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Do somatosensory conditions from the foot and ankle affect postural responses to plantar-flexor muscles fatigue during bipedal quiet stance?
Gait & Posture 36 (2012) 16–19
Contents lists available at SciVerse ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Do somatosensory conditions from the foot and ankle affect postural responses to plantar-flexor muscles fatigue during bipedal quiet stance? Petra Hlavackova a,b, Nicolas Vuillerme a,* a b
FRE 3405, AGIM (AGeing Imaging Modeling), CNRS-UJF-UPMF-EPHE, Grenoble, France Faculty of Physical Culture, Palacky University, Olomouc, Czech Republic
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 December 2009 Received in revised form 1 September 2011 Accepted 31 October 2011
The present study investigated the effects of somatosensory conditions at the foot and ankle on postural responses to plantar-flexor muscle fatigue during bipedal quiet stance. Twenty-two young healthy adults were asked to stand upright as still as possible with their eyes closed in three somatosensory conditions (normal, altered and improved) both prior to and after exercises inducing plantar-flexor muscle fatigue. In the normal condition, the postural task was executed on a firm support surface constituted by the force platform. In the altered condition, a 2-cm thick foam support surface was placed under the subjects’ feet. In the improved condition, increased cutaneous feedback at the foot and ankle was provided by strips of athletic tape applied across both their ankle joints. Muscle fatigue was induced in the plantar-flexor muscles of both legs through the execution of a repeated standing heel raise exercise. Centre of foot pressure displacements were recorded using a force platform. Results showed that plantar-flexor muscle fatigue yielded increased centre of foot pressure displacements under normal foot and ankle sensory conditions. Furthermore, this effect was exacerbated under altered foot and ankle sensory conditions and mitigated under improved foot and ankle sensory conditions. Altogether, the present findings suggested an increased reliance on somatosensory information from the foot and ankle for controlling upright posture in the presence of plantar-flexor muscle fatigue. ß 2011 Elsevier B.V. All rights reserved.
Keywords: Muscle fatigue Ankle Balance Foot Somatosensation Centre of foot pressure
1. Introduction It is now a generally held view that, depending on the sensory contexts and the neuromuscular constraints acting on an individual (e.g. [1–6]), the central nervous system can adaptively, dynamically and selectively adjust the relative contributions of sensory inputs (i.e. the sensory weights) to maintain upright stance. Among these sensory inputs, somatosensory information from the foot and ankle is recognised to play a crucial role (e.g. [7]). Various experimental manipulations of foot and ankle cutaneous mechanoreceptors have been employed to assess the contribution of feedback from cutaneous afferents. For instance, several studies have reported that (1) altering the quality of the postural support surface information by having individual standing on a compliant support surface results in a degradation of balance (e.g. [8,9]), while (2) increasing afferent feedback from cutaneous receptors in the skin of the foot and ankle through the application of foot and/or ankle appliances results in improvement of balance (e.g. [10–12]). Other studies have used plantar-flexor muscle fatiguing exercise to assess the contribution of ankle neuromuscular
* Corresponding author at: Faculty of Medicine, La Tronche Cedex, France. E-mail address: [email protected] (N. Vuillerme). 0966-6362/$ – see front matter ß 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2011.10.361
function to the control of bipedal posture. Generally, these studies reported a deterioration of bipedal postural control (e.g. [6,13–19]), which has been suggested to stem from an alteration of ankle proprioceptive acuity [20,21] and an inability to produce or sustain required force output with the fatigued plantar-flexor muscle. In the context of adaptive multisensory control of balance (e.g. [1–6]), the present study was designed to investigate the effects of somatosensory conditions from the foot and ankle on postural responses to plantar-flexor muscle fatigue during bipedal quiet stance. To achieve this goal, we employed an experimental procedure similar to that previously used in a study focussing on the effects of trunk extensor muscles fatigue on postural control during quiet standing under different somatosensory conditions from the foot and the ankle [22]. Somatosensation from the foot and the ankle was degraded by standing on a foam surface and facilitated through the increased cutaneous feedback at the foot and ankle provided by strips of athletic tape applied across both ankle joints. Postural responses were assessed by computing the displacements centre of foot pressure (CoP) using a force platform. It was hypothesised that the destabilizing effect of plantar-flexor muscle fatigue (e.g. [13–19]) would be exacerbated under altered foot and ankle sensory conditions and mitigated under improved foot and ankle sensory conditions.
P. Hlavackova, N. Vuillerme / Gait & Posture 36 (2012) 16–19 2. Methods
(2) the mean velocity of the CoP displacements which constitutes a good index of the amount of activity required to maintain stability [27].
2.1. Subjects
2.2. Experimental procedure A repeated measures design was used, wherein subjects completed trials of quiet stance by before and after fatigue in each of three conditions. Precisely, with their eyes closed, subjects stood barefoot on a force platform feet abducted at 308, heels separated by 3 cm, their arms hanging loosely by their sides and were asked to sway as little as possible in three foot and ankle sensory conditions (normal, altered and improved). In the normal condition, the postural task was executed on a firm support surface constituted by the force platform. In the altered condition, a 2-cm thick foam support surface (density of 25 kg/m3) was placed under the subjects’ feet [8]. In the improved condition, two pieces of 5-cm wide strips of athletic tape were applied in a proximal-distal direction directly to the skin in front of and behind the subject’s talocrural joints [22,23]. The first strip, starting approximately 10 cm proximal to the ankle joint line and ending 5 cm distal to the ankle joint line, was positioned directly on the skin over the anterior aspect of the ankle joint. The second strip was used posteriorly over the Achilles tendon and calcaneus. These strips of tape, used to selectively provide cutaneous sensory feedback around both ankles without the added mechanical constriction and mechanical pressure on subcutaneous structures associated with the application of ankle taping as used in athletic events, have previously been shown to improve ankle proprioceptive acuity in young healthy subjects [23]. These three foot and ankle sensory conditions were performed under two conditions of pre fatigue and post fatigue of the plantar-flexor muscle. The pre fatigue condition served as a control condition. For each foot and ankle sensory condition (normal, altered and improved), subjects performed three 32-s trials. The order of presentation of these three conditions was randomised over subjects to reduce potential order effects. In the post fatigue condition, the measurements were performed after a fatiguing procedure whose aim was to induce muscular fatigue at the plantar-flexor muscles of both legs until task failure (e.g. [6,14,16]). As previously done in other studies (e.g. [6,14,16]), standing subjects were asked to execute a repeated standing heel raise exercise, i.e. to perform toe-lifts as many times as possible following the beat of a metronome (40 beats/min). The examiner gave verbal encouragement and checked the exercise performance to ensure that the subjects worked maximally. The fatigue level was reached when subjects were no longer able to complete the exercise. Immediately after the cessation of exercise, the subjective exertion level was assessed through the Borg CR-10 scale [24]. Subjects rated their perceived fatigue in the plantar-flexor muscles as almost ‘‘extremely strong’’. Subjects rated their perceived exertion at the plantar-flexor muscles as almost ‘‘extremely strong’’ (mean Borg ratings of 8.1). The recovery process after fatigue procedures is often considered as a limitation for all fatigue experiments. In the present experiment, to ensure that balance measurement in the fatigue condition was obtained in a genuine fatigued state, various rules were respected: (1) the fatiguing exercise took place beside the force platform to minimise the time between the exercise-induced fatiguing exercise and the balance measurements (less than 1 min), (2) the fatiguing exercise was repeated prior to each balance measurement, and (3) the examiner checked that the subjects showed visible signs of fatigue and failed to perform the exercises due to fatigue. In doubtful cases, the examiner encouraged the subject to continue with a few more exercises. Note that before the completion of the present experiment, we conducted a pilot study to examine whether the proposed fatiguing protocol induced electrical signs of fatigue in plantar-flexor muscles. To this aim, electromyographic (EMG) activity of gastrocnemius and soleus muscles was recorded before and following to the exercise performance. Results showed that the exercise produced an EMG median frequency shift towards the lower frequencies ( 18%), suggesting the occurrence of physiological changes characteristic of muscle fatigue (e.g. [25]). These results ensuring that plantar-flexor muscle were fatigued at the end of the exercise hence allowed us to use this fatiguing procedure to investigate the effects of plantar-flexor muscle fatigue on postural control during bipedal quiet standing as previously done (e.g. [6,14,16]). Three additional trials for each condition of sensory inputs at the foot and ankle (normal, altered and improved) were executed, for a total of 18 trials. 2.3. Data collection and dependent measures A triangular force platform (Equi+, model PF01; Aix les Bains, France) was used to measure the displacements of the centre of foot pressure (CoP) (sampling rate: 64 Hz). Two dependant variables were used to describe subject’s postural behavior: (1) the surface area (mm2) covered by the trajectory of the CoP with a 90% confidence interval [26] which provides a measure of the size of the CoP over the support surface;
2.4. Statistical analysis The means of the three trials performed in each of experimental condition were used for statistical analyses in order to improve reliability. Results of a recent study established the ‘‘excellent’’ test–retest reliability of the CoP surface area and the CoP mean velocity parameters with three 30 s trial recordings [intra-class correlation coefficient (ICC) > 0.75] [28]. These dependant variables were tested for normality using the Shapiro–Wilk test and for equality of variance using the Levene test (Ps > 0.05). Two separate fatigues (pre fatigue vs. post fatigue) 3 foot and ankle sensory conditions (normal vs. altered vs. improved) analyses of variance (ANOVAs) with repeated measures on both factors was applied to the data surface area (mm2) covered by the trajectory of the CoP and the mean velocity of the CoP displacements. Post-hoc analyses (Newman–Keuls test) were performed whenever necessary. Level of significance was set at 0.05.
3. Results Analysis of the surface area covered by the trajectory of the CoP showed main effects of fatigue (F(1,21) = 7.86, P = 0.0106) and foot and ankle sensory condition (F(2,42) = 46.39, P = 0.0000) and a significant interaction of fatigue foot and ankle sensory conditions (F(2,42) = 4.70, P = 0.0144). As illustrated in Fig. 1, post-hoc analyses revealed that: (1) the post fatigue condition yielded a larger CoP surface area compared to the pre fatigue condition in the normal foot and ankle sensory condition (P = 0.0037; Fig. 1, left part), (2) this effect was exacerbated in the altered foot and ankle sensory condition (P = 0.0001; Fig. 1, middle part), whereas (3) no difference was found between the pre fatigue and post fatigue conditions in the improved foot and ankle sensory condition (P = 0.3170; Fig. 1, right part). Similar results were observed for the mean velocity of the CoP displacements. Indeed, analysis of the mean velocity of the CoP displacements showed main effects of fatigue (F(1,21) = 19.53, P = 0.0002) and foot and ankle sensory condition (F(2,42) = 66.50,
[(Fig._1)TD$IG]
700
Pre fatigue Post fatigue
***
600
CoP surface area (mm2)
Twenty-two young healthy adults (18 males and 4 females, age: 22.1 1.9 years; body weight: 72.1 4.5 kg; height: 174.3 3.4 cm; mean S.D.) voluntarily participated in the experiment. They gave their informed consent to the experimental procedure as required by the Helsinki declaration (1964) and the local Ethics Committee. None of the subjects presented any history of injury, surgery or pathology to either lower extremity that could affect their ability to perform the experiment.
17
500
400
300
**
200
100
0 Normal
Altered
Improved
Foot and ankle somatosensory conditions Fig. 1. Mean and standard deviation of the surface area covered by the trajectory of the CoP obtained for the three normal, altered and improved foot and ankle sensory conditions and the two conditions of pre fatigue and post fatigue of plantar-flexor muscle (**P < 0.01; ***P < 0.001).
[(Fig._2)TD$IG]
P. Hlavackova, N. Vuillerme / Gait & Posture 36 (2012) 16–19
18
25
Pre fatigue
CoP mean velocity (mm/s)
Post fatigue
***
20
15
**
10
5
0 Normal
Altered
Improved
Foot and ankle somatosensory conditions Fig. 2. Mean and standard deviation of mean velocity of the CoP displacements obtained for the three normal, altered and improved foot and ankle sensory conditions and the two conditions of pre fatigue and post fatigue of plantar-flexor muscle (**P < 0.01; ***P < 0.001).
P < 0.0000) and a significant interaction of fatigue foot and ankle sensory conditions (F(2,42) = 4.87, P = 0.0125). As illustrated in Fig. 2, post-hoc analyses revealed that: (1) the post fatigue condition yielded a higher mean velocity of the CoP displacements area compared to the pre fatigue condition in the normal foot and ankle sensory condition (P = 0.0037; Fig. 2, left part), (2) this effect was exacerbated in the altered foot and ankle sensory condition (P = 0.0001; Fig. 2, middle part), whereas (3) no difference was found between the pre fatigue and post fatigue conditions in the improved foot and ankle sensory condition (P = 0.2020; Fig. 2, right part). 4. Discussion In the normal foot and ankle sensory condition, a wider CoP surface area (Fig. 1, left part) and a larger CoP mean velocity (Fig. 2, left part) were observed in the post fatigue compared to the pre fatigue condition. These results are in accordance with previous studies reporting impaired bipedal postural control following fatiguing exercise of the plantar-flexor muscle, with a similar order of magnitude (e.g. [6,14–19]). Beyond these well-established observations, results further showed that standing on a foam support surface can modify the magnitude of the postural responses to plantar-flexors muscle fatigue, in two different ways. One the one hand, larger negative effects of fatigue on the CoP surface area (Fig. 1, middle part) and CoP mean velocity (Fig. 2, middle part) were observed in the altered condition than in the normal condition. Considering the functional significance of these two CoP-based parameters [27,29], these results suggest that plantar-flexor muscle fatigue impaired the effectiveness of the postural control system and increased the amount of postural regulatory activity required to control unperturbed bipedal posture when the quality of the postural support surface information was altered by standing on a foam support surface (altered condition) to a greater extent than when it was not (normal condition). On the other hand, the negative effects
of fatigue on the CoP surface area and CoP mean velocity observed in the two above-mentioned support surface conditions were suppressed in the improved condition (Fig. 1, right part and Fig. 2, right part, respectively). These results suggest that when the quality of the cutaneous information from the ankles was improved through the increased cutaneous feedback at the foot and ankle provided by strips of athletic tape applied across both ankle joints, plantar-flexor muscle fatigue did not impair the control unperturbed bipedal posture any more. At this point, it is important to mention the recent study by Singh et al. [11] which also reported that application of circumferential pressure near the ankle was effective in mitigating the adverse effects of plantarflexor muscle fatigue on the control of bipedal posture [11]. Interestingly, results further showed that this effectiveness was limited to certain individuals. In the latter study, however, muscle fatigue in the plantar-flexors and circumferential pressure were both applied unilaterally to the dominant side, so that the authors suggested that bilateral ankle LMF and pressure application could results in more substantial changes [11]. Along these lines, since group means could have concealed the existence of different of postural responses among the subjects, we decided to further examine the data of each subject in order to assess whether some of them were more sensitive than others to the improvement of foot and ankle somatosensation. In accordance with Singh et al.’s assumption, this individual analysis revealed that most subjects benefited from the increased cutaneous feedback at the foot and ankle provided by strips of athletic tape applied across both their ankle joints to limit the destabilizing effect of plantarflexor muscle fatigue (17 of 22 subjects decreased their CoP surface by 9%–65%, and 16 of them decreased their CoP mean velocity by 3%–26%). The observed differential postural effects of plantar-flexor muscle fatigue observed under normal, altered and improved foot and ankle somatosensory conditions support the hypothesis of the sensory reweighting hypothesis of the human postural control (e.g. [1–6]). This hypothesis supposes that the central nervous system selectively is able to adjust the relative contributions of sensory inputs (i.e. the sensory weights) to maintain upright stance depending on the sensory contexts and the neuromuscular constraints acting on the individual. Indeed, in conditions of altered ankle neuromuscular function induced by plantar-flexor muscle fatigue [20,21], recent studies have evidenced the ability of the central nervous system to efficiently use visual information [6–14], vestibular and neck somatosensory inputs [16] and haptic cues from the finger [19] providing more accurate and reliable information for ensuring adequate postural control. Along this line, it is possible that the central nervous system also increases the reliance on somatosensory inputs from the foot and ankle to maintain adequate upright stance. Interestingly, the proposed increased dependency on sensory information from the plantar sole and the ankle for controlling bipedal posture observed in the Post fatigue condition of the present study is not limited to muscle fatigue localized at the ankle joint. Indeed, a previous study has reported that the deleterious effect of trunk extensor muscles fatigue on the control of bipedal posture similarly was (1) exacerbated when young healthy subjects stood on a foam surface, and (2) mitigated in condition of increased cutaneous feedback at the foot and ankle provided by strips of athletic tape applied across both their ankle joints [22]. On the whole, these results give further support to the sensory weighting mechanisms involved in postural control according to which changes in the sensory environment and the neuromuscular state acting on the individual could bring about changes in the relative weights between information channels (e.g. [1–6]). Finally, the present findings stress the importance of sensory information from the foot and ankle to ensure an appropriate
P. Hlavackova, N. Vuillerme / Gait & Posture 36 (2012) 16–19
control of balance in the presence of plantar-flexor muscle fatigue. Since footwear represents a highly potential modifiable factor which is recognised to play a crucial role in improving balance control and reducing falls (e.g. see [10,30], for recent reviews), these results could significantly impact orthopaedic research and development. Along these lines, whether tubing (e.g. [31]) or vibrating (e.g. [32]) shoe insoles and incorporating a pressure plantar-based biofeedback system in footwear (e.g. [33]) could improve balance control in conditions of plantar-flexor muscles fatigue is currently being assessed. Acknowledgements This research was granted by the Ministry of Education, Youth and Sports of the Czech Republic (No. MSM 6198959221) ‘‘Physical Activity and Inactivity of the Inhabitants of the Czech Republic in the Context of Behavioral Changes’’, the Garches Foundation and AXA Research Fund (France). The authors would like to thank subject volunteers. Conflict of interest statement There are no conflicts of interest. References [1] Horak FB, Macpherson JM. Postural orientation and equilibrium. In: Rowell LB, Shepard JT, editors. Handbook of physiology. Exercise: regulation and integration of multiple systems. Oxford: Oxford University Press; 1996 . p. 255–92. [2] Nashner LM, Black FO, Wall III C. Adaptation to altered support and visual conditions during stance: patients with vestibular deficits. J Neurosci 1982;2: 536–44. [3] Peterka RJ. Sensorimotor integration in human postural control. J Neurophysiol 2002;88:1097–118. [4] Peterka RJ, Loughlin PJ. Dynamic regulation of sensorimotor integration in human postural control. J Neurophysiol 2004;91:410–23. ˆ B. Assessment of static postural control in teen[5] Vuillerme N, Marin L, Debu agers with Down syndrome. Adapt Phys Act Q 2001;18:417–33. [6] Vuillerme N, Burdet C, Isableu B, Demetz S. The magnitude of the effect of calf muscles fatigue on postural control during bipedal quiet standing with vision depends on the eye-visual target distance. Gait Posture 2006;24: 169–72. [7] Kavounoudias A, Roll R, Roll JP. Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation. J Physiol 2001;532:869–78. [8] Isableu B, Vuillerme N. Differential integration of kinaesthetic signals to postural control. Exp Brain Res 2006;174:763–8. [9] Patel M, Fransson PA, Lush D, Gomez S. The effect of foam surface properties on postural stability assessment while standing. Gait Posture 2008;28: 649–56. [10] Hijmans JM, Geertzen JH, Dijkstra PU, Postema K. A systematic review of the effects of shoes and other ankle or foot appliances on balance in older people and people with peripheral nervous system disorders. Gait Posture 2007;25: 316–23. Review.
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[11] Singh NB, Nussbaum MA, Madigan MA. Evaluation of circumferential pressure as an intervention to mitigate postural instability induced by localized muscle fatigue at the ankle. Int J Ind Ergon 2009;39:821–7. [12] You SH, Granata KP, Bunker LK. Effects of circumferential ankle pressure on ankle proprioception, stiffness, and postural stability: a preliminary investigation. J Orthop Sports Phys Ther 2004;34:449–60. [13] Bisson EJ, Chopra S, Azzi E, Morgan A, Bilodeau M. Acute effects of fatigue of the plantarflexor muscles on different postural tasks. Gait Posture 2010;32:482–6. [14] Ledin T, Fransson PA, Magnusson M. Effects of postural disturbances with fatigued triceps surae muscles or with 20% additional body weight. Gait Posture 2004;19:184–93. [15] Noda M, Demura S. Comparison of quantitative analysis and fractal analysis of center of pressure based on muscle fatigue. Percept Mot Skills 2006;102:529–42. [16] Pinsault N, Vuillerme N. Differential postural effects of plantar-flexor muscles fatigue under normal, altered and improved vestibular and neck somatosensory conditions. Exp Brain Res 2008;191:99–107. [17] Qu X, Nussbaum MA, Madigan ML. Model-based assessments of the effects of age and ankle fatigue on the control of upright posture in humans. Gait Posture 2009;30:518–22. [18] Vuillerme N, Forestier N, Nougier V. Attentional demands and postural sway: the effect of the calf muscles fatigue. Med Sci Sports Exerc 2002;34:1607–12. [19] Vuillerme N, Nougier V. Effect of light finger touch on postural sway after lower-limb muscular fatigue. Arch Phys Med Rehabil 2003;84:1560–3. [20] Vuillerme N, Boisgontier M, Chenu O, Demongeot J, Payan Y. Tongue-placed tactile biofeedback suppresses the deleterious effects of muscle fatigue on joint position sense at the ankle. Exp Brain Res 2007;183:235–40. [21] Vuillerme N, Boisgontier M. Muscle fatigue degrades force sense at the ankle joint. Gait Posture 2008;28:521–4. [22] Vuillerme N, Pinsault N. Re-weighting of somatosensory inputs from the foot and the ankle for controlling posture during quiet standing following trunk extensor muscles fatigue. Exp Brain Res 2007;183:323–7. [23] Simoneau GG, Degner RM, Kramper CA, Kittleson KH. Changes in ankle joint proprioception resulting from strips of athletic tape applied over the skin. J Athl Train 1997;32:141–7. [24] Borg G. Psychological scaling with applications in physical work and the perception of exertion. Scand J Work Environ Health 1990;16:55–8. [25] Enoka RM, Stuart DG. Neurobiology of muscle fatigue. J Appl Physiol 1992; 72:1631–48. [26] Tagaki A, Fujimura E, Suehiro S. A new method of statokinesigram area measurement. Application of a statistically calculated ellipse. In: Igarashi M, Black O, editors. Vestibular and visual control on posture and locomotor equilibrium. Baˆale: Karger; 1985. p. 74–9. [27] Geurts AC, Nienhuis B, Mulder TW. Intrasubject variability of selected forceplatform parameters in the quantification of postural control. Arch Phys Med Rehabil 1993;74:1144–50. [28] 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. [29] Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM. Measures of postural steadiness: differences between healthy young and elderly adults. IEEE Trans Biomed Eng 1996;43:956–66. [30] Menant JC, Steele JR, Menz HB, Munro BJ, Lord SR. Optimizing footwear for older people at risk of falls. J Rehabil Res Dev 2008;45:1167–81. Review. [31] Maki BE, Perry SD, Norrie RG, McIlroy WE. Effects of facilitation of sensation from plantar foot-surface boundaries on postural stabilization in young and older adults. J Gerontol A Biol Sci Med Sci 1999;54:M281–7. [32] Priplata A, Niemi J, Salen M, Harry J, Lipsitz LA, Collins JJ. Noise-enhanced human balance control. Phys Rev Lett 2002;89:238101. [33] Vuillerme N, Chenu O, Pinsault N, Boisgontier M, Demongeot J, Payan Y. Interindividual variability in sensory weighting of a plantar pressure-based, tongue-placed tactile biofeedback for controlling posture. Neurosci Lett 2007;421:173–7.
Contents lists available at SciVerse ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Do somatosensory conditions from the foot and ankle affect postural responses to plantar-flexor muscles fatigue during bipedal quiet stance? Petra Hlavackova a,b, Nicolas Vuillerme a,* a b
FRE 3405, AGIM (AGeing Imaging Modeling), CNRS-UJF-UPMF-EPHE, Grenoble, France Faculty of Physical Culture, Palacky University, Olomouc, Czech Republic
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 December 2009 Received in revised form 1 September 2011 Accepted 31 October 2011
The present study investigated the effects of somatosensory conditions at the foot and ankle on postural responses to plantar-flexor muscle fatigue during bipedal quiet stance. Twenty-two young healthy adults were asked to stand upright as still as possible with their eyes closed in three somatosensory conditions (normal, altered and improved) both prior to and after exercises inducing plantar-flexor muscle fatigue. In the normal condition, the postural task was executed on a firm support surface constituted by the force platform. In the altered condition, a 2-cm thick foam support surface was placed under the subjects’ feet. In the improved condition, increased cutaneous feedback at the foot and ankle was provided by strips of athletic tape applied across both their ankle joints. Muscle fatigue was induced in the plantar-flexor muscles of both legs through the execution of a repeated standing heel raise exercise. Centre of foot pressure displacements were recorded using a force platform. Results showed that plantar-flexor muscle fatigue yielded increased centre of foot pressure displacements under normal foot and ankle sensory conditions. Furthermore, this effect was exacerbated under altered foot and ankle sensory conditions and mitigated under improved foot and ankle sensory conditions. Altogether, the present findings suggested an increased reliance on somatosensory information from the foot and ankle for controlling upright posture in the presence of plantar-flexor muscle fatigue. ß 2011 Elsevier B.V. All rights reserved.
Keywords: Muscle fatigue Ankle Balance Foot Somatosensation Centre of foot pressure
1. Introduction It is now a generally held view that, depending on the sensory contexts and the neuromuscular constraints acting on an individual (e.g. [1–6]), the central nervous system can adaptively, dynamically and selectively adjust the relative contributions of sensory inputs (i.e. the sensory weights) to maintain upright stance. Among these sensory inputs, somatosensory information from the foot and ankle is recognised to play a crucial role (e.g. [7]). Various experimental manipulations of foot and ankle cutaneous mechanoreceptors have been employed to assess the contribution of feedback from cutaneous afferents. For instance, several studies have reported that (1) altering the quality of the postural support surface information by having individual standing on a compliant support surface results in a degradation of balance (e.g. [8,9]), while (2) increasing afferent feedback from cutaneous receptors in the skin of the foot and ankle through the application of foot and/or ankle appliances results in improvement of balance (e.g. [10–12]). Other studies have used plantar-flexor muscle fatiguing exercise to assess the contribution of ankle neuromuscular
* Corresponding author at: Faculty of Medicine, La Tronche Cedex, France. E-mail address: [email protected] (N. Vuillerme). 0966-6362/$ – see front matter ß 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2011.10.361
function to the control of bipedal posture. Generally, these studies reported a deterioration of bipedal postural control (e.g. [6,13–19]), which has been suggested to stem from an alteration of ankle proprioceptive acuity [20,21] and an inability to produce or sustain required force output with the fatigued plantar-flexor muscle. In the context of adaptive multisensory control of balance (e.g. [1–6]), the present study was designed to investigate the effects of somatosensory conditions from the foot and ankle on postural responses to plantar-flexor muscle fatigue during bipedal quiet stance. To achieve this goal, we employed an experimental procedure similar to that previously used in a study focussing on the effects of trunk extensor muscles fatigue on postural control during quiet standing under different somatosensory conditions from the foot and the ankle [22]. Somatosensation from the foot and the ankle was degraded by standing on a foam surface and facilitated through the increased cutaneous feedback at the foot and ankle provided by strips of athletic tape applied across both ankle joints. Postural responses were assessed by computing the displacements centre of foot pressure (CoP) using a force platform. It was hypothesised that the destabilizing effect of plantar-flexor muscle fatigue (e.g. [13–19]) would be exacerbated under altered foot and ankle sensory conditions and mitigated under improved foot and ankle sensory conditions.
P. Hlavackova, N. Vuillerme / Gait & Posture 36 (2012) 16–19 2. Methods
(2) the mean velocity of the CoP displacements which constitutes a good index of the amount of activity required to maintain stability [27].
2.1. Subjects
2.2. Experimental procedure A repeated measures design was used, wherein subjects completed trials of quiet stance by before and after fatigue in each of three conditions. Precisely, with their eyes closed, subjects stood barefoot on a force platform feet abducted at 308, heels separated by 3 cm, their arms hanging loosely by their sides and were asked to sway as little as possible in three foot and ankle sensory conditions (normal, altered and improved). In the normal condition, the postural task was executed on a firm support surface constituted by the force platform. In the altered condition, a 2-cm thick foam support surface (density of 25 kg/m3) was placed under the subjects’ feet [8]. In the improved condition, two pieces of 5-cm wide strips of athletic tape were applied in a proximal-distal direction directly to the skin in front of and behind the subject’s talocrural joints [22,23]. The first strip, starting approximately 10 cm proximal to the ankle joint line and ending 5 cm distal to the ankle joint line, was positioned directly on the skin over the anterior aspect of the ankle joint. The second strip was used posteriorly over the Achilles tendon and calcaneus. These strips of tape, used to selectively provide cutaneous sensory feedback around both ankles without the added mechanical constriction and mechanical pressure on subcutaneous structures associated with the application of ankle taping as used in athletic events, have previously been shown to improve ankle proprioceptive acuity in young healthy subjects [23]. These three foot and ankle sensory conditions were performed under two conditions of pre fatigue and post fatigue of the plantar-flexor muscle. The pre fatigue condition served as a control condition. For each foot and ankle sensory condition (normal, altered and improved), subjects performed three 32-s trials. The order of presentation of these three conditions was randomised over subjects to reduce potential order effects. In the post fatigue condition, the measurements were performed after a fatiguing procedure whose aim was to induce muscular fatigue at the plantar-flexor muscles of both legs until task failure (e.g. [6,14,16]). As previously done in other studies (e.g. [6,14,16]), standing subjects were asked to execute a repeated standing heel raise exercise, i.e. to perform toe-lifts as many times as possible following the beat of a metronome (40 beats/min). The examiner gave verbal encouragement and checked the exercise performance to ensure that the subjects worked maximally. The fatigue level was reached when subjects were no longer able to complete the exercise. Immediately after the cessation of exercise, the subjective exertion level was assessed through the Borg CR-10 scale [24]. Subjects rated their perceived fatigue in the plantar-flexor muscles as almost ‘‘extremely strong’’. Subjects rated their perceived exertion at the plantar-flexor muscles as almost ‘‘extremely strong’’ (mean Borg ratings of 8.1). The recovery process after fatigue procedures is often considered as a limitation for all fatigue experiments. In the present experiment, to ensure that balance measurement in the fatigue condition was obtained in a genuine fatigued state, various rules were respected: (1) the fatiguing exercise took place beside the force platform to minimise the time between the exercise-induced fatiguing exercise and the balance measurements (less than 1 min), (2) the fatiguing exercise was repeated prior to each balance measurement, and (3) the examiner checked that the subjects showed visible signs of fatigue and failed to perform the exercises due to fatigue. In doubtful cases, the examiner encouraged the subject to continue with a few more exercises. Note that before the completion of the present experiment, we conducted a pilot study to examine whether the proposed fatiguing protocol induced electrical signs of fatigue in plantar-flexor muscles. To this aim, electromyographic (EMG) activity of gastrocnemius and soleus muscles was recorded before and following to the exercise performance. Results showed that the exercise produced an EMG median frequency shift towards the lower frequencies ( 18%), suggesting the occurrence of physiological changes characteristic of muscle fatigue (e.g. [25]). These results ensuring that plantar-flexor muscle were fatigued at the end of the exercise hence allowed us to use this fatiguing procedure to investigate the effects of plantar-flexor muscle fatigue on postural control during bipedal quiet standing as previously done (e.g. [6,14,16]). Three additional trials for each condition of sensory inputs at the foot and ankle (normal, altered and improved) were executed, for a total of 18 trials. 2.3. Data collection and dependent measures A triangular force platform (Equi+, model PF01; Aix les Bains, France) was used to measure the displacements of the centre of foot pressure (CoP) (sampling rate: 64 Hz). Two dependant variables were used to describe subject’s postural behavior: (1) the surface area (mm2) covered by the trajectory of the CoP with a 90% confidence interval [26] which provides a measure of the size of the CoP over the support surface;
2.4. Statistical analysis The means of the three trials performed in each of experimental condition were used for statistical analyses in order to improve reliability. Results of a recent study established the ‘‘excellent’’ test–retest reliability of the CoP surface area and the CoP mean velocity parameters with three 30 s trial recordings [intra-class correlation coefficient (ICC) > 0.75] [28]. These dependant variables were tested for normality using the Shapiro–Wilk test and for equality of variance using the Levene test (Ps > 0.05). Two separate fatigues (pre fatigue vs. post fatigue) 3 foot and ankle sensory conditions (normal vs. altered vs. improved) analyses of variance (ANOVAs) with repeated measures on both factors was applied to the data surface area (mm2) covered by the trajectory of the CoP and the mean velocity of the CoP displacements. Post-hoc analyses (Newman–Keuls test) were performed whenever necessary. Level of significance was set at 0.05.
3. Results Analysis of the surface area covered by the trajectory of the CoP showed main effects of fatigue (F(1,21) = 7.86, P = 0.0106) and foot and ankle sensory condition (F(2,42) = 46.39, P = 0.0000) and a significant interaction of fatigue foot and ankle sensory conditions (F(2,42) = 4.70, P = 0.0144). As illustrated in Fig. 1, post-hoc analyses revealed that: (1) the post fatigue condition yielded a larger CoP surface area compared to the pre fatigue condition in the normal foot and ankle sensory condition (P = 0.0037; Fig. 1, left part), (2) this effect was exacerbated in the altered foot and ankle sensory condition (P = 0.0001; Fig. 1, middle part), whereas (3) no difference was found between the pre fatigue and post fatigue conditions in the improved foot and ankle sensory condition (P = 0.3170; Fig. 1, right part). Similar results were observed for the mean velocity of the CoP displacements. Indeed, analysis of the mean velocity of the CoP displacements showed main effects of fatigue (F(1,21) = 19.53, P = 0.0002) and foot and ankle sensory condition (F(2,42) = 66.50,
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Twenty-two young healthy adults (18 males and 4 females, age: 22.1 1.9 years; body weight: 72.1 4.5 kg; height: 174.3 3.4 cm; mean S.D.) voluntarily participated in the experiment. They gave their informed consent to the experimental procedure as required by the Helsinki declaration (1964) and the local Ethics Committee. None of the subjects presented any history of injury, surgery or pathology to either lower extremity that could affect their ability to perform the experiment.
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400
300
**
200
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0 Normal
Altered
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Foot and ankle somatosensory conditions Fig. 1. Mean and standard deviation of the surface area covered by the trajectory of the CoP obtained for the three normal, altered and improved foot and ankle sensory conditions and the two conditions of pre fatigue and post fatigue of plantar-flexor muscle (**P < 0.01; ***P < 0.001).
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0 Normal
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Foot and ankle somatosensory conditions Fig. 2. Mean and standard deviation of mean velocity of the CoP displacements obtained for the three normal, altered and improved foot and ankle sensory conditions and the two conditions of pre fatigue and post fatigue of plantar-flexor muscle (**P < 0.01; ***P < 0.001).
P < 0.0000) and a significant interaction of fatigue foot and ankle sensory conditions (F(2,42) = 4.87, P = 0.0125). As illustrated in Fig. 2, post-hoc analyses revealed that: (1) the post fatigue condition yielded a higher mean velocity of the CoP displacements area compared to the pre fatigue condition in the normal foot and ankle sensory condition (P = 0.0037; Fig. 2, left part), (2) this effect was exacerbated in the altered foot and ankle sensory condition (P = 0.0001; Fig. 2, middle part), whereas (3) no difference was found between the pre fatigue and post fatigue conditions in the improved foot and ankle sensory condition (P = 0.2020; Fig. 2, right part). 4. Discussion In the normal foot and ankle sensory condition, a wider CoP surface area (Fig. 1, left part) and a larger CoP mean velocity (Fig. 2, left part) were observed in the post fatigue compared to the pre fatigue condition. These results are in accordance with previous studies reporting impaired bipedal postural control following fatiguing exercise of the plantar-flexor muscle, with a similar order of magnitude (e.g. [6,14–19]). Beyond these well-established observations, results further showed that standing on a foam support surface can modify the magnitude of the postural responses to plantar-flexors muscle fatigue, in two different ways. One the one hand, larger negative effects of fatigue on the CoP surface area (Fig. 1, middle part) and CoP mean velocity (Fig. 2, middle part) were observed in the altered condition than in the normal condition. Considering the functional significance of these two CoP-based parameters [27,29], these results suggest that plantar-flexor muscle fatigue impaired the effectiveness of the postural control system and increased the amount of postural regulatory activity required to control unperturbed bipedal posture when the quality of the postural support surface information was altered by standing on a foam support surface (altered condition) to a greater extent than when it was not (normal condition). On the other hand, the negative effects
of fatigue on the CoP surface area and CoP mean velocity observed in the two above-mentioned support surface conditions were suppressed in the improved condition (Fig. 1, right part and Fig. 2, right part, respectively). These results suggest that when the quality of the cutaneous information from the ankles was improved through the increased cutaneous feedback at the foot and ankle provided by strips of athletic tape applied across both ankle joints, plantar-flexor muscle fatigue did not impair the control unperturbed bipedal posture any more. At this point, it is important to mention the recent study by Singh et al. [11] which also reported that application of circumferential pressure near the ankle was effective in mitigating the adverse effects of plantarflexor muscle fatigue on the control of bipedal posture [11]. Interestingly, results further showed that this effectiveness was limited to certain individuals. In the latter study, however, muscle fatigue in the plantar-flexors and circumferential pressure were both applied unilaterally to the dominant side, so that the authors suggested that bilateral ankle LMF and pressure application could results in more substantial changes [11]. Along these lines, since group means could have concealed the existence of different of postural responses among the subjects, we decided to further examine the data of each subject in order to assess whether some of them were more sensitive than others to the improvement of foot and ankle somatosensation. In accordance with Singh et al.’s assumption, this individual analysis revealed that most subjects benefited from the increased cutaneous feedback at the foot and ankle provided by strips of athletic tape applied across both their ankle joints to limit the destabilizing effect of plantarflexor muscle fatigue (17 of 22 subjects decreased their CoP surface by 9%–65%, and 16 of them decreased their CoP mean velocity by 3%–26%). The observed differential postural effects of plantar-flexor muscle fatigue observed under normal, altered and improved foot and ankle somatosensory conditions support the hypothesis of the sensory reweighting hypothesis of the human postural control (e.g. [1–6]). This hypothesis supposes that the central nervous system selectively is able to adjust the relative contributions of sensory inputs (i.e. the sensory weights) to maintain upright stance depending on the sensory contexts and the neuromuscular constraints acting on the individual. Indeed, in conditions of altered ankle neuromuscular function induced by plantar-flexor muscle fatigue [20,21], recent studies have evidenced the ability of the central nervous system to efficiently use visual information [6–14], vestibular and neck somatosensory inputs [16] and haptic cues from the finger [19] providing more accurate and reliable information for ensuring adequate postural control. Along this line, it is possible that the central nervous system also increases the reliance on somatosensory inputs from the foot and ankle to maintain adequate upright stance. Interestingly, the proposed increased dependency on sensory information from the plantar sole and the ankle for controlling bipedal posture observed in the Post fatigue condition of the present study is not limited to muscle fatigue localized at the ankle joint. Indeed, a previous study has reported that the deleterious effect of trunk extensor muscles fatigue on the control of bipedal posture similarly was (1) exacerbated when young healthy subjects stood on a foam surface, and (2) mitigated in condition of increased cutaneous feedback at the foot and ankle provided by strips of athletic tape applied across both their ankle joints [22]. On the whole, these results give further support to the sensory weighting mechanisms involved in postural control according to which changes in the sensory environment and the neuromuscular state acting on the individual could bring about changes in the relative weights between information channels (e.g. [1–6]). Finally, the present findings stress the importance of sensory information from the foot and ankle to ensure an appropriate
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control of balance in the presence of plantar-flexor muscle fatigue. Since footwear represents a highly potential modifiable factor which is recognised to play a crucial role in improving balance control and reducing falls (e.g. see [10,30], for recent reviews), these results could significantly impact orthopaedic research and development. Along these lines, whether tubing (e.g. [31]) or vibrating (e.g. [32]) shoe insoles and incorporating a pressure plantar-based biofeedback system in footwear (e.g. [33]) could improve balance control in conditions of plantar-flexor muscles fatigue is currently being assessed. Acknowledgements This research was granted by the Ministry of Education, Youth and Sports of the Czech Republic (No. MSM 6198959221) ‘‘Physical Activity and Inactivity of the Inhabitants of the Czech Republic in the Context of Behavioral Changes’’, the Garches Foundation and AXA Research Fund (France). The authors would like to thank subject volunteers. Conflict of interest statement There are no conflicts of interest. References [1] Horak FB, Macpherson JM. Postural orientation and equilibrium. In: Rowell LB, Shepard JT, editors. Handbook of physiology. Exercise: regulation and integration of multiple systems. Oxford: Oxford University Press; 1996 . p. 255–92. [2] Nashner LM, Black FO, Wall III C. Adaptation to altered support and visual conditions during stance: patients with vestibular deficits. J Neurosci 1982;2: 536–44. [3] Peterka RJ. Sensorimotor integration in human postural control. J Neurophysiol 2002;88:1097–118. [4] Peterka RJ, Loughlin PJ. Dynamic regulation of sensorimotor integration in human postural control. J Neurophysiol 2004;91:410–23. ˆ B. Assessment of static postural control in teen[5] Vuillerme N, Marin L, Debu agers with Down syndrome. Adapt Phys Act Q 2001;18:417–33. [6] Vuillerme N, Burdet C, Isableu B, Demetz S. The magnitude of the effect of calf muscles fatigue on postural control during bipedal quiet standing with vision depends on the eye-visual target distance. Gait Posture 2006;24: 169–72. [7] Kavounoudias A, Roll R, Roll JP. Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation. J Physiol 2001;532:869–78. [8] Isableu B, Vuillerme N. Differential integration of kinaesthetic signals to postural control. Exp Brain Res 2006;174:763–8. [9] Patel M, Fransson PA, Lush D, Gomez S. The effect of foam surface properties on postural stability assessment while standing. Gait Posture 2008;28: 649–56. [10] Hijmans JM, Geertzen JH, Dijkstra PU, Postema K. A systematic review of the effects of shoes and other ankle or foot appliances on balance in older people and people with peripheral nervous system disorders. Gait Posture 2007;25: 316–23. Review.
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[11] Singh NB, Nussbaum MA, Madigan MA. Evaluation of circumferential pressure as an intervention to mitigate postural instability induced by localized muscle fatigue at the ankle. Int J Ind Ergon 2009;39:821–7. [12] You SH, Granata KP, Bunker LK. Effects of circumferential ankle pressure on ankle proprioception, stiffness, and postural stability: a preliminary investigation. J Orthop Sports Phys Ther 2004;34:449–60. [13] Bisson EJ, Chopra S, Azzi E, Morgan A, Bilodeau M. Acute effects of fatigue of the plantarflexor muscles on different postural tasks. Gait Posture 2010;32:482–6. [14] Ledin T, Fransson PA, Magnusson M. Effects of postural disturbances with fatigued triceps surae muscles or with 20% additional body weight. Gait Posture 2004;19:184–93. [15] Noda M, Demura S. Comparison of quantitative analysis and fractal analysis of center of pressure based on muscle fatigue. Percept Mot Skills 2006;102:529–42. [16] Pinsault N, Vuillerme N. Differential postural effects of plantar-flexor muscles fatigue under normal, altered and improved vestibular and neck somatosensory conditions. Exp Brain Res 2008;191:99–107. [17] Qu X, Nussbaum MA, Madigan ML. Model-based assessments of the effects of age and ankle fatigue on the control of upright posture in humans. Gait Posture 2009;30:518–22. [18] Vuillerme N, Forestier N, Nougier V. Attentional demands and postural sway: the effect of the calf muscles fatigue. Med Sci Sports Exerc 2002;34:1607–12. [19] Vuillerme N, Nougier V. Effect of light finger touch on postural sway after lower-limb muscular fatigue. Arch Phys Med Rehabil 2003;84:1560–3. [20] Vuillerme N, Boisgontier M, Chenu O, Demongeot J, Payan Y. Tongue-placed tactile biofeedback suppresses the deleterious effects of muscle fatigue on joint position sense at the ankle. Exp Brain Res 2007;183:235–40. [21] Vuillerme N, Boisgontier M. Muscle fatigue degrades force sense at the ankle joint. Gait Posture 2008;28:521–4. [22] Vuillerme N, Pinsault N. Re-weighting of somatosensory inputs from the foot and the ankle for controlling posture during quiet standing following trunk extensor muscles fatigue. Exp Brain Res 2007;183:323–7. [23] Simoneau GG, Degner RM, Kramper CA, Kittleson KH. Changes in ankle joint proprioception resulting from strips of athletic tape applied over the skin. J Athl Train 1997;32:141–7. [24] Borg G. Psychological scaling with applications in physical work and the perception of exertion. Scand J Work Environ Health 1990;16:55–8. [25] Enoka RM, Stuart DG. Neurobiology of muscle fatigue. J Appl Physiol 1992; 72:1631–48. [26] Tagaki A, Fujimura E, Suehiro S. A new method of statokinesigram area measurement. Application of a statistically calculated ellipse. In: Igarashi M, Black O, editors. Vestibular and visual control on posture and locomotor equilibrium. Baˆale: Karger; 1985. p. 74–9. [27] Geurts AC, Nienhuis B, Mulder TW. Intrasubject variability of selected forceplatform parameters in the quantification of postural control. Arch Phys Med Rehabil 1993;74:1144–50. [28] 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. [29] Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM. Measures of postural steadiness: differences between healthy young and elderly adults. IEEE Trans Biomed Eng 1996;43:956–66. [30] Menant JC, Steele JR, Menz HB, Munro BJ, Lord SR. Optimizing footwear for older people at risk of falls. J Rehabil Res Dev 2008;45:1167–81. Review. [31] Maki BE, Perry SD, Norrie RG, McIlroy WE. Effects of facilitation of sensation from plantar foot-surface boundaries on postural stabilization in young and older adults. J Gerontol A Biol Sci Med Sci 1999;54:M281–7. [32] Priplata A, Niemi J, Salen M, Harry J, Lipsitz LA, Collins JJ. Noise-enhanced human balance control. Phys Rev Lett 2002;89:238101. [33] Vuillerme N, Chenu O, Pinsault N, Boisgontier M, Demongeot J, Payan Y. Interindividual variability in sensory weighting of a plantar pressure-based, tongue-placed tactile biofeedback for controlling posture. Neurosci Lett 2007;421:173–7.