Journal of Electromyography and Kinesiology xxx (2014) xxx–xxx
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Modulation of tibialis anterior muscle activity changes with upright stance width Thiago Lemos a,⇑, Luís A. Imbiriba b, Claudia D. Vargas a, Taian M. Vieira b,c a
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, RJ, Brazil Escola de Educação Física e Desportos, Universidade Federal do Rio de Janeiro, RJ, Brazil c Laboratorio di Ingegneria del Sistema Neuromuscolare, Politecnico di Torino, Torino, Italy b
a r t i c l e
i n f o
Article history: Received 27 February 2014 Received in revised form 20 June 2014 Accepted 15 July 2014 Available online xxxx Keywords: Posture control Surface EMG Tibialis anterior Stance width
a b s t r a c t When individuals stand with their feet apart, activation of tibialis anterior (TA) muscle seems to slightly exceed rest levels. In narrow stances, conversely, the stabilization of body lateral sways may impose marked, active demand on ankle inversors/eversors. In this study we investigate how much the modulation in TA activity, associated to center of pressure (COP) lateral sways, changes when stance width reduces. Surface EMG and COP coordinates were collected from 17 subjects at three different stances: feet apart, feet together and tandem. Pearson correlation analysis was applied to check whether the expected greater modulations in TA activity corresponded to a stronger association between fluctuations in EMG amplitude and COP lateral sways. When standing at progressively narrower stances participants showed larger fluctuations in COP lateral sways (p < 0.01) and higher EMG–COP association (p < 0.01); marked increases in TA activity were only observed in tandem stance (p < 0.001). Interestingly, more pronounced modulations in TA activity were observed for subjects showing greater association between EMG amplitude and COP sways in feet together and tandem stance (Pearson R > 0.56, p < 0.02), though not when standing with feet apart (R = 0.22, p = 0.40). These results indicate that the contribution of TA activity to lateral sway control increases for narrower stances. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction The human upright posture is often conceived as an inverted pendulum pivoted at the ankle joint, with minimal but significant contribution of hip joint (Creath et al., 2005). Ankle muscle activation seems crucial in compensating for impending forward but not backward falls during standing (Loram and Lakie, 2002; Morasso and Shieppati, 1999). Presumably because the body center of mass (COM) is on average fairly ahead of the ankle joint, reversion of forward falls demand fine and timely activation of plantar flexors (Gatev et al., 1999; Masani et al., 2013; Vieira et al., 2010). Backward sways, instead, are likely corrected by gravity rather than activation of ankle dorsal flexors; during standing, ankle dorsal flexors (e.g., tibialis anterior (TA) muscle) are activated at levels slightly above those observed at rest (Di Giulio et al., 2009; Joseph et al., 1955; Masani et al., 2013). Such infrequent instances of TA activation possibly depend on the occasional proximity of
⇑ Corresponding author. Address: Instituto de Biofísica Carlos Chagas Filho, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, Av. Brigadeiro Trompowski s/n, Cidade Universitária, Rio de Janeiro, RJ 21949-900, Brazil. E-mail address: [email protected] (T. Lemos).
COM to the ankle axis of rotation (Di Giulio et al., 2009; Joseph and Nightingale, 1956). Theoretical analysis, however, showed that postural sways occurring during standing affect differently ankle and hip muscles, depending on the stance width (Day et al., 1993; Winter et al., 1996). Specifically, when the feet are positioned closely together, lateral body sway is mainly accounted for by movements in the ankle rather than hip joint (see Fig. 8 of Day et al., 1993). Under these circumstances, activation of ankle inversors/eversors (e.g., TA muscle; Klein et al., 1996) is likely a key mechanism for the compensation of body sways in the frontal plane. Contribution of TA to ankle torque in the frontal plane has been substantiated by cadaveric and in vivo reports (Klein et al., 1996; Lee and Piazza, 2008; McCullough et al., 2011). Indeed, for ankle angles similar to those observed during standing, estimates of TA moment arm ranged from 3.8 to 16 mm (Klein et al., 1996; McCullough et al., 2011). It is therefore possible that the active contribution of TA to compensation of postural sways during standing increases for narrower stances. Indirect evidence on TA inversion torque has been further documented in response to postural perturbations applied along lateral directions (Brunt et al., 1992), in particular when subjects were asked to assume narrow stances (Henry et al., 2001). During
http://dx.doi.org/10.1016/j.jelekin.2014.07.009 1050-6411/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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T. Lemos et al. / Journal of Electromyography and Kinesiology xxx (2014) xxx–xxx
quiet standing, a recent report has evaluated variations in TA activity with postural sways exclusively for the tandem stance (Sozzi et al., 2013). It was shown that both TA activity and COP lateral sways increase when such a strictly narrow stance is maintained. Although these results suggest a marked contribution of the TA muscle to the active stabilization of lateral sways, the potential influence of different stances width (e.g., feet apart or together) on such contribution has been not investigated directly. Understanding how the nervous system activates the TA muscle when lateral stability is challenged during standing could potentially add to our current knowledge on the physiological processes leading to balance disorders (e.g., increased susceptibility to falls with age; Nelson-Wong et al., 2012; Rogers et al., 2003). In this study we therefore investigate how TA activation might be associated to different stance widths during standing. Three stances were tested, each imposing a progressively more severe challenge to stabilization in the frontal plane: feet apart, feet together and the tandem stance. Specifically, we ask whether the amount of modulation in the amplitude of surface electromyograms (EMGs) collected from the TA muscle depends on the degree of stability associated with each stance width. Greater modulations in EMG amplitude do not necessarily imply stronger association between variations in TA activity and shifts in postural sways. If fluctuations in TA activity increase for narrower stances, then we further ask whether such increase is related to postural lateral sways. In this case, given that narrower stances impose greater demands upon ankle inversors/eversors (Day et al., 1993; Winter et al., 1996), subjects exhibiting larger modulations in TA activity are expected to show stronger correlations between such modulations and center of pressure (COP) lateral sways. 2. Methods 2.1. Participants Seventeen subjects (nine females; range values; age: 19– 32 years; height: 153–186 cm; body mass 48–82 kg; BMI 18– 28 kg/m2) were recruited to participate in the study. None of the participants reported neurological or musculoskeletal diseases that could affect maintenance of standing posture. All subjects provided written informed consent prior to participation. Experiments were approved by the local ethical committee and conformed to the latest amendments set by the Declaration of Helsinki. 2.2. Experimental procedure Subjects were asked to stand quietly over a force-plate, with arms relaxed alongside their body and eyes open. Movements of head and arms were not allowed; whenever they occurred, the collected data was discarded and the trial started over. Participants were then instructed to stand quietly for 30 s at three stances: (i) feet apart, at the level of hip joints and parallel to sagittal plane; (ii) feet closely together; (iii) tandem stance, with the dominant foot behind and keeping the body weight distributed as equally as possible between legs. Acquisition commenced and ceased upon the issuing of an auditory cue. Trial order was randomized and three trials were applied for each stance with 1–2 min intervals in-between. According to a previous report, averaging three 30 s trials seems to ensure good reliability of posturographic measures (Pinsault and Vuillerme, 2009). 2.3. Data acquisition COP coordinates were calculated from the ground reaction forces measured with a force-plate (AccuSwayPLUS, AMTI). Reaction forces were sampled at 50 Hz with a 12 bits A/D converter.
Bipolar EMGs were recorded from the TA muscle of the dominant leg. Positioning of surface electrodes (Ag/AgCl, 8 mm diameter, 20 mm inter-electrode center-to-center distance) complied with SENIAM recommendations (Hermens et al., 1999). Briefly, after cleaning the skin with abrasive paste, electrodes were positioned at 1/3 of the distance between the tip of the fibula and the medial malleolus. EMGs were measured from the dominant (rear) leg as previous evidence suggests that, in response to unstable or narrowed widths stance, the TA of both legs are activated equally strongly (Dietz and Berger, 1982; Sozzi et al., 2013). EMGs were amplified by 2000 (10 – 750 Hz, anti-aliasing filter) and then digitized at 2000 Hz (MP100WS, BIOPAC Systems). Synchronization between EMG and COP coordinates was ensured through a common, digital trigger signal. 2.4. COP and EMG processing Variations in the size of postural sways and in the degree of TA activity were evaluated in terms of fluctuations in COP position and EMG amplitude. Initially, COP coordinates were low-pass filtered (5 Hz). After that, the standard deviation of COP position in the frontal plane was calculated over the whole (30 s) standing trial. Standard deviation values indicate how far and how often COP swayed away from its mean lateral position. Fluctuations in TA activity, instead, were calculated from EMG envelopes, obtained after full-wave rectification and low-pass filtering (2nd order Butterworth filter; 5 Hz cutoff) of raw EMGs. Such smoothed signal was further decimated with the same number of COP samples (i.e., 1500 samples; 30 s 50 samples/s). Finally, the coefficient of variation (COV; the standard deviation of EMG envelopes divided by their mean value) of EMG envelopes was computed over the whole standing trial, separately for each individual, trial and standing condition. Given that COV values are inherently normalized with respect to the mean value, they were unlikely affected by spurious changes in EMG amplitude typically resulting from individual, anatomical differences between subjects; e.g., fat thickness (Farina et al., 2002). Associations between COP lateral displacement and modulations in TA activity were evaluated through the cross-correlation function. EMG envelopes and COP coordinates in the frontal plane were cross-correlated and the peak correlation value (hereafter cross-correlation coefficient) occurring within a time lag within ±3 s was identified. Such temporal span was chosen in accordance with previous studies (Sozzi et al., 2013), which reported crosscorrelation peaks for the TA muscle occurring mostly within this time range. Greater cross-correlation coefficients indicate that changes in COP position and in EMG amplitude are more strongly associated between themselves. For simplification, the absolute value of the cross-correlation coefficients was used for analysis, since our main interest was on the magnitude of EMG–COP association, regardless of the phase difference between these signals. 2.5. Statistical analysis After ensuring the data distribution was not different from a Gaussian distribution (Kolmogorov–Smirnov test; p > 0.1 in all cases), repeated measures one-way ANOVA was applied to test for main effects of the three different stances on COP standard deviation, COV values and the cross-correlation coefficients. Tukey post hoc analysis was then considered for paired comparisons. Greater fluctuations in TA activity and in COP lateral position, however, do not imply that modulations in activity are associated to COP sways. In this case, for narrower stances, the fluctuations in the neural drive to TA should increase in correspondence of COP lateral sways and not sporadically throughout the standing trials. The Pearson correlation coefficient was therefore applied to check for whether changes in the degree of modulation in TA activity (i.e.,
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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COV values) were associated to the EMG–COP cross-correlation coefficient. Threshold for statistical significance was set at p 6 0.05. 3. Results 3.1. Postural sway and muscle activity The size of postural sways in the frontal plane and the degree of TA activity changed markedly with the stance width. Fig. 1 shows COP lateral displacements for a representative participant and for each of the three stances. When standing with feet apart, COP displacement were confined to 10 mm (range value; Subject 03; Fig. 1a). This figure doubled and trebled when this subject stood with his feet together and on tandem stance, respectively (Fig. 1b and c). As for the postural sways, marked changes in the amplitude of EMGs collected from TA muscles were observed between stances (Fig. 1d). While the amplitude of EMGs remained relatively constant when standing with feet apart (COV = 15%) and feet together (COV = 17%), modulations in TA activity were evident for tandem stance (COV = 94%). When considering all participants, significant changes in postural sways and in the degree of TA activity were observed. Specifically, COP displacements were larger for narrower stances (ANOVA main effect; p < 0.001). Post-hoc analysis revealed that COP standard deviation in feet apart stance was smaller than in feet together (p < 0.001) and tandem (p < 0.001) stances (Fig. 2a). Increases in COP displacement from feet together to tandem stances were not similarly large though still statistically significant (p < 0.001). Statistical differences between standing conditions were also observed for COV values calculated from EMG envelopes (ANOVA main effect; p < 0.001; Fig. 2b). COV mean value obtained for tandem stance was higher than that observed during feet apart and feet together (p < 0.001 for both cases); there were no changes in COV values from feet apart to feet together (p = 0.65). Moreover, during tandem stance COV values showed a marked variability across subjects (Fig. 2b). 3.2. Cross-correlation between COP position and EMG envelopes
Fig. 2. The size of lateral postural sways, quantified through COP standard deviation (SDml) in frontal plane, is shown for each of the three standing conditions ((a); white bar: feet apart; grey bar: feet together; black bar: tandem stance). The degree of modulation of TA activity (b) was computed for each stance width as the coefficient of variation (COV) of EMG envelopes (see Section 2). The EMG–COP cross-correlation coefficient (c) is shown as absolute values (see Section 2). Data is presented as mean ± SD. *Significant different from feet apart; #Significant different from feet together.
Regardless of the standing condition, cross-correlation coefficients between EMG envelopes and COP displacements varied
Fig. 1. Postural sway and modulation of TA activity for a single representative subject are shown for sagittal (forward–backward) and frontal (lateral) planes during feet apart (a), feet together (b) and tandem (c) stances. Schematic illustrations (in reduced scale) of feet position during each stance are shown in each panel. EMGs collected from the tibialis anterior (TA) muscle for the same subject are shown in (d), separately for each feet position (from top to bottom: feet apart, feet together and tandem).
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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markedly across participants. Some subjects exhibited relatively high cross-correlation coefficients (Fig. 3a). Others, instead, yielded clearly low cross-correlation coefficients (Fig. 3b). Across participants, indeed, peaks in EMG–COP cross-correlation function spanned a somewhat wide range for each stance. Besides this large variability, the temporal association between fluctuations in EMG envelopes and in COP position increased significantly from the widest to the narrowest stance (ANOVA main effect; p < 0.0001; Fig. 2c); cross-correlation coefficients were lower for the feet apart than for the feet together (p = 0.05) and tandem stances (p < 0.001), being also lower for the feet together than for the tandem stance (p = 0.03). 3.3. Size of fluctuation in muscle activity in relation to EMG–COP association The size of fluctuations in EMG amplitude increased with the strength of the temporal association between modulations in COP position and in EMG amplitude, only for the feet together and tandem stances. Specifically, significant association between COV values and EMG–COP cross-correlation coefficients were observed for the feet together (Pearson R = 0.62; p = 0.008; Fig. 4b) and tandem (Pearson R = 0.56; p = 0.02; Fig. 4c) though not for feet apart stance (R = 0.22; p = 0.40; Fig. 4a). 4. Discussion In this study we evaluated whether the amount of modulation in TA activity changes in correspondence to COP lateral displacement for different stance widths. Previous work has reported increases in TA activity in response to postural perturbations in lateral direction (Brunt et al., 1992; Henry et al., 2001) and in the strictly narrow, tandem stance (Sozzi et al., 2013). The present study goes further and provides evidence that, when standing at progressively narrower stances, fluctuations in TA activity are significantly more associated to lateral COP sways. 4.1. Narrow stances impose greater active demands upon the tibialis anterior muscle Reducing the stance width resulted in a significant increase in COP lateral sways, with marked changes in TA activation for the
narrower stances. Lateral sways were at least three times greater in feet together and tandem stances when compared to those observed for the feet apart stance (Fig. 2); previous studies reported similarly larger COP displacement for narrower stances (Day et al., 1993; Winter et al., 1996). Such augmented COP sway is presumably due to a weaker mechanical linkage between hip and ankle joints as stance width decreases (Day et al., 1993). For wider stances, hip and ankle joints are more strongly mechanically coupled in the frontal plane. In this case, ankle and hip joint angle changes approximately equally with lateral shifts in body COM. For narrower stances, conversely, body sways in the frontal plane result predominantly from variations in the ankle rather than hip joint angle. It is therefore reasonable to expect the narrower stances to impose greater demands upon muscles contributing to ankle torque in the frontal plane (e.g., TA muscle; Lee and Piazza, 2008). Indeed, theoretical reports predict a somewhat strong reliance on ankle inversors/eversors for the compensation of body lateral sways (Day et al., 1993; Winter et al., 1996). Experimental evidence showing greater EMG amplitudes in response to disturbances applied along lateral directions (Brunt et al., 1992; Henry et al., 2001) has substantiated these predictions. Moreover, in agreement with a previous study (Sozzi et al., 2013), our results show significant increases in the amplitude of EMG collected from the TA muscle when participants stood in tandem position (Fig. 1d). The larger fluctuations in EMG amplitude and in COP sways reported in Fig. 2, however, are not necessarily associated between themselves. Cross-correlation analysis revealed that the greater modulations in TA activity and COP sways were indeed associated. Peaks in the cross-correlation function calculated between EMG envelopes and COP sways were within the range of values typically reported in the literature (Gatev et al., 1999; Sozzi et al., 2013). Interestingly, these peak values largely depended on subjects’ stance width, being progressively higher for the narrower stances (Fig. 2c). In addition, they showed a significant, positive association with the size of fluctuations in EMG amplitude for narrow stances (Fig. 4). Results presented in Fig. 4 specifically indicate that for narrower stances, TA activity was modulated to larger extents and in correspondence of COP sways. It must be noted that the size of both COP displacements (Fig. 2a) and fluctuations in EMG amplitude (Fig. 2b) increased with the decrease of stance width. A positive correlation between COP displacements and COV values would not however indicate if the greater modulations in TA activity for the narrower stance widths were temporally associated to COP sways. Our results shown in Fig. 4 do suggest a significant effect of stance width on the association between the amount of neural drive to the TA muscle and COP sways. 4.2. How does the contribution of tibialis anterior to body stabilization depend on stance width?
Fig. 3. An example of associated fluctuations in EMG amplitude and COP lateral sway from two representative subjects in tandem stance is shown. To highlight the associations between changes in TA activation and in COP position, EMG envelopes (black traces) and COP (grey traces) are presented for a relatively short (15 s) epoch. Subject 02 (a) shows higher cross-correlation coefficient (0.50) and COV (125%) values when compared to subject 08 ((b); cross-correlation coefficient of 0.24; COV = 19%).
When subjects stood at a comfortable posture, marginal changes in TA activation were most commonly observed (Fig. 2b; see also Joseph et al., 1955; Joseph and Nightingale, 1956; Masani et al., 2013). Likely because of such muscle silencing at a comfortable stance, changes in TA fibers’ length reflect strongly the changes in ankle joint angle (Di Giulio et al., 2009); in this case TA is thus probably more suited to signaling changes in body COM than to compensating them, i.e., it serves a proprioceptive role. However, our results possibly suggest the TA muscle serves different roles for the control of standing posture, depending on how large the stance width is. When subjects stood at narrower stances, we observed that modulations in TA activity were markedly greater and more strongly associated to COP lateral shifts (Fig. 4). Considering an active muscle unlikely constitutes an accurate source of proprioception (Loram et al., 2009), our findings suggest
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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Fig. 4. Scatter plots showing the degree of modulation of TA activity (i.e., COV values), in the ordinate, and the cross-correlation coefficient between EMG envelopes and COP lateral sways, in the abscissa, for the feet apart (a), feet together (b) and tandem (c) positions. Least-squares regression lines are shown to emphasize the changes in the relationship between COV and cross-correlation coefficient among stances.
the TA role shifts from signaling body sways (proprioceptive role) to providing significant contributions to body lateral stabilization (active role) when subjects stand at progressively narrower stances. Such a switch of TA postural role with stance width raises the question of which ankle muscle, if any, is best suited to provide information about the ankle joint angular position and velocity in narrow stances. One possibility posits different roles for different regions of individual muscles. Di Giulio et al. (2009), for example, observed opposite changes in the length of fibers occupying the deep and superficial TA regions (see their Fig. 3D and E). In addition, anatomical studies revealed inhomogeneous distributions in the number of alpha and gamma motoneurons (Iliya and Dum, 1984) and of muscle spindles (Barker and Chin, 1960) between TA compartments. If length changes and activation distributes unevenly across distinct TA regions, then TA fibers occupying different locations could possibly serve different roles for the control of standing posture. According to a recent report, however, in the presence of TA activity during standing, changes in fascicle length occurring in different TA regions were decoupled from postural sways (Day et al., 2013). In spite of such contradiction on the potential regionalization of the TA proprioceptive role during standing, these previous accounts were not sought to investigate the regional changes in TA architecture and activation with stance width. This issue could be tested with recent technologies combining ultrasound imaging and surface electromyography (Botter et al., 2013). 4.3. Practical implications of the active contribution of tibialis anterior for lateral body stabilization From a practical point of view, the potential active role of TA during standing could have relevant implications for the understanding and for the prevention of falls during different circumstances. It is well documented, for instance, that aging is accompanied by severe impairment in body lateral stability, which seems to raise the overall risk of fall in the elderly (Bonnet et al., 2013; Maki et al., 1994; reviewed in Rogers and Mille, 2003). Interestingly, reduced strength of ankle dorsiflexors has been suggested a main factor distinguishing fallers from non-fallers (LaRoche et al., 2010; Lord et al., 1991). It should be noted that crucial demands for active stabilization of ankle lateral movements might not be imposed exclusively during standing. A recent survey (Robinovitch et al., 2013) indeed revealed that: (i) subjects fall more frequently when walking forward; (ii) weight shifting is the most frequent cause of falls. Both conditions demand a fine control of body position and motion in the frontal plane (MacKinnon and Winter, 1993). In addition, subjects at increased risk of fall, such
as severe parkinsonian patients, seem to often maintain a reduced base of support while standing and walking (Charllet et al., 1998). If the TA muscle serves a distinctive, active role for the stabilization of body lateral sways at narrow stances, improving the neural control of this muscle should therefore be conceived in rehabilitation and training programs aimed at fall prevention.
4.4. Some considerations on inter-individual variability and EMG recordings In tandem stance, the size of fluctuations in EMG amplitude varied remarkably between subjects. Differences in the intrinsic ankle stiffness between subjects could possibly explain such variability. Direct measurements of ankle stiffness, for example, yielded values ranging from about 40% to 90% of the load stiffness (i.e., the gravitational toppling torque; Loram and Lakie, 2002). Moreover, large inter-individual variability has been reported for TA stiffness (Almqvist et al., 2007; Maganaris and Paul, 1999). Subjects exhibiting lower ankle stiffness are therefore expected to rely more strongly on muscle activation to maintain their standing posture. Different load sharing between other synergists contributing to ankle torque in the frontal plane (e.g., gastrocnemius; Lee and Piazza, 2008; Vieira et al., 2013) is an alternative, or perhaps an additional, possibility accounting for the large between-subject variability in tandem stance. Such factors likely explain the slightly lower correlation values observed when comparing the tandem with the feet together stance (cf. Pearson R values in Fig. 4c and b respectively). Regardless of whether COV variability reported in Fig. 4c was explained by individual differences in ankle stiffness, in load sharing strategies or in both, distinct degrees of TA activation emerged when lateral stability was challenged. Variations in EMG amplitude might not be unequivocally related to changes in TA activation. Although we have conceived the modulation in EMG amplitude in terms of altered degree of TA activation, one could argue such modulation reflects shifts in the innervation zone in relation to electrode position (Farina et al., 2001). We however believe this possibility is unlikely for three reasons: (i) changes in TA length during standing are markedly small (200 lm; Di Giulio et al., 2009); (ii) as electrode position was the same throughout experiments, shifts in innervation zone would affect likely equally all standing conditions; (iii) our electrodes were positioned proximally to TA regions where innervation zone is typically observed (Saitou et al., 2000). Differences in the amount of fluctuations in EMG amplitude with stance width were therefore unlikely due to changes in innervation zone location. Whether these fluctuations reflect global changes in TA activity (Di Giulio et al., 2009) remains however to be investigated.
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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Conflict of interest The authors declare that they have no conflict of interest.
Acknowledgements This study was supported by CAPES-COFECUB, CNPq (Grant 478537/2012-3 to C.D.V.) and FAPERJ (Grant INST-110.842/ 2012 to T.V.; E-26/110.526/2012 to C.D.V.; E-26/102.224/2013 to L.A.I.). T.L. is recipient of a CAPES-PNPD fellowship. This study was supported by the Italian bank foundations, ‘‘Compagnia di San Paolo’’ and ‘‘Fondazione Cassa di Risparmio di Torino’’.
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Loram ID, Lakie M, Di Giulio I, Maganaris CN. The consequences of short-range stiffness and fluctuating muscle activity for proprioception of postural joint rotations: the relevance to human standing. J Neurophysiol 2009;102:460–74. Lord SR, Clark RD, Webster IW. Postural stability and associated physiological factors in a population of aged persons. J Gerontol 1991;46:M69–76. MacKinnon CD, Winter DA. Control of whole body balance in the frontal plane during human walking. J Biomech 1993;26:633–44. Maganaris CN, Paul JP. In vivo human tendon mechanical properties. J Physiol 1999;521:307–13. Maki BE, Holliday PJ, Topper AK. A prospective study of postural balance and risk of falling in an ambulatory and independent elderly population. J Gerontol 1994;49:M72–84. Masani K, Sayenko DG, Vette AH. What triggers the continuous muscle activity during upright standing? Gait Posture 2013;37:72–7. McCullough MBA, Ringleb SI, Arai K, Kitaoka HB, Kaufman KR. Moment arms of the ankle throughout the range of motion in three planes. Foot Ankle Int 2011;32:300–6. Morasso PG, Shieppati M. Can muscle stiffness alone stabilize upright standing? J Neurophysiol 1999;82:1622–6. Nelson-Wong E, Appell R, McKay M, Nawaz H, Roth J, Sigler R, et al. Increased fall risk is associated with elevated co-contraction about the ankle during static balance challenges in older adults. Eur J Appl Physiol 2012;112:1379–89. Pinsault N, Vuillerme N. Test–retest reliability of centre of foot pressure measures to assess postural control during unperturbed stance. Med Eng Phys 2009;31:276–86. Robinovitch SN, Feldman F, Yang Y, Schonnop R, Leung PM, Sarraf T, et al. Video capture of the circumstances of falls in elderly people residing in long-term care: an observational study. Lancet 2013;381:47–54. Rogers MW, Mille M-L. Lateral stability and falls in older people. Exerc Sport Sci Rev 2003;31:182–7. Rogers ME, Rogers NL, Takeshima N, Islam MM. Methods to assess and improve the physical parameters associated with fall risk in older adults. Prev Med 2003;36:255–64. Saitou K, Masuda T, Michikami D, Kojima R, Okada M. Innervation zones of the upper and lower limb muscles estimated by using multichannel surface EMG. J Hum Ergol 2000;29:35–52. Sozzi S, Honeine J-L, Do M-C, Schieppati M. Leg muscle activity during tandem stance and the control of body balance in the frontal plane. Clin Neurophysiol 2013;124:1175–86. Vieira TMM, Windhorst U, Merletti R. Is the stabilization of quiet upright stance in humans driven by synchronized modulations of the activity of medial and lateral gastrocnemius muscles? J Appl Physiol 2010;108:85–97. Vieira TMM, Minetto MA, Hodson-Tole EF, Botter A. How much does the human medial gastrocnemius muscle contribute to ankle torques outside the sagittal plane? Hum Mov Sci 2013;32:753–67. Winter DA, Prince F, Frank JS, Powell C, Zabjek KF. Unified theory regarding A/P and M/L balance in quiet stance. J Neurophysiol 1996;75:2334–43.
Thiago Lemos is graduated in Physical Education (2004), and obtained the D.Sc dregree in Physiology (emphasis in Neuroscience) from the Federal University of Rio de Janeiro (2012). Currently he is a Postdoctoral fellow from the Graduate Program in Rehabilitation Science, Centro Universitário Augusto Motta, Brazil. His research interest in focused on the cognitive and neuromuscular processes underlying human postural control.
Luis Aureliano Imbiriba is graduated in Physical Education (1994), and obtained his M.Sc. in Biomedical Engineering (1997) and his D.Sc. in Physiology (2007) from the Federal University of Rio de Janeiro, Brazil. Currently he is an Adjunct Professor within the School of Physical Education and Sports from the Federal University of Rio de Janeiro. His main interests are postural control, neural control of movement and motor imagery.
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
T. Lemos et al. / Journal of Electromyography and Kinesiology xxx (2014) xxx–xxx Claudia Domingues Vargas is a biologist. She did her master in Biophysics (1992) and her Ph.D. in Biological Science at the Federal University of Rio de Janeiro (1997). She is Associate Professor at the Department of Neurobiology of the Institute of Biophysics Carlos Chagas Filho, Federal University of Rio de Janeiro, since 1997. Her main scientific interests are motor cognition, control of posture and voluntary movement and brain plasticity after peripheral lesions. She is founder and head of the Laboratory of Neuroscience and Rehabilitation of the Institute of Neurology Deolindo Couto of the Federal University of Rio de Janeiro, funded by FAPERJ and CNPq. She has also been working on the interdisciplinary domain of Neuromathematics, in association with the Núcleo de Apoio à Pesquisa em Modelagem Estocástica e Complexidade (NUMEC) of IME/USP. She is also principal investigator at the Center of Research, Innovation and Dissemination in Neuromathematics (NeuroMat), funded by FAPESP since 2013.
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Taian M.M. Vieira is graduated in Physical Education and, in January 2005, obtained his M.Sc. in Biomedical Engineering, from the Federal University of Rio de Janeiro, Brazil. With a doctoral scholarship provided by the Brazilian Research Council (CNPq), at January 2011, he obtained the Ph.D. degree in Biomedical Engineering from the Politecnico di Torino, Italy. Throughout his doctoral studies, he received two student presentation awards by international, scientific societies. Recently, in July 2011, he was the inaugural winner of the Emerging Scientist Award of the International Society of Biomechanics. Currently, Taian Vieira is Adjunct Professor within the School of Sports Science, at the Federal University of Rio de Janeiro, Brazil. His research interest is chiefly focused on the use of electromyography to gain insights into the control of human posture, movement and performance.
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
Contents lists available at ScienceDirect
Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Modulation of tibialis anterior muscle activity changes with upright stance width Thiago Lemos a,⇑, Luís A. Imbiriba b, Claudia D. Vargas a, Taian M. Vieira b,c a
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, RJ, Brazil Escola de Educação Física e Desportos, Universidade Federal do Rio de Janeiro, RJ, Brazil c Laboratorio di Ingegneria del Sistema Neuromuscolare, Politecnico di Torino, Torino, Italy b
a r t i c l e
i n f o
Article history: Received 27 February 2014 Received in revised form 20 June 2014 Accepted 15 July 2014 Available online xxxx Keywords: Posture control Surface EMG Tibialis anterior Stance width
a b s t r a c t When individuals stand with their feet apart, activation of tibialis anterior (TA) muscle seems to slightly exceed rest levels. In narrow stances, conversely, the stabilization of body lateral sways may impose marked, active demand on ankle inversors/eversors. In this study we investigate how much the modulation in TA activity, associated to center of pressure (COP) lateral sways, changes when stance width reduces. Surface EMG and COP coordinates were collected from 17 subjects at three different stances: feet apart, feet together and tandem. Pearson correlation analysis was applied to check whether the expected greater modulations in TA activity corresponded to a stronger association between fluctuations in EMG amplitude and COP lateral sways. When standing at progressively narrower stances participants showed larger fluctuations in COP lateral sways (p < 0.01) and higher EMG–COP association (p < 0.01); marked increases in TA activity were only observed in tandem stance (p < 0.001). Interestingly, more pronounced modulations in TA activity were observed for subjects showing greater association between EMG amplitude and COP sways in feet together and tandem stance (Pearson R > 0.56, p < 0.02), though not when standing with feet apart (R = 0.22, p = 0.40). These results indicate that the contribution of TA activity to lateral sway control increases for narrower stances. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction The human upright posture is often conceived as an inverted pendulum pivoted at the ankle joint, with minimal but significant contribution of hip joint (Creath et al., 2005). Ankle muscle activation seems crucial in compensating for impending forward but not backward falls during standing (Loram and Lakie, 2002; Morasso and Shieppati, 1999). Presumably because the body center of mass (COM) is on average fairly ahead of the ankle joint, reversion of forward falls demand fine and timely activation of plantar flexors (Gatev et al., 1999; Masani et al., 2013; Vieira et al., 2010). Backward sways, instead, are likely corrected by gravity rather than activation of ankle dorsal flexors; during standing, ankle dorsal flexors (e.g., tibialis anterior (TA) muscle) are activated at levels slightly above those observed at rest (Di Giulio et al., 2009; Joseph et al., 1955; Masani et al., 2013). Such infrequent instances of TA activation possibly depend on the occasional proximity of
⇑ Corresponding author. Address: Instituto de Biofísica Carlos Chagas Filho, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, Av. Brigadeiro Trompowski s/n, Cidade Universitária, Rio de Janeiro, RJ 21949-900, Brazil. E-mail address: [email protected] (T. Lemos).
COM to the ankle axis of rotation (Di Giulio et al., 2009; Joseph and Nightingale, 1956). Theoretical analysis, however, showed that postural sways occurring during standing affect differently ankle and hip muscles, depending on the stance width (Day et al., 1993; Winter et al., 1996). Specifically, when the feet are positioned closely together, lateral body sway is mainly accounted for by movements in the ankle rather than hip joint (see Fig. 8 of Day et al., 1993). Under these circumstances, activation of ankle inversors/eversors (e.g., TA muscle; Klein et al., 1996) is likely a key mechanism for the compensation of body sways in the frontal plane. Contribution of TA to ankle torque in the frontal plane has been substantiated by cadaveric and in vivo reports (Klein et al., 1996; Lee and Piazza, 2008; McCullough et al., 2011). Indeed, for ankle angles similar to those observed during standing, estimates of TA moment arm ranged from 3.8 to 16 mm (Klein et al., 1996; McCullough et al., 2011). It is therefore possible that the active contribution of TA to compensation of postural sways during standing increases for narrower stances. Indirect evidence on TA inversion torque has been further documented in response to postural perturbations applied along lateral directions (Brunt et al., 1992), in particular when subjects were asked to assume narrow stances (Henry et al., 2001). During
http://dx.doi.org/10.1016/j.jelekin.2014.07.009 1050-6411/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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T. Lemos et al. / Journal of Electromyography and Kinesiology xxx (2014) xxx–xxx
quiet standing, a recent report has evaluated variations in TA activity with postural sways exclusively for the tandem stance (Sozzi et al., 2013). It was shown that both TA activity and COP lateral sways increase when such a strictly narrow stance is maintained. Although these results suggest a marked contribution of the TA muscle to the active stabilization of lateral sways, the potential influence of different stances width (e.g., feet apart or together) on such contribution has been not investigated directly. Understanding how the nervous system activates the TA muscle when lateral stability is challenged during standing could potentially add to our current knowledge on the physiological processes leading to balance disorders (e.g., increased susceptibility to falls with age; Nelson-Wong et al., 2012; Rogers et al., 2003). In this study we therefore investigate how TA activation might be associated to different stance widths during standing. Three stances were tested, each imposing a progressively more severe challenge to stabilization in the frontal plane: feet apart, feet together and the tandem stance. Specifically, we ask whether the amount of modulation in the amplitude of surface electromyograms (EMGs) collected from the TA muscle depends on the degree of stability associated with each stance width. Greater modulations in EMG amplitude do not necessarily imply stronger association between variations in TA activity and shifts in postural sways. If fluctuations in TA activity increase for narrower stances, then we further ask whether such increase is related to postural lateral sways. In this case, given that narrower stances impose greater demands upon ankle inversors/eversors (Day et al., 1993; Winter et al., 1996), subjects exhibiting larger modulations in TA activity are expected to show stronger correlations between such modulations and center of pressure (COP) lateral sways. 2. Methods 2.1. Participants Seventeen subjects (nine females; range values; age: 19– 32 years; height: 153–186 cm; body mass 48–82 kg; BMI 18– 28 kg/m2) were recruited to participate in the study. None of the participants reported neurological or musculoskeletal diseases that could affect maintenance of standing posture. All subjects provided written informed consent prior to participation. Experiments were approved by the local ethical committee and conformed to the latest amendments set by the Declaration of Helsinki. 2.2. Experimental procedure Subjects were asked to stand quietly over a force-plate, with arms relaxed alongside their body and eyes open. Movements of head and arms were not allowed; whenever they occurred, the collected data was discarded and the trial started over. Participants were then instructed to stand quietly for 30 s at three stances: (i) feet apart, at the level of hip joints and parallel to sagittal plane; (ii) feet closely together; (iii) tandem stance, with the dominant foot behind and keeping the body weight distributed as equally as possible between legs. Acquisition commenced and ceased upon the issuing of an auditory cue. Trial order was randomized and three trials were applied for each stance with 1–2 min intervals in-between. According to a previous report, averaging three 30 s trials seems to ensure good reliability of posturographic measures (Pinsault and Vuillerme, 2009). 2.3. Data acquisition COP coordinates were calculated from the ground reaction forces measured with a force-plate (AccuSwayPLUS, AMTI). Reaction forces were sampled at 50 Hz with a 12 bits A/D converter.
Bipolar EMGs were recorded from the TA muscle of the dominant leg. Positioning of surface electrodes (Ag/AgCl, 8 mm diameter, 20 mm inter-electrode center-to-center distance) complied with SENIAM recommendations (Hermens et al., 1999). Briefly, after cleaning the skin with abrasive paste, electrodes were positioned at 1/3 of the distance between the tip of the fibula and the medial malleolus. EMGs were measured from the dominant (rear) leg as previous evidence suggests that, in response to unstable or narrowed widths stance, the TA of both legs are activated equally strongly (Dietz and Berger, 1982; Sozzi et al., 2013). EMGs were amplified by 2000 (10 – 750 Hz, anti-aliasing filter) and then digitized at 2000 Hz (MP100WS, BIOPAC Systems). Synchronization between EMG and COP coordinates was ensured through a common, digital trigger signal. 2.4. COP and EMG processing Variations in the size of postural sways and in the degree of TA activity were evaluated in terms of fluctuations in COP position and EMG amplitude. Initially, COP coordinates were low-pass filtered (5 Hz). After that, the standard deviation of COP position in the frontal plane was calculated over the whole (30 s) standing trial. Standard deviation values indicate how far and how often COP swayed away from its mean lateral position. Fluctuations in TA activity, instead, were calculated from EMG envelopes, obtained after full-wave rectification and low-pass filtering (2nd order Butterworth filter; 5 Hz cutoff) of raw EMGs. Such smoothed signal was further decimated with the same number of COP samples (i.e., 1500 samples; 30 s 50 samples/s). Finally, the coefficient of variation (COV; the standard deviation of EMG envelopes divided by their mean value) of EMG envelopes was computed over the whole standing trial, separately for each individual, trial and standing condition. Given that COV values are inherently normalized with respect to the mean value, they were unlikely affected by spurious changes in EMG amplitude typically resulting from individual, anatomical differences between subjects; e.g., fat thickness (Farina et al., 2002). Associations between COP lateral displacement and modulations in TA activity were evaluated through the cross-correlation function. EMG envelopes and COP coordinates in the frontal plane were cross-correlated and the peak correlation value (hereafter cross-correlation coefficient) occurring within a time lag within ±3 s was identified. Such temporal span was chosen in accordance with previous studies (Sozzi et al., 2013), which reported crosscorrelation peaks for the TA muscle occurring mostly within this time range. Greater cross-correlation coefficients indicate that changes in COP position and in EMG amplitude are more strongly associated between themselves. For simplification, the absolute value of the cross-correlation coefficients was used for analysis, since our main interest was on the magnitude of EMG–COP association, regardless of the phase difference between these signals. 2.5. Statistical analysis After ensuring the data distribution was not different from a Gaussian distribution (Kolmogorov–Smirnov test; p > 0.1 in all cases), repeated measures one-way ANOVA was applied to test for main effects of the three different stances on COP standard deviation, COV values and the cross-correlation coefficients. Tukey post hoc analysis was then considered for paired comparisons. Greater fluctuations in TA activity and in COP lateral position, however, do not imply that modulations in activity are associated to COP sways. In this case, for narrower stances, the fluctuations in the neural drive to TA should increase in correspondence of COP lateral sways and not sporadically throughout the standing trials. The Pearson correlation coefficient was therefore applied to check for whether changes in the degree of modulation in TA activity (i.e.,
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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COV values) were associated to the EMG–COP cross-correlation coefficient. Threshold for statistical significance was set at p 6 0.05. 3. Results 3.1. Postural sway and muscle activity The size of postural sways in the frontal plane and the degree of TA activity changed markedly with the stance width. Fig. 1 shows COP lateral displacements for a representative participant and for each of the three stances. When standing with feet apart, COP displacement were confined to 10 mm (range value; Subject 03; Fig. 1a). This figure doubled and trebled when this subject stood with his feet together and on tandem stance, respectively (Fig. 1b and c). As for the postural sways, marked changes in the amplitude of EMGs collected from TA muscles were observed between stances (Fig. 1d). While the amplitude of EMGs remained relatively constant when standing with feet apart (COV = 15%) and feet together (COV = 17%), modulations in TA activity were evident for tandem stance (COV = 94%). When considering all participants, significant changes in postural sways and in the degree of TA activity were observed. Specifically, COP displacements were larger for narrower stances (ANOVA main effect; p < 0.001). Post-hoc analysis revealed that COP standard deviation in feet apart stance was smaller than in feet together (p < 0.001) and tandem (p < 0.001) stances (Fig. 2a). Increases in COP displacement from feet together to tandem stances were not similarly large though still statistically significant (p < 0.001). Statistical differences between standing conditions were also observed for COV values calculated from EMG envelopes (ANOVA main effect; p < 0.001; Fig. 2b). COV mean value obtained for tandem stance was higher than that observed during feet apart and feet together (p < 0.001 for both cases); there were no changes in COV values from feet apart to feet together (p = 0.65). Moreover, during tandem stance COV values showed a marked variability across subjects (Fig. 2b). 3.2. Cross-correlation between COP position and EMG envelopes
Fig. 2. The size of lateral postural sways, quantified through COP standard deviation (SDml) in frontal plane, is shown for each of the three standing conditions ((a); white bar: feet apart; grey bar: feet together; black bar: tandem stance). The degree of modulation of TA activity (b) was computed for each stance width as the coefficient of variation (COV) of EMG envelopes (see Section 2). The EMG–COP cross-correlation coefficient (c) is shown as absolute values (see Section 2). Data is presented as mean ± SD. *Significant different from feet apart; #Significant different from feet together.
Regardless of the standing condition, cross-correlation coefficients between EMG envelopes and COP displacements varied
Fig. 1. Postural sway and modulation of TA activity for a single representative subject are shown for sagittal (forward–backward) and frontal (lateral) planes during feet apart (a), feet together (b) and tandem (c) stances. Schematic illustrations (in reduced scale) of feet position during each stance are shown in each panel. EMGs collected from the tibialis anterior (TA) muscle for the same subject are shown in (d), separately for each feet position (from top to bottom: feet apart, feet together and tandem).
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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T. Lemos et al. / Journal of Electromyography and Kinesiology xxx (2014) xxx–xxx
markedly across participants. Some subjects exhibited relatively high cross-correlation coefficients (Fig. 3a). Others, instead, yielded clearly low cross-correlation coefficients (Fig. 3b). Across participants, indeed, peaks in EMG–COP cross-correlation function spanned a somewhat wide range for each stance. Besides this large variability, the temporal association between fluctuations in EMG envelopes and in COP position increased significantly from the widest to the narrowest stance (ANOVA main effect; p < 0.0001; Fig. 2c); cross-correlation coefficients were lower for the feet apart than for the feet together (p = 0.05) and tandem stances (p < 0.001), being also lower for the feet together than for the tandem stance (p = 0.03). 3.3. Size of fluctuation in muscle activity in relation to EMG–COP association The size of fluctuations in EMG amplitude increased with the strength of the temporal association between modulations in COP position and in EMG amplitude, only for the feet together and tandem stances. Specifically, significant association between COV values and EMG–COP cross-correlation coefficients were observed for the feet together (Pearson R = 0.62; p = 0.008; Fig. 4b) and tandem (Pearson R = 0.56; p = 0.02; Fig. 4c) though not for feet apart stance (R = 0.22; p = 0.40; Fig. 4a). 4. Discussion In this study we evaluated whether the amount of modulation in TA activity changes in correspondence to COP lateral displacement for different stance widths. Previous work has reported increases in TA activity in response to postural perturbations in lateral direction (Brunt et al., 1992; Henry et al., 2001) and in the strictly narrow, tandem stance (Sozzi et al., 2013). The present study goes further and provides evidence that, when standing at progressively narrower stances, fluctuations in TA activity are significantly more associated to lateral COP sways. 4.1. Narrow stances impose greater active demands upon the tibialis anterior muscle Reducing the stance width resulted in a significant increase in COP lateral sways, with marked changes in TA activation for the
narrower stances. Lateral sways were at least three times greater in feet together and tandem stances when compared to those observed for the feet apart stance (Fig. 2); previous studies reported similarly larger COP displacement for narrower stances (Day et al., 1993; Winter et al., 1996). Such augmented COP sway is presumably due to a weaker mechanical linkage between hip and ankle joints as stance width decreases (Day et al., 1993). For wider stances, hip and ankle joints are more strongly mechanically coupled in the frontal plane. In this case, ankle and hip joint angle changes approximately equally with lateral shifts in body COM. For narrower stances, conversely, body sways in the frontal plane result predominantly from variations in the ankle rather than hip joint angle. It is therefore reasonable to expect the narrower stances to impose greater demands upon muscles contributing to ankle torque in the frontal plane (e.g., TA muscle; Lee and Piazza, 2008). Indeed, theoretical reports predict a somewhat strong reliance on ankle inversors/eversors for the compensation of body lateral sways (Day et al., 1993; Winter et al., 1996). Experimental evidence showing greater EMG amplitudes in response to disturbances applied along lateral directions (Brunt et al., 1992; Henry et al., 2001) has substantiated these predictions. Moreover, in agreement with a previous study (Sozzi et al., 2013), our results show significant increases in the amplitude of EMG collected from the TA muscle when participants stood in tandem position (Fig. 1d). The larger fluctuations in EMG amplitude and in COP sways reported in Fig. 2, however, are not necessarily associated between themselves. Cross-correlation analysis revealed that the greater modulations in TA activity and COP sways were indeed associated. Peaks in the cross-correlation function calculated between EMG envelopes and COP sways were within the range of values typically reported in the literature (Gatev et al., 1999; Sozzi et al., 2013). Interestingly, these peak values largely depended on subjects’ stance width, being progressively higher for the narrower stances (Fig. 2c). In addition, they showed a significant, positive association with the size of fluctuations in EMG amplitude for narrow stances (Fig. 4). Results presented in Fig. 4 specifically indicate that for narrower stances, TA activity was modulated to larger extents and in correspondence of COP sways. It must be noted that the size of both COP displacements (Fig. 2a) and fluctuations in EMG amplitude (Fig. 2b) increased with the decrease of stance width. A positive correlation between COP displacements and COV values would not however indicate if the greater modulations in TA activity for the narrower stance widths were temporally associated to COP sways. Our results shown in Fig. 4 do suggest a significant effect of stance width on the association between the amount of neural drive to the TA muscle and COP sways. 4.2. How does the contribution of tibialis anterior to body stabilization depend on stance width?
Fig. 3. An example of associated fluctuations in EMG amplitude and COP lateral sway from two representative subjects in tandem stance is shown. To highlight the associations between changes in TA activation and in COP position, EMG envelopes (black traces) and COP (grey traces) are presented for a relatively short (15 s) epoch. Subject 02 (a) shows higher cross-correlation coefficient (0.50) and COV (125%) values when compared to subject 08 ((b); cross-correlation coefficient of 0.24; COV = 19%).
When subjects stood at a comfortable posture, marginal changes in TA activation were most commonly observed (Fig. 2b; see also Joseph et al., 1955; Joseph and Nightingale, 1956; Masani et al., 2013). Likely because of such muscle silencing at a comfortable stance, changes in TA fibers’ length reflect strongly the changes in ankle joint angle (Di Giulio et al., 2009); in this case TA is thus probably more suited to signaling changes in body COM than to compensating them, i.e., it serves a proprioceptive role. However, our results possibly suggest the TA muscle serves different roles for the control of standing posture, depending on how large the stance width is. When subjects stood at narrower stances, we observed that modulations in TA activity were markedly greater and more strongly associated to COP lateral shifts (Fig. 4). Considering an active muscle unlikely constitutes an accurate source of proprioception (Loram et al., 2009), our findings suggest
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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Fig. 4. Scatter plots showing the degree of modulation of TA activity (i.e., COV values), in the ordinate, and the cross-correlation coefficient between EMG envelopes and COP lateral sways, in the abscissa, for the feet apart (a), feet together (b) and tandem (c) positions. Least-squares regression lines are shown to emphasize the changes in the relationship between COV and cross-correlation coefficient among stances.
the TA role shifts from signaling body sways (proprioceptive role) to providing significant contributions to body lateral stabilization (active role) when subjects stand at progressively narrower stances. Such a switch of TA postural role with stance width raises the question of which ankle muscle, if any, is best suited to provide information about the ankle joint angular position and velocity in narrow stances. One possibility posits different roles for different regions of individual muscles. Di Giulio et al. (2009), for example, observed opposite changes in the length of fibers occupying the deep and superficial TA regions (see their Fig. 3D and E). In addition, anatomical studies revealed inhomogeneous distributions in the number of alpha and gamma motoneurons (Iliya and Dum, 1984) and of muscle spindles (Barker and Chin, 1960) between TA compartments. If length changes and activation distributes unevenly across distinct TA regions, then TA fibers occupying different locations could possibly serve different roles for the control of standing posture. According to a recent report, however, in the presence of TA activity during standing, changes in fascicle length occurring in different TA regions were decoupled from postural sways (Day et al., 2013). In spite of such contradiction on the potential regionalization of the TA proprioceptive role during standing, these previous accounts were not sought to investigate the regional changes in TA architecture and activation with stance width. This issue could be tested with recent technologies combining ultrasound imaging and surface electromyography (Botter et al., 2013). 4.3. Practical implications of the active contribution of tibialis anterior for lateral body stabilization From a practical point of view, the potential active role of TA during standing could have relevant implications for the understanding and for the prevention of falls during different circumstances. It is well documented, for instance, that aging is accompanied by severe impairment in body lateral stability, which seems to raise the overall risk of fall in the elderly (Bonnet et al., 2013; Maki et al., 1994; reviewed in Rogers and Mille, 2003). Interestingly, reduced strength of ankle dorsiflexors has been suggested a main factor distinguishing fallers from non-fallers (LaRoche et al., 2010; Lord et al., 1991). It should be noted that crucial demands for active stabilization of ankle lateral movements might not be imposed exclusively during standing. A recent survey (Robinovitch et al., 2013) indeed revealed that: (i) subjects fall more frequently when walking forward; (ii) weight shifting is the most frequent cause of falls. Both conditions demand a fine control of body position and motion in the frontal plane (MacKinnon and Winter, 1993). In addition, subjects at increased risk of fall, such
as severe parkinsonian patients, seem to often maintain a reduced base of support while standing and walking (Charllet et al., 1998). If the TA muscle serves a distinctive, active role for the stabilization of body lateral sways at narrow stances, improving the neural control of this muscle should therefore be conceived in rehabilitation and training programs aimed at fall prevention.
4.4. Some considerations on inter-individual variability and EMG recordings In tandem stance, the size of fluctuations in EMG amplitude varied remarkably between subjects. Differences in the intrinsic ankle stiffness between subjects could possibly explain such variability. Direct measurements of ankle stiffness, for example, yielded values ranging from about 40% to 90% of the load stiffness (i.e., the gravitational toppling torque; Loram and Lakie, 2002). Moreover, large inter-individual variability has been reported for TA stiffness (Almqvist et al., 2007; Maganaris and Paul, 1999). Subjects exhibiting lower ankle stiffness are therefore expected to rely more strongly on muscle activation to maintain their standing posture. Different load sharing between other synergists contributing to ankle torque in the frontal plane (e.g., gastrocnemius; Lee and Piazza, 2008; Vieira et al., 2013) is an alternative, or perhaps an additional, possibility accounting for the large between-subject variability in tandem stance. Such factors likely explain the slightly lower correlation values observed when comparing the tandem with the feet together stance (cf. Pearson R values in Fig. 4c and b respectively). Regardless of whether COV variability reported in Fig. 4c was explained by individual differences in ankle stiffness, in load sharing strategies or in both, distinct degrees of TA activation emerged when lateral stability was challenged. Variations in EMG amplitude might not be unequivocally related to changes in TA activation. Although we have conceived the modulation in EMG amplitude in terms of altered degree of TA activation, one could argue such modulation reflects shifts in the innervation zone in relation to electrode position (Farina et al., 2001). We however believe this possibility is unlikely for three reasons: (i) changes in TA length during standing are markedly small (200 lm; Di Giulio et al., 2009); (ii) as electrode position was the same throughout experiments, shifts in innervation zone would affect likely equally all standing conditions; (iii) our electrodes were positioned proximally to TA regions where innervation zone is typically observed (Saitou et al., 2000). Differences in the amount of fluctuations in EMG amplitude with stance width were therefore unlikely due to changes in innervation zone location. Whether these fluctuations reflect global changes in TA activity (Di Giulio et al., 2009) remains however to be investigated.
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
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T. Lemos et al. / Journal of Electromyography and Kinesiology xxx (2014) xxx–xxx
Conflict of interest The authors declare that they have no conflict of interest.
Acknowledgements This study was supported by CAPES-COFECUB, CNPq (Grant 478537/2012-3 to C.D.V.) and FAPERJ (Grant INST-110.842/ 2012 to T.V.; E-26/110.526/2012 to C.D.V.; E-26/102.224/2013 to L.A.I.). T.L. is recipient of a CAPES-PNPD fellowship. This study was supported by the Italian bank foundations, ‘‘Compagnia di San Paolo’’ and ‘‘Fondazione Cassa di Risparmio di Torino’’.
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Thiago Lemos is graduated in Physical Education (2004), and obtained the D.Sc dregree in Physiology (emphasis in Neuroscience) from the Federal University of Rio de Janeiro (2012). Currently he is a Postdoctoral fellow from the Graduate Program in Rehabilitation Science, Centro Universitário Augusto Motta, Brazil. His research interest in focused on the cognitive and neuromuscular processes underlying human postural control.
Luis Aureliano Imbiriba is graduated in Physical Education (1994), and obtained his M.Sc. in Biomedical Engineering (1997) and his D.Sc. in Physiology (2007) from the Federal University of Rio de Janeiro, Brazil. Currently he is an Adjunct Professor within the School of Physical Education and Sports from the Federal University of Rio de Janeiro. His main interests are postural control, neural control of movement and motor imagery.
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
T. Lemos et al. / Journal of Electromyography and Kinesiology xxx (2014) xxx–xxx Claudia Domingues Vargas is a biologist. She did her master in Biophysics (1992) and her Ph.D. in Biological Science at the Federal University of Rio de Janeiro (1997). She is Associate Professor at the Department of Neurobiology of the Institute of Biophysics Carlos Chagas Filho, Federal University of Rio de Janeiro, since 1997. Her main scientific interests are motor cognition, control of posture and voluntary movement and brain plasticity after peripheral lesions. She is founder and head of the Laboratory of Neuroscience and Rehabilitation of the Institute of Neurology Deolindo Couto of the Federal University of Rio de Janeiro, funded by FAPERJ and CNPq. She has also been working on the interdisciplinary domain of Neuromathematics, in association with the Núcleo de Apoio à Pesquisa em Modelagem Estocástica e Complexidade (NUMEC) of IME/USP. She is also principal investigator at the Center of Research, Innovation and Dissemination in Neuromathematics (NeuroMat), funded by FAPESP since 2013.
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Taian M.M. Vieira is graduated in Physical Education and, in January 2005, obtained his M.Sc. in Biomedical Engineering, from the Federal University of Rio de Janeiro, Brazil. With a doctoral scholarship provided by the Brazilian Research Council (CNPq), at January 2011, he obtained the Ph.D. degree in Biomedical Engineering from the Politecnico di Torino, Italy. Throughout his doctoral studies, he received two student presentation awards by international, scientific societies. Recently, in July 2011, he was the inaugural winner of the Emerging Scientist Award of the International Society of Biomechanics. Currently, Taian Vieira is Adjunct Professor within the School of Sports Science, at the Federal University of Rio de Janeiro, Brazil. His research interest is chiefly focused on the use of electromyography to gain insights into the control of human posture, movement and performance.
Please cite this article in press as: Lemos T et al. Modulation of tibialis anterior muscle activity changes with upright stance width. J Electromyogr Kinesiol (2014), http://dx.doi.org/10.1016/j.jelekin.2014.07.009
