Evidence of Proactive Forefoot Control During Landings on Inclined Surfaces

Transcription

1 Journal of Motor Behavior, 27, Vol. 39, No. 2, Copyright 27 Heldref Publications Evidence of Proactive Forefoot Control During Landings on Inclined Surfaces Gaspar Morey-Klapsing Adamantios Arampatzis Gert-Peter Brüggemann Institute of Biomechanics and Orthopedics German Sport University Cologne ABSTRACT. The notion of proactive control of landings is generally accepted, and some underlying mechanisms have already been described. Only little is known on adjustments at the foot level, however. The authors therefore investigated the foot and ankle behavior of 24 participants as they landed on differently inclined surfaces. A 4-segment model of the foot and ankle provided 3-dimensional kinematics. They also analyzed activation patterns from several muscles and the ground reaction force. Participants anticipated the different surfaces, as shown by the forefoot kinematics and the activation patterns before touch down. Anticipation of the surface inclination led to adjustments in forefoot orientation and probably also in joint stiffness. The authors suggest that those adjustments tend to enhance the self-stabilizing potential of the mechanical system. The enhancement of that potential would ease the subsequent stabilization, reducing the demands on the neural system. Key words: foot kinematics, joint stabilization, landing, proactive control E vidence suggests that, because of the inherent latencies of feedback loops, pure reactive responses are insufficient to ensure joint stabilization (Grüneberg, Nieuwenhuijzen, & Duysens, 23; Isakov, Mizrahi, Solzi, Susak, & Lotem, 1986; Konradsen, Voigt, & Hojsgaard, 1997). The insufficiency is especially evident in acute situations, such as landings, in which high forces (Mizrahi & Susak, 1982), joint moments (DeVita & Skelly, 1992), and fast joint rotations (Arampatzis, Brüggemann, & Morey- Klapsing, 22; Mizrahi & Susak) happen within 4 5 ms after touch down (TD). Dyhre-Poulsen, Simonsen, and Voigt (1991) found that during that early stage of landing, the excitability of the motoneuron pool is down-regulated (reduced). In addition to the lowered reflex responsiveness, not enough time is available for building up any significant reflex activity in response to the collision with the ground (Duncan & McDonagh, 2; Grüneberg et al., 23). It is therefore reasonable to suppose that there are other mechanisms responsible for successful landing stabilization. For example, prelanding electromyographic (EMG) amplitude and timing were scaled in proportion to drop height (Santello & McDonagh, 1998; for a review of motor control during landings, see Santello, 25). One fundamental mechanism favoring joint stabilization after impact is anticipation (Lacquaniti & Maioli, 1989). Furthermore, self-stabilizing mechanisms of the human musculoskeletal system that is, stabilizing reactions that arise solely from the passive interaction between the anatomical structures and the external forces have been described earlier (Moritz & Farley, 24; Wagner & Blickhan, 23). Such mechanisms can react as soon as the disturbance appears, and because of that zero delay reaction, they have also been termed preflexes (Loeb, 1995). Preflexes are, a priori, independent of neural feedback and the inherent latencies, and possibly represent a main mechanism contributing to joint stabilization (Wagner & Blickhan). It has thus been observed that the tuning (e.g., segment orientation and muscular preactivation) of the musculoskeletal system before the collision with the ground influences the later landing performance (DeVita & Skelly, 1992; Dufek & Bates, 199; McKinley & Pedotti, 1992). Anticipation relies on proactive adjustments but, to some extent, also on feedback. For example, the instant of ground contact as well as surface inclination can be predicted from visual feedback cues, but to produce an adequate Correspondence address: Adamantios Arampatzis, Institute of Biomechanics and Orthopedics, German Sport University Cologne, Carl-Diem-Weg, 6, D-5933 Cologne, Germany. address: arampatzis@dshs-koeln.de 89

2 G. Morey-Klapsing, A. Arampatzis, & G.-P. Brüggemann response one needs an adequate interpretation of those cues and a suitable internal model for predicting their consequences (Flanagan, Vetter, Johansson, & Wolpert, 23; Lacquaniti & Maioli, 1989). From the aforementioned examples, we can conclude that feedforward strategies and feedback information determine the motor commands for landing and that any interaction with the environment will include the passive mechanical response of the system (passive dynamics). Although proactive control of landing is generally accepted in the research community and also is experimentally supported (Arampatzis, Morey-Klapsing, & Brüggemann, 23; Caster & Bates, 1995; Duncan & McDonagh, 2; Dyhre-Poulsen et al., 1991; McKinley & Pedotti, 1992; Moritz & Farley, 24; Santello & McDonagh, 1998; Thompson & McKinley, 1995), little is known on the specific adjustments taking place at the foot level. Arampatzis et al. (22; Arampatzis et al., 23) found that after TD, the ankle joint may demonstrate the same behavior throughout different surface conditions or falling heights, whereas adjustments take place at the forefoot joints. Consequently, one should be careful when interpreting results from simple foot models because an absence of adaptation for example, at the ankle joint does not imply an absence of adaptation at the whole foot. To our knowledge, investigators have not used detailed foot models to study anticipatory foot behavior during landings. The first and most direct interaction with the environment during locomotion occurs at the feet. Gaining insight into the anticipatory behavior at the feet could provide useful information for the planning and control of fall prevention and rehabilitation programs, shoe design, as well as for the planning of further motor-control-oriented studies that may lead to a better understanding of how our biological system deals with different surface characteristics. Our aim in the present study was to identify proactive adjustments at the foot level to differing surface inclinations in the frontal plane during landings. One can hypothesize that one role of feedforward strategies is to enable the performer to take advantage of the self-stabilizing mechanisms of the involved structures by means of an appropriate adjustment of segment orientation and joint stiffness that would consequently ease the task of the reactive stabilizing mechanisms. We therefore recorded the foot kinematics, the EMG signals of six muscles of the lower leg (peroneus longus [PL], peroneus brevis [PB], tibialis anterior [TA], gastrocnemius lateralis [GL], gastrocnemius medialis [GM], and soleus [SOL]), and the ground reaction forces (GRF) during landings from a 4-cm height before and after collision with the ground onto three surfaces; a level one, and two surfaces inclined 3 either laterally (lowered lateral border, inducing inversion) or medially (lowered medial border, inducing eversion). Method All participants (12 men and 12 women, aged 2 33 years, and all active in sports from recreational to competitive level) gave their informed consent to participate in this study. We asked them to perform one-leg drop landings from a 4-cm-high box onto three differently inclined surfaces: one level surface and two surfaces inclined 3 either laterally or medially. Participants performed three consecutive trials per surface condition. The order of surface presentation was randomized. We instructed the participants to hold their hands on their hips, to initiate the drop by forwarding the right foot and pushing off from the box with the left one, and, finally, to land on their left foot, stabilizing their body as soon as possible. All participants had to perform at least three successful trials per condition. A trial was considered successful when (a) the measuring systems recorded the corresponding data, (b) participants stabilized the landing without touching the ground with the right foot, and (c) there was no hop, that is, loss of ground contact with the foot after TD. During the drop landings, we recorded kinematics, EMG, and GRF. We synchronized the EMG and the GRF by means of a TTL (Transistor Transistor Logic) signal; that is, a digital signal that switched between and 5 V, providing a neat flag. The signal was fed onto both data-acquisition boards. Four parallel-switched lightemitting diodes that we used to synchronize the cameras with each other and with the remaining systems lit up simultaneously. Kinematics We modeled the lower leg and the foot by means of a multibody system composed of four rigid bodies (Figure 1). Detailed information on the original model can be found in Arampatzis et al. (22) and Arampatzis et al. (23); the modified version used in the present study is described in Morey-Klapsing, Arampatzis, and Brüggemann, (25a, 25b). The motions between the rear foot and the shank (referred to herein as ankle joint), the medial column of the forefoot to the rear foot (referred to herein as medial foot joint), and the lateral column of the forefoot to the rear foot (referred to herein as lateral foot joint) were considered in the model. Seventeen skin-mounted reflective markers defined the model and the zero angles during a reference measurement (Figure 1, Table 1). The position for reference measure was defined as the foot plane on the ground, with its longitudinal axis pointing forward and the shank vertical (tip of the medial malleolus directly below the tip of the caput fibula). We calculated the model motion from the coordinates from 12 of those markers filmed during the landings. In an attempt to account for skin motion, we attached the markers to the model by means of spring-damping elements. Joint motion was given by the relative rotation between the two coordinate systems attached to each of the two connected segments. The kinematics of the ankle and the medial and the lateral foot joints were given by the orientation of the most distal joint coordinate system with respect to the more proximal in the following rotation sequence: eversion inversion, dorsiflexion plantarflexion, and adduction abduction. 9 Journal of Motor Behavior

3 Proactive Forefoot Control in Landing A B C D FIGURE 1. (A) Lateral, (B) frontal, and (C) medial views of the reference measurement defining the foot model and (D) a view of the model containing the four considered segments: leg, rear foot, medial forefoot, and lateral forefoot. TABLE 1. List of Markers Used to Define the Model and to Steer Its Motion Marker Pertaining segment Bony landmarks 1. Caput metatarsale I (most medial point) Medial foot joint 2. Caput metatarsale V (most lateral point) Lateral foot joint 3. Tuberositas naviculare (most medial point) Medial foot joint 4. Os cuboideum (diagonal superior to the basis of the fifth metatarsal) Lateral foot joint 5. Malleolus medialis (most medial point) Leg 6. Malleolus lateralis (most lateral point) Leg 7. Condilus medialis tibiae (most medial point) Leg 8. Caput fibula (most lateral point) Leg Other markers 9. Caput metatarsale I (medial superior) Medial foot joint 1. Caput metatarsale V (lateral superior) Lateral foot joint 11. Caput metatarsale II III (between second and third metatarsal heads) Lateral and medial foot joints 12. Metatarsus I (more proximal) Medial foot joint 13. Metatarsus V (more proximal) Lateral foot joint 14. Calcaneus medial (more anterior) Rear foot 15. Calcaneus medial (more posterior) Rear foot 16. Calcaneus lateral Rear foot 17. Fascies tibiae Leg Note. To define the model, the authors fixed eight markers at anatomical landmarks and nine more markers on not strictly defined anatomical positions but rather on locations where lesser skin movements were expected. Markers 1, 2, 4, 7, and 8 were needed only for the model definition and were detached before the landings. The model does not represent true bony motion; however, it allows one to describe foot motion more accurately than simpler models do. Four cameras captured marker motion: two operating at 12 Hz (NTSC, Peak Performance Technologies, Centennial, CO) and two operating at 25 Hz (one Redlake 25C and one Kodak motion corder analyzer SR-5c; Roper Scientific MASD, San Diego, CA). We digitized the video data by using the MOTUS 6 software (Peak Performance Technologies). After obtaining the three-dimensional (3D) coordinates from each camera pair, we interpolated the data by using quintic splines to achieve a common frequency with the analogue data (EMG and GRF) sampled at 1 Hz. In most of the trials, one of the markers defining the medial column of the forefoot could not be tracked accurately during the first phase of the whole landing because, March 27, Vol. 39, No. 2 91

4 G. Morey-Klapsing, A. Arampatzis, & G.-P. Brüggemann in that position, markers of the medial aspect of the foot were overlapped in the camera view. There were not enough data to perform statistics regarding the motion of the medial foot joint during that phase. Therefore, for that joint, we present results only from 6 ms after TD on. EMG For EMG collection, we used bipolar, preamplified (analogue RC-filter 1- to 5-Hz bandwidth) leadoffs (Biovision, Wehrheim, Germany) and autoadhesive, gelled Ag/AgCl surface electrodes (pick-up surface.8 cm 2, interelectrode distance 2 cm) placed above the bellies of the studied muscles, parallel to the presumed muscle fiber direction. We sampled at 1 Hz the signals from six muscles of the lower leg, PL, PB, SOL, GL, GM, and TA. Although we detected no artifacts produced by passive leg shaking or by slight hopping after preparation, artifacts appeared at individually fixed time intervals after impact in several cases, mainly during the inclined conditions. We were able to remove them without substantial alteration of the remaining signal by applying a 3-Hz fast Fourier transform (FFT) high-pass filter. We did so for all EMG signals. Afterward, we smoothed the curves by means of a 3-point backand-forth moving root mean square (RMS) algorithm. Starting from the end of the signal, we substituted the RMS of points 1 3 for the 3th value, and we then substituted the RMS of points 2 31 for the 31st value, and so on. We did the same thing afterward to the resulting signal, but starting from the beginning. The obtained signals were smooth enough to allow a point-by-point comparison of the EMG (see Data Analysis). In the postprocessing, neither the filtering nor the smoothing introduced any substantial time shifts in the signals (see Figure 2). We then normalized the curves to the RMS of the EMG signal recorded during the ground contact phase of defined one-legged horizontal jumps onto the 3 laterally inclined surface (we used the mean of three trials). Raw (RC 1 5 filter) FFT 3-Hz high-pass RMS 3 points back and forth 3,5 3, 2,5 ADU 2, 1,5 1, FIGURE 2. Raw, filtered, and smoothed electromyographic signal of the peroneus longus from 1 participant who was landing on the level surface. The raw signal corresponds to the signal as captured (an RC 1-5 Hz filter was included in the amplifier). The 3-Hz high-pass fast Fourier transform (FFT) filter removed the artifact without substantial alteration of the remaining signal. The authors smoothed the filtered signal by using a 3-point root mean square (RMS) smoothing. The strong filtering was needed for a millisecond-by-millisecond comparison. Note that for figure clarity, the raw and the filtered signals were rectified before they were plotted, whereas the actual data were rectified in the smoothing process. ADU = analogue digital units (values as sampled by the data-acquisition board). 92 Journal of Motor Behavior

5 Proactive Forefoot Control in Landing GRF We measured the GRF at 1 Hz by means of a forceplate (Kistler, Type 9881B21, Winterthur, Switzerland) embedded in the floor. The landing surfaces were fixed (securely screwed) on the plate. The center of the plate was 35 cm in front of the edge of the starting box. That distance proved to be the mean distance from the box at which the participants landed centered onto the plate. We determined the instant of TD from the GRF data when the vertical force exceeded 2 N, which happened within the first 1 or 2 ms after TD (Figure 3). The three components of the GRF data were analyzed separately. Data Analysis We used the following software for data analysis: To calculate the model and the kinematics, we used the simulation software ALASKA (Advanced Lagrangian Solver in Kinetic Analysis, Version 3.; Chemnitz, Germany). Using the Peak Motus software (Peak Performance Technologies, Inc., Centennial, CO), we obtained the 3D coordinates of the markers by digitizing the video sequences. We used self-written MAT- LAB (The MathWorks, Natick, MA) code to filter, smooth, and average the data, and the statistical software package SPSS Version 11 (SPSS Inc., Chicago, IL) to do the statistics. We averaged three trials per condition from each participant. In that way, we obtained 24 mean curves for each condition and parameter, which we then entered into the statistics. Kinematics measurements included eversion inversion, dorsiflexion plantarflexion, and adduction abduction motions for each of the three considered joints from 2 ms before to 4 ms after TD, and EMG from each of the six muscles from 2 ms before to 4 ms after TD. GRF measures included mediolateral, anteroposterior, and vertical force components from TD to 4 ms afterward. The kinematics measures were available only for 21 participants. We found only about half of the data to be normally distributed (Shapiro Wilk test, p >.5). Consequently, we chose a nonparametric test for K related samples (Friedman test) to study the effect of surface inclination on the measured variables. We analyzed all data millisecond by millisecond for each of the parameters. We set the level of significance to α =.5. When differences were found, we applied the Wilcoxon test for pairwise comparisons. We adjusted the level of significance (α =.5) in accordance with Bonferroni. To describe the magnitude of the variation between conditions, we calculated the RMS differences between the means of each participant for every millisecond. For considering a significant difference to be meaningful, we defined a relevance threshold: For the kinematics, we chose an absolute threshold of 2 because that threshold corresponds to the typical difference between stable and unstable Fz (N) 4, 3,5 3, Fz (N) N A Fz (N) 2,5 2, Fz (N) N B 2,5 2, , ,5 1, 1, Time (s) Time (s) 1.3 FIGURE 3. Vertical force curves from 2 participants landing on the level surface. (A) The participant touches the ground first with the toes. The first peak after 12 ms corresponds to the ball impact after toe rotation and compression of the soft tissue. The second (main) peak corresponds to heel impact. (B) The participant touches the ground with toes and ball almost simultaneously; the early peak disappears. Both zoomed areas show that the 2-N touchdown detection threshold was reached within the first millisecond after touchdown. March 27, Vol. 39, No. 2 93

6 G. Morey-Klapsing, A. Arampatzis, & G.-P. Brüggemann ankles in joint position-sense tests (Konradsen 22). For the EMG and the GRF, the RMS difference had to be above 1% of the maximal value of the corresponding mean curve obtained for the level condition. We arbitrarily chose that threshold because differences below 1% are often considered normal deviations in clinical diagnoses. Results In this section, whenever we refer to differences (higher or lower values) between conditions, we mean that they were significant (p <.5) and above the relevance threshold as described in the Method section. The inverse applies when we refer to the absence of differences or to similar values among conditions, that is, a p >.5 or a difference below the relevance threshold, or both. Plots showing the mean curves from all participants among conditions represent the effects of surface inclination on the measured parameters. We did not make statistical comparisons between the means; instead, we compared the participants themselves among those conditions. Whereas the overall shape of the different curves was similar for all participants, there were characteristic individual differences, mainly in the amplitudes but also in shifts along the y-axis. Therefore, the mean curves did not necessarily match the data from single individuals. Those interindividual differences were often higher than were the differences between conditions (see the individual plots in Figures 4 and 5, and compare Tables 2 4 with the corresponding Figures 4 8). However, the effects of the different surfaces were common to almost all participants, as reflected by the observed significant differences between conditions presented next. Kinematics At TD, the ankle was strongly plantarflexed. The toes were extended (dorsiflexed) so that the plantar aponeurosis was tightened, stiffening the longitudinal foot axis and contributing to the absorption of the imminent impact. Whereas no proactive adjustments in ankle position were observed, the lateral forefoot shifted its eversion inversion pattern according to surface inclination; it was more inverted before landings onto the laterally inclined surface (Figure 6). An adjustment such as that probably was also present at the medial forefoot, but we could not analyze it (see Method). On the level and the medially inclined surfaces, the lateral forefoot eversion inversion kinematics behaved similarly until the first 15 ms after TD. Throughout most of the contact phase, both forefoot joints showed a significantly shifted eversion inversion curve according to surface inclination (Figure 6). The shift in the ordinates exceeded by about 1 the differences in surface inclination (for the lateral foot joint, 4., 4.1, and 8.1, respectively, Participant Participant Level Lateral Medial Level Lateral Medial A B Inversion Eversion C FIGURE 4. Inversion eversion motion at the three studied joints (A) ankle, (B) medial forefoot joint, and (C) lateral forefoot joint on all three surfaces (level, laterally inclined, and medially inclined), from 2 different individuals. 94 Journal of Motor Behavior

7 Proactive Forefoot Control in Landing Participant A Level Lateral Medial Participant B Level Lateral Medial PL PB EMG Activity TA FIGURE 5. Electromyographic (EMG) activity profiles from the peroneus longus (PL), peroneus brevis (PB), and tibialis anterior (TA) muscles on all three surfaces (level, laterally inclined, and medially inclined) from 2 different individuals. between the level and the laterally inclined, level and medially inclined, and both inclined surfaces; and, correspondingly, for the medial foot joint, 3.6, 3.4, and 7.1, respectively, between those surfaces. The ankle joint displayed no significant differences in the eversion inversion pattern (Figure 6). Regarding the dorsiflexion plantarflexion (Figure 7), the ankle joint again showed no significant differences among the surface conditions. The medial foot joint showed significantly lower dorsiflexion values when landing onto the medially inclined surface throughout the whole available data than it did when landing onto the laterally inclined one, and for several time intervals compared with its values for landings onto the level surface. The level and the laterally inclined surfaces produced no differing dorsiflexion plantarflexion patterns at the medial foot joint until almost the end of the observed time window (38 ms). The different surface conditions seemed not to have any significant influence before TD on the lateral foot joint s dorsiflexion plantarflexion behavior. After TD, that joint showed lower dorsiflexion values for landings onto the laterally inclined surface than for landings onto the level one (from 56 ms to 167 ms). No differences were apparent between the level and the medially inclined surfaces, and, only for a short time window between 16 and 32 ms, the medially inclined surface led to slightly higher dorsiflexion values than did the laterally inclined surface. The adduction abduction showed almost no relevant differences among the tested surface conditions at any studied joint. Only the lateral foot joint was more abducted for several short time intervals post-td when landing on the medially inclined surface than it was when landing on the level one. Electromyography We grouped the proactive surface effects found on the EMG into early (more than 6 ms before TD) and late (less than 5 ms before and 35 ms after TD) effects. The everting PL therefore showed lower activation levels when landing on the laterally inclined surface (Figure 8) early before TD (approximately 16 to 12 ms). Conversely, the inverting TA had lower activity levels when landing on the medially inclined surface than it did when landing on the laterally inclined one from 96 to 54 ms before TD. At the slightly March 27, Vol. 39, No. 2 95

8 G. Morey-Klapsing, A. Arampatzis, & G.-P. Brüggemann TABLE 2. Intrasubject (Intra) and Intersubject (Inter) Variability (deg) for the Kinematics, as Indicated by the Corresponding Mean Standard Deviations for the Different Conditions and Time Intervals (ms) Level Lateral Medial Motion Interval Intra Inter Intra Inter Intra Inter Ei Dp Aa Ei Dp Aa Ei Dp Aa Angle joint 2 to to to to to to Medial foot joint 2 to t to to to to Lateral foot joint 2 to to to to to to Note. Ei = eversion inversion; Dp = dorsiflexion plantarflexion; Aa = adduction abduction. inverting triceps surae, the GM demonstrated early proactive adjustments to surface inclination, showing lower activation levels before landings onto the medially inclined surface (Figure 9). The SOL behaved similarly, but only for a very discrete time window (Figure 9). Late anticipatory adjustments approximately 35 ms before and after ground contact were also found (Figures 8 and 9). Both peronei were more active during landing onto the laterally inclined surface, followed by landings onto the level surface, and finally onto the medially inclined one. Those differences were often reversed later in time, more than 15 ms post-td. Just before TD, the SOL was less active when landing on the medially inclined surface than when landing on the laterally inclined one. The GL s behavior was similar for all surfaces, and there were no significant differences before TD for any of the triceps surae muscles between the level and the laterally inclined conditions (Figure 9). GRF In general, the GRF showed moderately smoother patterns for the landings on the medially inclined surface. That was especially true for the mediolateral forces during the first 5 ms, but also for the vertical impact force, which was 1% lower for landings onto the medially inclined surface than for landings onto the laterally inclined one (Figure 1). Discussion Critical Review of the Method To ensure a good spatial resolution to increase the accuracy of the kinematics, we chose the narrowest possible 96 Journal of Motor Behavior

9 Proactive Forefoot Control in Landing TABLE 3. Intrasubject (Intra) and Intersubject (Inter) Variability of the Electromyographic Signal (EMG), as Indicated by the Corresponding Mean Standard Deviations for Different Conditions and Time Intervals (ms) Level (% EMG) Lateral (% EMG) Medial (% EMG) Interval Intra Inter Intra Inter Intra Inter Penoneus longus 2 to to to Peroneus brevis 2 to to to Tibialis anterior 2 to to to Gastrocnemius lateralis 2 to to to Gastrocnemius medialis 2 to to to Soleus 2 to to to TABLE 4. Intrasubject (Intra) and Intersubject (Inter) Variability for the Ground Reaction Force, as Indicated by the Corresponding Mean Standard Deviations for the Different Conditions and the Given Time Interval (ms) Level Lateral Medial Force Interval Intra Inter Intra Inter Intra Inter Fx(AP) to Fy(ML) to Fz(Vert) to Note. Fx(AP) = anteroposterior force; Fy(ML) = mediolateral force; Fz(Vert) = vertical force. Units are N/kg of body weight. March 27, Vol. 39, No. 2 97

10 G. Morey-Klapsing, A. Arampatzis, & G.-P. Brüggemann Level vs. Lateral Level vs. Medial Lateral vs. Medial A B C Inversion Eversion (deg) FIGURE 6. Pairwise comparison of the inversion eversion motion between the different surface conditions (level vs. lateral, level vs. medial, and lateral vs. medial). The different rows contain the three studied joints: (A) ankle, (B) medial foot joint, and (C) lateral foot joint (n = 21). The zero in the time axis corresponds to touchdown. The shaded areas indicate relevant differences, that is, significant (p <.5) and above 2. For the medial foot joint, no data were available until 6 ms after touchdown (see Method, Kinematics). field of view. As a consequence of the narrow field of view, however, the time window before TD was shortened. For several participants (those with bigger feet or those who landed in extreme plantarflexion), there were only three frames available in the 12-Hz cameras before TD. Additional kinematic data before TD could have served to strengthen the relationship between the differences observed in the EMG and the kinematics. Nevertheless, the short time window available was enough to provide evidence of the proactive adjustments taking place in forefoot orientation in response to the presented surface inclinations. Because important differences were observed near TD, we needed accurate detection and synchronization to ensure that the observed differences in the kinematics and the EMG were in fact happening before TD. We determined TD as the instant at which the vertical GRF increased above 2 N. Figure 3 shows two slightly different vertical force curves corresponding to landings in which the plate was touched first with the toes or with the toes and the ball of the foot simultaneously. In both cases, the 2-N threshold was reached within the first millisecond. Assuming identification takes place in the second millisecond after TD, the detection method would maximally contribute 1 ms to the synchronization error. The biggest source of synchronization error arises from the kinematics of the 12-Hz cameras. At worst, they may contain time shifts just below one frame duration (8.33 ms). Those shifts are not systematic and may happen in either direction. Even assuming 1.-ms ms synchronization error, which is very unlikely, that is less than half the available time window before TD. Therefore, we are sure that most of the data assumed to be before TD actually pertained to that period. For the EMG, one should ensure that signal treatment does not influence the signal in a manner that could affect the conclusions drawn from the data analysis. The RC 1- to 5-Hz filter integrated in the amplifier may have introduced a maximal delay of 8 ms for the lowest frequency content and possibly around 2 ms for the whole signal. Any delay means that the actual signal took place earlier. The implemented FFT filter preserved the time characteristics of the original signal quite well, with minor shifts in either direction of single rises and falls. The subsequent smoothing canceled out those minor shifts. One must perform the smoothing to allow a millisecond-by-millisecond comparison, but that could create artificially high signals in advance to a steep increase in the original trace. As shown in Figure 2, however, those rises were not steep enough to produce a 98 Journal of Motor Behavior

11 Proactive Forefoot Control in Landing Level vs. Lateral Level vs. Medial Lateral vs. Medial A B C Plantarflexion Dorsiflexion (deg) FIGURE 7. Pairwise comparison of the plantarflexion dorsiflexion motion between the different surface conditions (level vs. lateral, level vs. medial, and lateral vs. medial). The different rows contain the three studied joints: (A) ankle, (B) medial foot joint, and (C) lateral foot joint (n = 21). The zero in the time axis corresponds to touchdown. The shaded areas indicate relevant differences, that is, significant (p <.5) and above 2. substantial left shift. Although slight left shifts may be introduced, those are partly compensated by the right shift of the RC-filter and would anyway be too low to account for all the differences observed in the period immediately before TD. In addition, at the EMG, the first 35 ms after TD can also be considered part of the proactive adjustment because no reflex activity can be expected before that. The model we used does not contain any true anatomical joints and is driven by skin markers. Therefore, the model gave only an approximation of real foot motion. However, the model showed a systematic proactive adjustment to the expected surfaces that cannot be attributed to chance. Interpretation of the Results One-leg landings from 4 cm onto surfaces differing by 3 and 6 in frontal plane inclination were studied. Proactive adjustments in forefoot orientation in response to frontal plane inclination were observed as a higher lateral forefoot inversion before landings onto the laterally inclined surface (Figure 6). The finding that such adjustments could not be found at the ankle joint emphasizes the importance of forefoot motion. The observed adjustments in segment orientation were underpinned by the EMG data (Figures 8 and 9). Those changes in activation that appeared early in the landing phase, more than 6 ms before TD when the overall activation of the muscles surrounding the ankle was low, were partially reflected in the differences in segment orientation. The differences in activation, which appeared in immediate proximity to TD, when the overall activation of the corresponding musculature was relatively high, probably reflected different activation demands (i.e., stiffness tuning) of those muscles in the different conditions. The different demands can arise from differences in the external moments appearing at TD (Wright, Neptune, van den Bogert, & Nigg, 2) and in the load sharing with passive structures. Furthermore, differences in the muscle potential as a result of the force velocity and force length relationships would also change the activation demands (van Soest & Bobbert, 1993). Proactive adjustments in segment orientation would probably serve to minimize the stabilization requirements of the biological system, on the one hand by reducing the external moments acting around the joints and on the other by taking the best advantage of the system s self-stabilizing mechanisms. Therefore, the higher inversion observed when landing onto the laterally inclined surface would prevent, at least partially, a sudden, rapid inversion tilt that would happen when landing in a neutral position onto a laterally inclined surface. Such an adaptation of foot sole inclination to the ground done at the ankle level would place that joint in a March 27, Vol. 39, No. 2 99

12 G. Morey-Klapsing, A. Arampatzis, & G.-P. Brüggemann Level vs. Lateral Level vs. Medial Lateral vs. Medial PL PB EMG Activity TA FIGURE 8. Pairwise comparison of the electromyographic (EMG) activities between the different surface conditions (level vs. lateral, level vs. medial, and lateral vs. medial). The different rows contain the studied muscles (N = 24): peroneus brevis (PB), peroneus longus (PL), and tibialis anterior (TA). The zero in the time axis corresponds to touchdown. The shaded areas indicate relevant differences, that is, significant (p <.5) and above 1% of the maximal value of the level condition. very exposed position. A flexible and well-oriented forefoot could prevent the mentioned tilt and also reduce the lever arm of the GRF acting around the ankle joint. On all three surfaces, a few milliseconds after TD, the forefoot and rear foot started everting (Figure 6). The strong medial passive constraints (e.g., spring ligament) as well as active muscles (e.g., tibialis posterior and peronei) will counteract the external everting moment. The fact that no significant everting shift was found between the level and the medially inclined surfaces could reflect a different strategy used for medially inclined surfaces as compared with that used for laterally inclined ones. Therefore, allowing a slight inverted position at TD when landing onto the medially inclined surface could provide the strong medial passive constraints a longer path to damp the GRF causing the everting moment. The important role of passive self-stabilizing mechanisms in easing the stabilizing task of the central nervous system is further supported by the findings of O Connor and Hamill (24), who studied running in frontal plane wedged shoes, and suggested that acute changes in frontal plane motion may not require an active response by the neuromuscular system (p. 76). In conclusion, we found surface-specific adjustments in frontal plane forefoot orientation and in muscle activation before TD. Altering of segment orientation and activation levels can change the potential of passive (bony and ligamentous) and active (muscles) structures to counteract imminent destabilizing forces. That means that the destabilizing moments occurring during landings as well as the potential of the biological system to cope with them may be influenced before TD. Correct prediction of the disturbance to come would therefore allow a better adjustment of the involved structures. Segment orientation and muscle activation could be tuned appropriately before the foot touches the ground, in that way taking better advantage of the selfstabilizing mechanisms. Such proactive adjustments would further relieve the neural system because the stabilizing demands would be reduced. Whereas the presented results do not prove that the mechanisms just described in this paragraph are used, they strongly support that view. We suggest that the motor system uses the proactive adjustments observed at the forefoot level to achieve the most favorable conditions for an effective subsequent exploitation of the self-stabilizing mechanisms. REFERENCES Arampatzis, A. J., Brüggemann, G. P., & Morey-Klapsing, G. (22). A three-dimensional shank foot model to determine the 1 Journal of Motor Behavior

13 Proactive Forefoot Control in Landing Level vs. Lateral Level vs. Medial Lateral vs. Medial GL GM 12 EMG Activity Sol FIGURE 9. Pairwise comparison of the electromyographic (EMG) activities between the different surface conditions (level vs. lateral, level vs. medial, and lateral vs. medial). The different rows contain the studied muscles (n = 24): gastrocnemius lateralis (GL), gastrocnemius medialis (GM), and soleus (Sol). The zero in the time axis corresponds to touchdown. The shaded areas indicate relevant differences, that is, significant (p <.5) and above 1% of the maximal value of the level condition. foot motion during landings. Medicine & Science in Sports & Exercise, 34, Arampatzis, A., Morey-Klapsing, G. M., & Brüggemann, G. P. (23). The effect of falling height on muscle activity and foot motion during landings. Journal of Electromyography and Kinesiology, 13, Caster, B. L., & Bates, B. T. (1995). The assessment of mechanical and neuromuscular response strategies during landing. Medicine & Science in Sports & Exercise, 27, DeVita, P., & Skelly, W. (1992). Effect of landing stiffness on joint kinetics and energetics in the lower extremity. Medicine & Science in Sports & Exercise, 1, Dufek, J. S., & Bates, B. T. (199). The evaluation and prediction of impact forces during landings. Medicine & Science in Sports & Exercise, 22, Duncan, A., & McDonagh, M. J. (2). Stretch reflex distinguished from pre-programmed muscle activations following landing impacts in man. The Journal of Physiology, 562, Dyhre-Poulsen, P., Simonsen, E. B., & Voigt, M. (1991). Dynamic control of muscle stiffness and H reflex modulation during hopping and jumping in man. The Journal of Physiology, 437, Flanagan, J. R., Vetter, P., Johansson, R. S., & Wolpert, D. M. (23). Prediction precedes control in motor learning. Current Biology, 13, Grüneberg, C., Nieuwenhuijzen, P. H., & Duysens, J. (23). Reflex responses in the lower leg following landing impact on an inverting and non-inverting platform. The Journal of Physiology, 55, Isakov, E., Mizrahi, J., Solzi, P., Susak, Z., & Lotem, M. (1986). Response of the peroneal muscles to sudden inversion of the ankle during standing. International Journal of Sport Biomechanics, 2, Konradsen, L. (22). Factors contributing to chronic ankle instability: Kinesthesia and joint position sense. Journal of Athletic Training, 37, Konradsen, L., Voigt, M., & Hojsgaard, C. (1997). Ankle inversion injuries. The role of the dynamic defense mechanism. American Journal of Sports Medicine, 25, Lacquaniti, F., & Maioli, C. (1989). The role of preparation in tuning anticipatory and reflex responses during catching. The Journal of Neuroscience, 9, Loeb, G. E. (1995). Control implications of musculoskeletal mechanics. Abstracts of the Annual International Conference of the IEEE EMBS, 17, McKinley, P., & Pedotti, A. (1992). Motor strategies in landing from a jump: The role of skill in task execution. Experimental Brain Research, 9, Mizrahi, J., & Susak, Z. (1982). Analysis of parameters affecting impact force attenuation during landing in human vertical free fall. Engineering in Medicine, 11, Morey-Klapsing, G., Arampatzis, A., & Brüggemann, G. P. (25a). Joint stabilizing response to expected and unexpected tilts. Foot & Ankle, 26, Morey Klapsing, G., Arampatzis, A., & Brüggemann, G. P. March 27, Vol. 39, No. 2 11

14 G. Morey-Klapsing, A. Arampatzis, & G.-P. Brüggemann Level vs. Lateral Level vs. Medial Lateral vs. Medial Ground Reaction Force (N/kg) Lateral Medial Anterior Posterior Vertical FIGURE 1. Pairwise comparison of the ground reaction forces (GRF) between the different surface conditions: level vs. lateral, level vs. medial, and lateral vs. medial. The different rows contain the mean mediolateral, anteroposterior, and vertical GRF curves, respectively. The zero in the time axis corresponds to touchdown. The shaded areas indicate relevant differences, that is, significant (p <.5) and above 1% of the maximal value of the level condition. (25b). Joint stabilizing response to lateral and medial tilts. Clinical Biomechanics, 2, Moritz, C. T., & Farley, C. T. (24). Passive dynamics change leg mechanics for an unexpected surface during human hopping. Journal of Applied Physiology, 97, O Connor, K. M., & Hamill, J. (24). The role of selected extrinsic foot muscles during running. Clinical Biomechanics, 19, Santello, M. (25). Review of motor control mechanisms underlying impact absorption from falls. Gait & Posture, 21, Santello, M., & McDonagh, M. J. (1998). The control of timing and amplitude of EMG activity in landing movements in humans. Experimental Physiology, 83, Thompson, H. W., & McKinley, P. A. (1995). Landing from a jump: The role of vision when landing from known and unknown heights. NeuroReport, 6, van Soest, A. J., & Bobbert, M. F. (1993). The contribution of muscle properties in the control of explosive movements. Biological Cybernetics, 69, Wagner, H., & Blickhan, R. (23). Stabilizing function of antagonistic neuromusculoskeletal systems: An analytical investigation. Biological Cybernetics, 89, Wright, I. C., Neptune, R. R., van den Bogert, A. J., & Nigg, B. M. (2). The influence of foot positioning on ankle sprains. Journal of Biomechanics, 33, Submitted November 3, 25 Revised January 5, 26 Second revision February 28, Journal of Motor Behavior

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