and acts sions of COM and COM for both outward (RR) and ML AP in the direction opposite to the perturbation. Perturbation inward (RL) perturbations. COM following out- ML peak was fully contained during the “in-stance” period for pertur- ward perturbation was significantly affected by the speed bation intensities of 5% and 10% while following a perturba- of walking (F 2, 18 =10 015, p =0 001), the perturbation tion intensity of 15%, there was medial displacement of intensity (F 3, 27 = 274 194, p <0 001), and their interac- COP and related decrease in GRF in the “stepping tion (F 6, 54 =9 790, p <0 001). Post hoc analysis has ML ML period” (from approx. 50% to approx. 100% of a gait cycle) shown significantly larger peak COM displacements ML that finally contained the instability. for all intensities and at all speeds in comparison to Applied Bionics and Biomechanics 5 S = 0.4 m/s S = 0.6 m/s S = 0.8 m/s 1 2 3 200 200 200 100 100 100 00 0 −100 −100 −100 −200 −200 −200 COP COM 100 100 100 50 50 50 0 0 0 −50 −50 −50 −100 −100 −100 200 200 200 100 100 100 0 0 0 −100 −100 −100 −200 −200 −200 Time (s) Time (s) Time (s) −0.5 0 0.5 1 1.5 2 2.5 −0.5 0 0.5 1 1.5 2 2.5 −0.5 0 0.5 1 1.5 100 100 100 50 50 50 0 0 0 −50 −50 −50 −100 −100 −100 −50 050 100 150 −50 0 50 100 150 −50 0 50 100 150 % gait cycle % gait cycle % gait cycle AP In-stance Stepping RR ML Perturbation interval F = 10% BW Unperturbed gait F = 15% BW F = 5% BW Figure 3: Kinematics and kinetics of balancing responses following outward RR perturbation assessed in a representative subject. The first row shows the trajectories of COP (solid lines) and COM (dotted lines), while the second row shows GRF trajectories. The third ML ML ML row shows COP (solid lines) and COM (dotted lines) trajectories, while the fourth row shows GRF trajectories. Each graph AP AP AP contains responses to all three perturbation intensities along with the trajectories assessed during the unperturbed walking sessions. The left, middle, and right columns show the balancing responses at speeds S , S , and S , respectively. Half a stride prior to and one and a half 1 2 3 strides following the perturbation commencement are shown. A stride is defined as the period between two consecutive right-foot contacts. The trajectories displayed show mean values of seven balancing responses. p =0 unperturbed walking. COM following outward per- 352). Post hoc analysis has shown significantly larger AP peak turbation was significantly affected by the speed of walking peak COM displacements for majority of intensities at all ML (F 2, 18 =69 523, p <0 001), the perturbation intensity speeds in comparison to unperturbed walking. (F 3, 27 =88 255, p <0 001), and their interaction (F 6, 54 =5 551, p <0 001). Post hoc analysis has shown 3.3. Spatiotemporal Parameters. Figure 6 shows spatiotempo- significantly larger peak COM displacements for all inten- ral parameters for unperturbed walking during the unper- AP sities and at all speeds in comparison to unperturbed walk- turbed walking sessions (UWS) and for unperturbed ing. COM following inward perturbation was walking during the perturbed walking sessions (PWS). Step ML peak significantly affected by the intensity of perturbation lengths and step times were significantly affected only by (F 3, 27 =53 150, p <0 001) and interaction between inten- the walking speed (step length F 2, 18 =354 221, p <0 001; sity and speed (F 6, 54 =3 556, p =0 005) but not by the step time F 2, 18 = 238 195, p <0 001) but not by the walk- speed of walking (F 2, 18 =3 088, p =0 070). Post hoc anal- ing condition (step length F 1, 9 =3 089, p =0 113; step ysis has shown significantly larger peak COM displace- time F 1, 9 =4 822, p =0 056) nor the interaction between ML ments for all intensities and at all speeds in comparison to the walking condition and the walking speed (step length unperturbed walking. COM following inward pertur- F 2, 18 =1 304, p =0 296; step time F 2, 18 =2 866, p = AP peak bation was significantly affected only by the perturbation 0 083). Step lengths increased with increased walking speed intensity (F 3, 27 =18 892, p <0 001) but not by the walk- while the step times decreased with increased walking ing speed (F 2, 18 =1 620, p =0 225) nor the interaction speed. Step widths were significantly affected by walking between the intensity and walking speed (F 6, 54 =1 140, speed (F 2, 18 =4 996, p =0 019) and walking condition GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML 6 Applied Bionics and Biomechanics S = 0.4 m/s S = 0.6 m/s S = 0.8 m/s 1 2 3 200 200 200 100 100 100 00 0 −100 −100 −100 −200 −200 −200 COP COM 100 100 100 50 50 50 0 0 0 −50 −50 −50 −100 −100 −100 200 200 200 100 100 100 0 0 0 −100 −100 −100 −200 −200 −200 Time (s) Time (s) Time (s) −0.5 0 0.5 1 1.5 2 2.5 −0.5 0 0.5 1 1.5 2 2.5 −0.5 0 0.5 1 1.5 100 100 100 50 50 50 0 0 0 −50 −50 −50 −100 −100 −100 −50 050 100 150 −50 0 50 100 150 −50 0 50 100 150 % gait cycle % gait cycle % gait cycle AP RL In-stance Stepping ML Perturbation interval F = 10% BW Unperturbed gait F = 15% BW F = 5% BW Figure 4: Kinematics and kinetics of balancing responses following inward RL perturbation assessed in a representative subject. The first row shows the trajectories of COP (solid lines) and COM (dotted lines), while the second row shows GRF trajectories. The third row ML ML ML shows COP (solid lines) and COM (dotted lines) trajectories, while the fourth row shows GRF trajectories. Each graph contains AP AP AP responses to all three perturbation intensities along with the trajectories assessed during the unperturbed walking sessions. The left, middle, and right columns show the balancing responses at speeds S , S , and S , respectively. Half a stride prior to and one and a half 1 2 3 strides following the perturbation commencement are shown. A stride is defined as the period between two consecutive right-foot contacts. The trajectories displayed show mean values of seven balancing responses. 5% and 10% while at 0.8 m/s, significantly shorter steps were (F 1, 9 =70 489, p <0 001) but not by interaction of the two (F 2, 18 =0 830, p =0 452). Post hoc analysis has made at a perturbation intensity of 15% in comparison to shown that the difference between step widths of unper- unperturbed walking. Post hoc analysis further revealed that turbed walking during unperturbed walking sessions and step widths at a walking speed of 0.4 m/s were not statisti- during perturbed walking sessions was on average 4 cm. cally different; at the walking speed of 0.6 m/s, step width at the strongest perturbation was significantly smaller in Figure 7 shows spatiotemporal parameters for perturbed walking following outward (RR) and inward (RL) perturba- comparison to unperturbed walking while at a walking tions. Step lengths, step widths, and step times following out- speed of 0.8 m/s, step widths for all intensities were signifi- ward perturbation were significantly affected by the walking cantly smaller in comparison to unperturbed walking. Post speed (step length F 2, 18 =38 259, p <0 001; step width hoc analysis for step times has shown significantly longer steps at 0.4 m/s for all intensities in comparison to unper- F 2, 18 =8 869, p =0 002; and step time F 2, 18 = 153 168, p <0 001), by intensity (step length F 3, 27 = turbed walking; at 0.6 m/s, this was the case for intensities 6 721, p =0 002; step width F 3, 27 =51 945, p <0 001; of 5% and 10% while at 0.8 m/s, the step time for an inten- and step time F 3, 27 =12 214, p <0 001), and by interac- sity of 10% was significantly longer in comparison to unper- tion of both factors (step length F 6, 54 =5 407, p <0 001; turbed walking. step width F 6, 54 =12 023, p <0 001; and step time F 6, Step lengths and step times following inward perturba- 54 =13 333, p <0 001). Post hoc analysis showed no signif- tion were significantly affected by the walking speed (step icant differences in step lengths at 0.4 m/s; at 0.6 m/s, signifi- length F 2, 18 =43 703, p <0 001; step time F 2, 18 = cantly longer steps were taken at perturbation intensities of 75 724, p <0 001) but not the step width (F 2, 18 =3 085, GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML GRF (N) COP , COM (mm) GRF (N) COP , COM (mm) AP AP AP ML ML ML Applied Bionics and Biomechanics 7 Speed: p = 0.001 Force: p < 0.001 Interaction: p < 0.001 150 0 ⁎ ⁎ 100 −50 50 −100 Speed: p < 0.001 Force: p < 0.001 Interaction: p = 0.001 0 −150 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) (a) 0 0 −50 −50 Speed: p < 0.225 Force: p < 0.001 Interaction: p = 0.352 −100 −100 Speed: p = 0.07 Force: p < 0.001 Interaction: p = 0.005 −150 −150 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) (b) Unperturbed gait F = 10% BW F = 5% BW F = 15% BW 1 3 Figure 5: Group average (±standard deviation) of peak COM and COM excursions across the three walking speeds during unperturbed ML AP walking and perturbed walking is shown for outward RR (a) and inward RL (b) perturbations along with the p values of 2-way rmANOVA. Asterisks ( ) indicate significant difference from unperturbed walking in Bonferroni post hoc pairwise comparisons (p <0 016). p =0 071). On the other hand, perturbation intensity had Post hoc analysis has shown a decrease of step lengths significant effect on step length, step width, and step time and step times and an increase of step widths with (step length F 3, 27 = 195 329, p <0 001; step width F 3, increased intensity at all tested speeds in comparison to 27 =31 060, p <0 001; and step time F 3, 27 = 361 699, unperturbed walking. p <0 001). Only step width and step time were signifi- cantly affected by interaction of both factors (step width 3.4. Lateral GRF Impulses. Figure 8 shows the integral of F 6, 54 =2 758, p =0 021; step time F 6, 54 =44 580, p < GRF over the “in-stance” and “stepping” periods of ML 0 001) and not the step length (F 6, 54 =1 103, p =0 373). dynamic responses following outward (RR) and inward RL RR COM (mm) COM (mm) ML peak ML peak COM (mm) COM (mm) AP peak AP peak 8 Applied Bionics and Biomechanics Speed: p < 0.001 Speed: p = 0.019 Speed: p < 0.001 Walking conditions: p = 0.113 Walking conditions: p < 0.001 Walking conditions: p = 0.056 Interaction: p = 0.296 Interaction: p = 0.452 Interaction: p = 0.083 600 250 1.2 ⁎ ⁎ 500 1 400 0.8 300 0.6 200 0.4 100 0.2 0 0 0 0.4 0.6 0.8 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) Walking speed (m/s) UWS PWS Figure 6: Group average (±standard deviation) of step lengths, step widths, and step times across the three walking speeds during unperturbed walking in unperturbed walking session (UWS) and during unperturbed walking in perturbed walking sessions (PWS) is shown along with the p values of 2-way rmANOVA. Asterisks ( ) indicate significant difference from unperturbed walking in post hoc pairwise comparisons (p <0 05). (RL) perturbations. GRF following outward per- for the “stepping” period at speeds of 0.4 m/s and 0.6 m/s ML impulse turbation was significantly affected by the walking speed showed significantly higher values of GRF for inten- ML impulse (“in-stance” F 2, 18 =37 079, p <0 001; “stepping” F 2, sities of 10% and 15% while at 0.8 m/s, significantly higher 18 =82 463, p <0 001), by intensity (“in-stance” F 3, 27 = values were observed for all intensities in comparison to 26 849, p <0 001; “stepping” F 3, 27 =87 569, p <0 001), unperturbed walking. and by interaction of both factors (“in-stance” F 6, 54 = 10 037, p <0 001; “stepping” F 6, 54 =24 318, p <0 001) 4. Discussion during both periods. Post hoc analysis for the “in-stance” period has shown significant increases for intensities of 5% The main aim of this study was to investigate how slower and 10% at a walking speed of 0.4 m/s while GRF walking speeds and various intensities of perturbing pushes ML impulse value at an intensity of 15% was not significantly different delivered at the heel strike influence the selection of dynamic from unperturbed walking. At 0.6 m/s, GRF values balancing responses. ML impulse at intensities of 5% and 10% were significantly increased Responses after inward perturbations were similar at all while GRF value at an intensity of 15% was signifi- tested speeds and consistently employed a predominantly ML impulse cantly decreased in comparison to unperturbed walking. At stepping strategy facilitated by a shortened stance. Wider 0.8 m/s, only GRF value at an intensity of 5% was steps and shorter stances were applied with increasing per- ML impulse significantly increased while GRF turbation strengths. The role of hip/inertial balancing strate- values at intensi- ML impulse ties of 10% and 15% were significantly decreased. Post hoc gies was not observed. These observations are well in line analysis for the “stepping” period has shown no statistically with the observations of other studies which were mostly per- significant differences among intensity factors at a walking formed at higher walking speeds [4, 5, 7, 11]. speed of 0.4 m/s. At walking speeds 0.6 m/s and 0.8 m/s, the On the contrary, when subjects were faced with outward perturbations, additional inertial balancing strategies were GRF shows increasingly smaller values with increas- ML impulse ing intensity of perturbation in comparison to unperturbed used. The predominant inertial strategy associated with the walking. counter-rotation of body segments changing GRF is the hip Following inward perturbation, GRF was signif- strategy [12, 17, 21]. Depending on the walking speed and ML impulse icantly affected in both periods by the perturbation intensity perturbation intensity, the relative contribution of individual balancing strategy also varied. At the slowest walking speed, (“in-stance” F 3, 27 =53 116, p <0 001; “stepping” F 3, 27 =28 598, p <0 001) and by interaction of both factors we consistently observed a significant contribution of hip (“in-stance” F 6, 54 =4 832, p =0 001; “stepping” F 6, 54 strategy in the first half of the “in-stance” period. The hip =7 391, p <0 001) but was not significantly affected by strategy was augmented with an ankle strategy, displacing walking speed (“in-stance” F 2, 18 =1 289, p =0 300; “step- the COP in the lateral direction away from the direction of ping” F 2, 18 =1 319, p =0 292). Post hoc analysis for the perturbation [13]. The stance duration was significantly lon- “in-stance” period at all speeds showed increasingly smaller ger for all perturbation intensities. At medium walking speed, values of GRF with increasing intensity of perturba- the hip strategy augmented with an ankle strategy was suffi- ML impulse tion in comparison to unperturbed walking. Post hoc analysis cient at the weakest perturbation magnitude while a stepping Step length (mm) Step width (mm) Step time (s) Applied Bionics and Biomechanics 9 Speed: p < 0.001 Speed: p < 0.001 Speed: p < 0.001 Force: p = 0.002 Force: p = 0.002 Force: p < 0.001 Interaction: p < 0.001 Interaction: p < 0.001 Interaction: p < 0.001 600 300 1.5 500 250 400 400 1 300 150 200 100 0.5 100 50 0 0 0 0.4 0.6 0.8 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) Walking speed (m/s) (a) Speed: p < 0.001 Speed: p = 0.071 Speed: p < 0.001 Force: p < 0.001 Force: p < 0.001 Force: p < 0.001 Interaction: p = 0.373 Interaction: p = 0.021 Interaction: p < 0.001 600 300 1.5 ⁎ ⁎ ⁎ ⁎ 500 ⁎ 400 1 200 150 ⁎ ⁎ ⁎ 100 ⁎ 100 0.5 −100 0 0 −200 0.4 0.6 0.8 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) Walking speed (m/s) (b) Unperturbed gait F = 10% BW F = 5% BW F = 15% BW Figure 7: Group average (±standard deviation) of step lengths, step widths, and step times across the three walking speeds during unperturbed walking and perturbed walking is shown for outward RR (a) and inward RL (b) perturbations along with the p values of 2- way rmANOVA. Asterisks ( ) indicate significant difference from unperturbed walking in Bonferroni post hoc pairwise comparisons (p <0 016). strategy was gradually added with increasing perturbation 4.1. Synergy of Balancing Strategies following Outward intensity. At the highest walking speed, stepping was the Perturbations. This study provides an important insight into main strategy used to counteract the effects of perturbation the balancing strategies used at walking speeds that are well while the duration of stance was similar to those in unper- below those normally used and which may be more relevant turbed walking. for understanding the challenges of gait stability following RL RR Step length (mm) Step length (mm) Step widthh (mm) Step widthh (mm) Step time (s) Step time (s) 10 Applied Bionics and Biomechanics In-stance Stepping 60 60 40 40 Speed: p < 0.001 Force: p < 0.001 Interaction: p < 0.001 20 20 0 0 −20 −20 ⁎ Speed: p < 0.001 Force: p < 0.001 −40 −40 Interaction: p < 0.001 −60 −60 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) (a) 60 60 ⁎ ⁎ 40 40 Speed: p < 0.001 Force: p < 0.001 Interaction: p < 0.001 20 20 0 0 −20 −20 ⁎ ⁎ ⁎ ⁎ −40 −40 Speed: p < 0.001 Force: p < 0.001 Interaction: p < 0.001 −60 −60 0.4 0.6 0.8 0.4 0.6 0.8 Walking speed (m/s) Walking speed (m/s) (b) Unperturbed gait F = 10% BW F = 5% BW F = 15% BW 1 3 Figure 8: Group average (±standard deviation) of integrals of GRF over the “in-stance” and “stepping” periods across the three walking ML speeds during unperturbed walking and perturbed walking is shown for outward RR (a) and inward RL (b) perturbations along with the p values of 2-way rmANOVA. Asterisks ( ) indicate significant difference from unperturbed walking in Bonferroni post hoc pairwise comparisons (p <0 016). perturbations in the frontal plane in clinical populations. opinion that control of human gait is predominantly This study complements the existing body of knowledge on achieved through foot placement [3–5, 7, 10]. Stepping strat- the organization of balancing responses during walking fol- egy may well be the primary and energetically wise optimal lowing perturbations acting in the frontal plane. The results coping option following perturbations at normal speeds of of this study to some extent challenge the currently accepted walking; however, the inherent time-delay associated with RR RR GRF (Ns) GRF (Ns) ML impulse ML impulse GRF (Ns) GRF (Ns) ML impulse ML impulse Applied Bionics and Biomechanics 11 swing time needed for a stepping strategy to start acting ing an outward perturbation at low walking speed in more against a perturbation after an outward perturbation is recip- details. rocal to the walking speed. This becomes critical at lower 4.2. Shortening and Prolongation of the Stance Duration as a speeds of walking in particular when the perturbation is Balancing Strategy. It was shown that humans while walking applied in early stance thus maximizing the time for instabil- at normal speeds and when subjected to larger perturbations ity to develop. Wang and Srinivasan [22] have indicated that of inward direction react more quickly by shortening their as much as 80% of the variance in deviations of foot place- stance duration so that the next step which is also a corrective ment from the average during unperturbed walking at speeds step is made earlier [4, 11]. Our results show that this is also ranging from 1 to 1.4 m/s could be explained by deviations the case for lower speeds. from the average in pelvis position and speed at midstance. However, when reacting to outward perturbations at Vlutters et al. [23] have also shown a similar correlation for lower speeds, the stance phase was in most cases substantially perturbed walking at speed of 1.2 m/s. However, a study from prolonged, thus prolonging utilization of the “in-stance” hip Stimpson et al. [24] that examined step-by-step control of strategy resulting in an increase of GRF in the first half of ML step width during unperturbed walking at speeds ranging the stance that acted in the direction opposite to the move- from 0.2 to 1.2 m/s has shown that the strength of the rela- ment of COM. tionship between the step width and pelvis mechanics is sig- nificantly reduced at lower speeds. These findings imply that 4.3. Braking of the Movement in the Plane of Progression as a utilization of adequate foot placement (stepping strategy) as Balancing Strategy. Both types of perturbation lead to tempo- the main strategy to maintain dynamic stability in the frontal rary slowing down of progression in the sagittal plane, which plane depends substantially on walking speed. Therefore, was more pronounced for outward perturbations at lower during very slow walking, which is characteristic for clinical speeds and stronger perturbations. Similar results were also populations, other balancing mechanisms, primarily the observed in the studies of Hof et al. [4, 11, 13], however, at inertial strategy in a form of hip strategy, which are consid- higher walking speeds. It seems that slowing down of the ered to have a limited control ability to counteract pertur- movement in the plane of progression following perturbation bations applied in the frontal plane during walking at acting in the frontal plane is related to stiffening of the ankle normally used speeds [2], should be employed earlier in [13] and also knee and hip joints [19] of the stance leg. the stance to impede the development of instability and thus decisively contribute to successful correction of an out- 4.4. Widening of Steps as a General Strategy to Increase ward perturbation. Stability when Faced with the Prospect of a Period of Previous studies have shown that mediolateral ankle Perturbations. Several studies have identified a common pre- strategy is employed following an outward push regardless cautionary strategy of widening steps when faced with pro- of walking speed and intensity of perturbation [4, 5, 13] spective perturbations [14, 15]. The results of our study probably because it can, according to the inverted pendulum show that the subjects consistently adopted wider steps dur- model, act fast against the developing instability by increas- ing perturbed walking sessions. In our opinion, this further ing GRF in the direction opposite to the action of a pertur- ML stresses the importance of utilizing the hip balancing strate- bation. This is also what we observed in this study. No gies in the first half of the stance at the lowest speed of walk- visually noticeable movement of the trunk or the arms was ing as seen in this study, since in a real-life situation, the observed following perturbations in our study, which is con- occurrence of perturbation cannot be expected in advance. sistent with observations from other studies using similar Therefore, the narrower stepping that is normally exercised perturbation intensities and at walking speeds of 1.2 m/s [4] during walking would facilitate an even larger destabilizing and 0.6 m/s [5]. However, the observed impulse-like increase effect of a perturbation applied in the frontal plane as com- of GRF immediately after the perturbation commence- ML pared to walking with adopted wider stepping. ment at low walking speed is not consistent with the inverted pendulum model [1, 12] and implies movement of other 4.5. Relevance of COM-Based Pushes to Real-Life Situations. body segments. Balancing activity during the “in-stance” Hof and Duysens [13] compared the results of ankle muscle activity responses obtained in their study, where the pushes period following the commencement of outward perturba- tion seems to be similar to balancing while standing on one at the level of COM were applied, to the ankle muscle activity leg [12, 17] where visually notable counter-rotation of body obtained in studies that used walking surface translations as a segments resulting in an increase of GRF that acts in the source of perturbation. They concluded that the lateral trans- ML opposite direction of the COM movement is readily used lation of the floor is comparable to inward (medial) perturba- ML tion at the level of the waist while the medial translation of to maintain balance. Our recent study [18] and the study from Vlutters et al. [19] have shown pronounced activity of the floor is similar to outward (lateral) perturbation at the hip abductors of the stance leg following an outward pertur- waist level. Oddsson et al. [8] applied surface translations bation which seems to be the cause of the observed impulse- and observed that lateral translation of the standing foot dur- like increase in GRF constituting a hip strategy. Since this ing the midstance caused the upcoming step to be wider ML GRF impulse was rather small, it has limited capacity to while a medially directed translation caused the upcoming ML substantially move the relatively heavy trunk. Future studies step to be narrower. This is also in agreement with the notion should explore the neuromechanics of the “in-stance” balan- of Hof and Duysens [13] with respect to the similarity of sur- cing responses (consisting of ankle and hip strategies) follow- face translation-based and waist push-based perturbations. 12 Applied Bionics and Biomechanics viduals with gait pathology. Able-bodied and neurologically 4.6. Methodological Considerations and Study Limitations. We limited our analysis to single perturbation timing. impaired subjects have in general different repertoires of The instant of perturbation commencement at the begin- available muscle actions to react to unexpected mechanical perturbations. Balancing responses as assessed in able- ning of the stance was selected because this particular tim- ing gives the perturbation opportunity to develop instability bodied subjects can be regarded as optimal solution for a for the longest period until the leg in swing can enter given speed of walking and a given perturbation strength. stance onto a new location. For example, Oddsson et al. In this study, we found differences in a way how the able- [8] have applied perturbations during the midstance and bodied population reacts to perturbations of the same inten- sity at different speeds of walking. A significant balancing not at the beginning of the stance phase when one would normally expect a real slip to occur. They did that in order activity must commence already during the “in-stance to avoid possible tripping which is clearly associated with period,” which is not the case for higher walking speeds. the stepping response following an outward perturbation. This implies that at low speed of walking, the task of balan- Therefore, a perturbation applied at the beginning of the cing for neurologically impaired will be substantially the same as for able-bodied, and if they will not react appropri- stance seems to be the most challenging to cope with. Additionally, at this perturbation timing, the responses ately already in the “in-stance period,” this will have conse- throughout the varied speeds and intensities finished at quences for subsequent phases of response. Therefore, the end of the next step (within one stride—0–100% of understanding balancing responses in able-bodied individ- a gait cycle). This enabled consistent treatment of all uals at speeds that are similar to those used by neurologi- cally impaired individuals enables us to better understand responses. However, from a methodological point of view, the inclusion of two additional instances of perturbation what the task at hand is for neurologically impaired when occurrence (at 30% and 60% of stance) increased the subjected to mechanical perturbation. level of unpredictability which increases the strength of our findings. 5. Conclusion The largest perturbation intensity used in this study was 15% of body weight which was also the value used in our pre- vious study [7]. At this perturbation intensity, no noticeable In conclusion, our findings reveal reactive dynamic balancing trunk movement or arm movement was observed; however, responses following perturbations delivered at the waist at at the lowest treadmill speed, a perturbation of 15% elicited very slow walking speeds. The responses to inward perturba- responses in some subjects that, beside hip strategy, also tions predominantly consist of a stepping strategy at all required utilization of stance foot repositioning through walking speeds and all tested perturbation intensities. The pivoting on the toes and heel which has also been shown in responses to outward perturbations are highly dependent our previous study [14]. This response indicates that if we on the walking speed and perturbation intensity. Our inter- increased the perturbation magnitude even further, addi- pretation is that at the slowest speed and lowest intensity, tional balancing strategies such as trunk rotation, rapid arm the hip strategy is dominant while at the greatest speed and leg movements, and possibly also hopping on the stance and highest intensity, the stepping strategy dominates. leg could be employed, possibly resulting in inconsistent and Between these two extremes, a synergy of both strategies is variable within-subject responses. used with the relative share of each strategy depending on The balance assessment robot was controlled such that the walking speed and perturbation intensity. Further stud- the interaction forces between the walking subject and pelvis ies should explore in more details the neuromechanics of link were as low as possible. We have assessed the peak the “in-stance” balancing responses (consisting of ankle interaction forces in a previous study and found that the and hip strategies) following an outward perturbation at influence of these forces on COP and GRF in sagittal and low walking speeds. frontal planes as well as on EMGs of major lower limb mus- The results related to balancing responses following out- cles during unperturbed walking had negligible effects in the ward perturbations have implications for the development of range of walking speed from 0.4 to 0.8 m/s [25]. In another a screening method which could identify potential fallers study, we have demonstrated that the interaction between among either elderly or neurologically impaired populations. the balance assessment robot and the pelvis of a walking Inability to generate an adequate “in-stance” response at subject is purely passive; thus, the interaction forces can be slower speeds of walking could be an indication of dimin- perceived as reflected inertia which was estimated for the ished balancing abilities. The results of this study may also balance assessment robot to be below 5 kg at walking speed be very relevant to the developers of control approaches of 0.85 m/s [7]. This is below a value of 6 kg identified in applied in robot exoskeletons that are used to support walk- the study of Meuleman et al. [26] that can be added to the ing and balance functions. pelvis without significantly affecting the gait. Therefore, we may conclude that the interaction forces between the bal- ance assessment robot and the walking subject had minimal Data Availability influence on the dynamic balancing responses observed in this study. The datasets used and/or analyzed during the current study A valid question one can pose is how relevant may be are available from the corresponding author on request for the balancing responses assessed in healthy people to indi- reasonable use. Applied Bionics and Biomechanics 13 [8] L. I. E. Oddsson, C. Wall III, M. D. McPartland, D. E. Krebs, Ethical Approval and C. A. Tucker, “Recovery from perturbations during paced Ethical approval for this study was obtained from Republic walking,” Gait & Posture, vol. 19, no. 1, pp. 24–34, 2004. of Slovenia National Medical Ethics Committee, decision [9] Z. Potocanac, M. Pijnappels, S. Verschueren, J. van Dieën, and number 80/03/15. J. 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