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Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion
Journal of Electromyography and Kinesiology xxx (2013) xxx–xxx
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Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion Katsuo Fujiwara a,⇑, Chie Yaguchi b a b
Department of Human Movement and Health, Graduate School of Medical Science, Kanazawa University, 13-1 Takara-machi, Kanazawa 920-8640, Japan Department of Physical Therapy, Faculty of Human Science, Hokkaido Bunkyo University, 5-196-1, Kogane-chuo, Eniwa 061-1449, Japan
a r t i c l e
i n f o
Article history: Received 28 August 2012 Received in revised form 19 July 2013 Accepted 28 July 2013 Available online xxxx Keywords: Anticipatory postural control Arm movement Center of foot pressure Electromyogram Strategy
a b s t r a c t In bilateral shoulder flexion with the arms moving from the sides of the body to the horizontal level while standing, no preceding activation of the triceps surae (TS) with respect to focal muscles has been found. Considering that preceding activation would offer a useful indicator of anticipatory postural control, it was attempted to induce preceding activation by limiting the anterior displacement range of the center of foot pressure in the anteroposterior direction (CoPap). Subjects were 13 healthy young adults. The 50% anterior range of CoPap displacement caused by shoulder flexion was calculated, and the floor inclined by the subject’s weight when CoPap extended beyond that range. Subjects were instructed not to incline the floor during shoulder flexion. Under the limitation condition, the ankle and knee joints plantarflexed and extended at 1.1°, respectively, with no hip movement; that is, the whole body inclined backward by pivoting at the ankle. This limitation resulted in preceding muscle activation of TS as well as erector spinae and biceps femoris, and no significant differences in onset time were seen between these muscles. These results demonstrated that by limiting CoPap anterior displacement, preceding activation of TS could be induced with backward inclination of the whole body. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction With rapid movements of the arms while standing, the postural muscles of the legs and trunk are automatically activated before the focal muscles of the arms, to moderate any disturbances of posture and equilibrium caused by the arm movement (Belen’kiı˘ et al., 1967). Cordo and Nashner (1982) reported that the timing of postural muscle activation changes according to internal and external conditions. In addition, they proposed that the preceding muscle activation is clearly observed in those postural muscles playing the most important roles in balance maintenance. Marked preceding activation is found in the biceps femoris (BF), and the onset time was found to be earlier under conditions of rapid (Lee et al., 1987) and self-paced shoulder flexion (Fujiwara et al., 2011b), anterior initial position of the center of gravity (COG) (Fujiwara et al., 2003) and postural movement patterns in which the legs and trunk or trunk alone were inclined backward (Fujiwara et al., 2007). However, when shoulder flexion has been performed in previous studies with the arm moving from the side of the body to the horizontal level, preceding activation of the triceps surae (TS) has not been observed (Bouisset and Zattara, 1981). This ⇑ Corresponding author. Tel.: +81 76 265 2225; fax: +81 76 234 4219.
presumably results from a lack of task condition in which the preceding activation of TS is necessary for postural control. The present study was designed to provide useful background information in order to subsequently select tasks in which preceding activation of TS is recognized. For postural control during transient floor translation, a postural movement pattern focused on the hip joint (hip strategy) is adopted with a narrow base of support in the anteroposterior direction, while with a wide support base, the movement pattern focused on the ankle joint (ankle strategy) (Horak and Nashner, 1986). The muscles around the hip joint and the lower leg muscles are mainly activated in these hip and ankle strategies, respectively. These findings indicate that in transient floor translation with a wide support base, torque around the ankle starts to change earliest, so the focus of postural control is put on the lower leg muscles, while with a narrow support base, the focus is switched to the muscles around the hip joint. However, no studies have examined activation patterns of postural muscles during bilateral shoulder flexion on a stable platform when subjects try to keep the center of foot pressure in the anteroposterior direction (CoPap) within a restrictive range of the support base. We considered that with bilateral shoulder flexion from the body side position, preceding activation of TS might be induced by narrowing only the anterior range of the support base, while keeping a wide posterior range. In this case, to limit anterior displacement of CoPap, a strategy in which the center of body mass
E-mail address: [email protected] (K. Fujiwara). 1050-6411/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jelekin.2013.07.015
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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K. Fujiwara, C. Yaguchi / Journal of Electromyography and Kinesiology xxx (2013) xxx–xxx
moves backward with the postural control focused on the ankle is adopted, and any preceding activation of TS would be clearly apparent. In the present study, the floor was inclined when CoPap extended beyond a determined anterior range. Based on the feedback information of floor inclination, the subjects were required to control their posture to avoid inclining the floor. A standing posture with the upper limbs at the side of the body is fundamental and arm movements from this position are frequently performed during daily life. In the elderly, decreased muscle strength of the lower legs leads to deterioration in balance function (Horak et al., 1989). Fujiwara et al. (2011a) reported that during shoulder flexion from hands at the side of the body, the soleus (Sol) activated slightly earlier following muscle training of TS, but clear preceding activation was not observed. If preceding activation of TS is able to be induced for young adults during shoulder flexion from this hand position, this task condition could be effectively applied for the elderly (Woollacott and Manchester, 1993). We therefore investigated the onset timing of TS and postural movement patterns by narrowing the anterior range of the support base, first in young adults. Our working hypothesis was that during bilateral shoulder flexion with limitation of CoPap anterior displacement, the preceding activation of TS would be induced, with backward inclination of the whole body pivoting at the ankles. 2. Methods 2.1. Subjects Subjects comprised 7 men and 6 women. Mean values (standard deviation (SD)) for age, height, weight, foot length and lower leg length were 24.8 (5.0) years, 165.5 (8.1) cm, 59.3 (8.1) kg, 24.5 (1.5) cm and 40.5 (2.3) cm, respectively. No subjects reported any history of neurological or orthopedic impairment. In accordance with the Declaration of Helsinki, all subjects provided informed consent after receiving an explanation of the experimental protocol, which was approved by our institutional ethics committee. 2.2. Apparatus To measure CoPap, a force platform (FPA34; Electro-design, Noda, Japan) was used. CoPap position was shown as a percentage of the distance from the heel in relation to foot length (%FL). CoPap electronic signals were sent simultaneously to three devices: a computer (PC9801BX; NEC, Tokyo, Japan) to determine CoPap position; another computer (Dimension E521; Dell Japan, Kawasaki, Japan) for analysis; and an oscilloscope (DS6612; Iwatsu, Tokyo, Japan) to monitor the results. The onset time of postural muscles is influenced by CoPap position just before shoulder flexion (Fujiwara et al., 2003). To control initial CoPap positions, the first computer, which received CoPap data via an analog-to-digital (A/D) converter (PIO9045; I/O-Data, Kanazawa, Japan) with a 20-Hz sampling rate and 12-bit resolution, generated a buzzing sound when CoPap was located within a range of ±1 cm of the quiet standing posture (QSP range). Since the SD for CoPap fluctuation during QSP for 60 s was approximately 0.5 cm for young healthy subjects (Goshima, 1986), the QSP range corresponds to ±2 SDs of the fluctuation. The 50% range of most anterior displacement of the CoPap caused by shoulder flexion was calculated. To limit the anterior displacement range of CoPap, we used a handmade inclination board on the force platform that underwent forward-inclination by 10° due to the subject’s weight when CoPap extended beyond that range (Fig. 1). Arm acceleration was recorded using a miniature unidirectional accelerometer (AS-5GB; Kyowa, Tokyo, Japan) placed on the dorsal
surface of the right wrist. To detect the beginning of arm movement, the axis of sensitivity before shoulder flexion was along the anteroposterior direction. To measure arm, trunk and leg motions in the sagittal plane during shoulder flexion, a position sensor system (C5949; Hamamatsu Photonics, Hamamatsu, Japan) was used. The sensor head was placed 4.0 m away from the right side of the subject. Lightemitting diode (LED) targets were placed over the following landmarks on the right side: the wrist; spinous process of C7; midpoint of the greater trochanter (GT); lateral epicondyle (LE); lateral malleolus (LM); and the fifth metatarsal head (MH) (Fig. 1). The x- and y-coordinates of LED targets were recorded at 0.3-mm resolution. A fixation point was presented at the center of an eye-trek facemounted display (FMD011F; Olympus, Tokyo, Japan). Warning (S1) and response (S2) signals were auditory stimuli delivered via earphones with frequency, intensity, duration and inter-stimulus interval of 2000 Hz, 35 dB above the auditory threshold, 100 ms and 2 s, respectively. Surface electrodes (30-mm diameter, 13-mm diameter capture area, P-00-S; Ambu, Ballerup, Denmark) were used in bipolar derivation to record electromyographic (EMG) activity of the following muscles: the anterior deltoid (AD) as a focal muscle for shoulder flexion; rectus abdominis (RA) at the level of the navel, erector spinae (ES) at the level of the iliac crest, rectus femoris (RF) at the midpoint between the anterior inferior iliac spine and upper border of the patella, long head of BF at the midpoint between the ischial tuberosity and head of the fibula, tibialis anterior (TA), medial head of gastrocnemius (GcM) and Sol as postural muscles (Fig. 1). Electrode locations for AD, TA, GcM and Sol were the midportion of the muscle belly. Electrodes were placed on the right side of the body with an inter-electrode (center-to-center) distance of about 3 cm. A ground electrode was placed over the right LM. These electrodes were fixed after shaving and cleaning the skin with alcohol. Inter-electrode impedance, as measured by an impedance tester, was reduced to below 5 kX. EMG signals from electrodes were amplified (4000) and band-pass filtered (5–500 Hz) using an analog amplifier (Biotop-6R12; NEC-Sanei, Tokyo, Japan; common mode rejection ratio, 86 dB; input impedance, >10 MX). All electrical signals, including CoPap, arm acceleration, x- and y-coordinates of each LED, S1 and S2 signals and each EMG, were sent to the computer for analysis via A/D converters (ADJ-98; Canopus, Kobe, Japan) with a 1000-Hz sampling rate and 16-bit resolution. 2.3. Procedure All measurements were performed on the force platform while standing barefoot with feet 10 cm apart and parallel, elbows extended, and hands positioned on the thigh anterior to GT (Fig. 1). Subjects were instructed to gaze at the fixation point during all measurements. First, after the experimenter told the subject to maintain a stabilized QSP and confirmed the stabilization, CoPap fluctuation for 10 s was measured and the mean position was calculated. The mean value of five measurements was adopted as the QSP position. Next, bilateral shoulder flexion trials were commenced. Subjects maintained CoPap position within the QSP range for at least 3 s while hearing the buzzing sound. S1 was randomly presented within 1–3 s after the experimenter stopped the buzzing sound, and then S2 was started 2 s after S1. In response to S2, subjects flexed the arms at maximum speed, stopped voluntarily at the shoulder level, and maintained this position for 3 s. Shoulder flexion trials were repeated 20 times on the flat floor (no-limitation condition, nLC), and the 50% range of most anterior displacement of the CoPap was calculated. Inclination axis of the floor was set
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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Face-mounted display
EMG C7
LED
Accelerometer
Anterior deltoid Erector spinae
QSP position
Wrist Rectus abdominis
Greater trochanter
CoPap Foot position
Biceps femoris
Inclination board Force platform
50 % range of CoP anterior displacement
Rectus femoris Lateral epicondyle
Gastrocnemius Soleus Ground
4.0 m
Tibialis anterior Lateral malleous Force platform
Fifth metatarsal head Position sensor camara
Fig. 1. Experimental set-up for measurement of EMG and postural movement during shoulder flexion and for limitation of CoPap anterior displacement.
at that range (mean position for 20 trials) (Fig. 1). Subjects were then instructed not to incline the floor during the shoulder flexion (limitation condition, LC). Shoulder flexion trials under LC were repeated 20 times. To familiarize subjects with the task, 10 practice trials for each condition were performed before the experimental trials. Under each condition, experimental trials in which CoPap position just before the shoulder flexion was beyond the QSP range were rejected. Furthermore, under LC, trials in which the subject failed to prevent inclination of the floor were also rejected. The experiment was conducted with a 30-s standing rest between each trial and a 3-min seated rest between conditions.
2.4. Data analysis Under LC, the percentage of inclined trials among all trials was calculated. All data were analyzed blinded to condition using signal-processing software (BIMUTAS II; Kissei Comtec, Matsumoto, Japan). We defined the first deviation in the accelerometer signal as the start point of arm movement (Fig. 2). The end of arm movement was defined as the end of the second burst of AD activity included in the envelop line that first deviated below the mean +2 SDs just before 500 ms of arm lowering, with reference to the curves of wrist position and arm acceleration. The interval between start point and endpoint of arm movement was defined as the arm movement duration. Mean CoPap positions were calculated for the periods from 300 to 150 ms with respect to the burst onset of AD (before arm movement period) and from 0 to +150 ms with respect to the endpoint of arm movement (after arm movement period) (Fig. 2). Differences between these mean positions were defined as CoPap displacements. Ankle (LE – LM – MH), knee (GT – LE – LM), and hip (C7 – GT – LE) angles in the sagittal plane were calculated using Excel 2010 software (Microsoft, Tokyo, Japan) based on x- and y-coordinates of LED targets (Fig. 2). For each angle, mean values were then calculated for the periods before and after arm movement. Differences in mean angles between the two time periods were calculated and defined as movement angles of the ankle, knee, and hip, respec-
tively (Fig. 2). Movement angles were considered positive for dorsiflexion of the ankle and flexion of the knee and hip. EMGs were analyzed as described below with reference to a previous study (Fujiwara et al., 2011b) (Fig. 2). To exclude electrocardiographic and movement artifacts, all EMGs were high-pass filtered at 40 Hz using a seventh-order Butterworth method and then full-wave rectified (rEMG). Mean and SD of the amplitude for background activity of each muscle was calculated during the period from 150 to 0 ms with respect to S2 onset for AD and from 300 to 150 ms with respect to burst onset of AD for postural muscles. Burst activation of each muscle was identified when onset was within +100 to +300 ms after S2 onset for AD and 150 to +100 ms with respect to burst onset of AD for postural muscles, and when the envelope line of the burst activity deviated more than the mean +2 SDs from background activity for at least 50 ms. Burst onset was defined as the time point at which the above deviation began in the EMG wave included in the envelope line. AD reaction time was defined as the time difference between S2 onsets and the AD burst. The onset time of postural muscles was defined as the time difference between burst onsets of postural muscles and AD, and presented as a negative value when burst onset of postural muscles preceded AD. Preceding EMG bursts of postural muscles were observed only in the dorsal muscles. Subsequently, activities of the frontal muscles (RA, RF and TA) sometimes or scarcely occurred between bimodal bursts in the dorsal muscles. As a result, only EMG bursts in the dorsal postural muscles were analyzed. To investigate EMG activity before S2, rEMG of each postural muscle from 500 ms before S1 to S2 was averaged for each condition. Then the averaged waveform was low-pass filtered at 40 Hz to detect the envelop line of the activity. In each averaged waveform, mean amplitude was calculated for 100 ms just before S2. To analyze the activity level for burst activation after arm movement, EMG of each muscle in the period from 300 to +200 ms with respect to burst onset of the muscle was averaged separately for each condition. The averaged EMG waveforms were then smoothed using a 40-Hz low-pass filter (Fujiwara et al., 2011b) to detect the envelop line of the averaged burst activity. EMG peak amplitude from baseline and latency with respect to burst onset were measured.
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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K. Fujiwara, C. Yaguchi / Journal of Electromyography and Kinesiology xxx (2013) xxx–xxx
1.0 mV
Anterior deltoid Rectus abdominis Erector spinae Rectus femoris Biceps femoris Tibialis anterior Gastrocnemius Soleus
5 cm
CoPap
5°
Hip joint
5°
Knee joint
5°
Ankle joint Acceleration of arm movement
onset -300 ms
onset -150ms
End+150ms
5G 80 cm
Wrist position
5V
S2
S2 onset
Burst onset of anterior deltoid
Endpoint of 100 ms arm movement
Fig. 2. Representative waveforms of each measurement data under the limitation condition. Arrows with thin straight and dashed lines indicate onset of burst activation of postural muscles and start point of arm movement, respectively. Arrows with thick straight and dashed lines indicate CoPap displacement and each movement angle.
2.5. Statistical analysis 60
no-limitation limitation
***
55
CoPap position (%FL)
Shapiro-Wilk tests confirmed that all data satisfied the assumption of a normal distribution. A one-sample t-test was used to assess whether burst onset of the postural muscles and angles of the ankle, knee and hip after arm movement differed significantly from that of AD and those before arm movement, respectively. A paired t-test was used to assess differences between conditions in CoPap displacement, arm movement duration, each movement angle, AD reaction time, postural muscle activities before S2 and peak amplitudes and latencies of each muscle. Two-way analysis of variance was used to assess the effect of condition (nLC and LC) and muscle on onset time of postural muscles. When a significant interaction between these factors was shown, post-hoc multiple-comparison analyses using Tukey’s honestly significant difference test were performed to assess differences among muscles. Pearson correlations were used to evaluate the magnitude of correlation between each parameter. The alpha level was set at p < 0.05. All statistical analyses were performed using SPSS software (version 14.0J, SPSS Japan, Tokyo, Japan).
50
45
Limited position
40
35
30 start point
endpoint
Fig. 3. Means and standard deviations of CoPap position at the start point and endpoint of the arm movement. p < 0.001.
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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3. Results
60
4
Movement angle (degrees)
3 2
no-limitation limitation
p = 0.06
***
*
1 0
†
-1
†
†
-2
†
-3 -44 Ankle
Knee
Hip
(Joint)
Fig. 4. Means and standard deviations of movement angles of the ankle, knee and hip p < 0.05; p < 0.001. Significant differences between before and after the arm movement (p < 0.05).
40
Onset time (ms)
Fig. 3 shows CoPap positions at the start point and endpoint of arm movement. Position at the endpoint of arm movement in LC was slightly posterior (2.9%FL (2.2)) to the determined position (4.7%FL (2.0) anterior to QSP position). CoPap displacement was significantly smaller in LC than in nLC (a decrease of 4.9%FL (2.7), i.e., 12.0 mm (6.7)) (t12 = 6.6, p < 0.001). No significant differences were found in the percentage of inclined trials between first and last halves of trials and the percentage of inclined trials among all trials was 13.4% (8.4). Fig. 4 shows movement angles of the ankle, knee, and hip. Angles of the ankle in LC, knee in both conditions and hip in nLC after arm movement were significantly larger in the plantarflexion and extension directions, respectively, than before arm movement (t12 > 2.3, p < 0.05). No significant differences were found between before and after arm movement in angles of ankle in nLC and hip in LC. Significant differences were found between conditions in movement angles of the ankle and knee (t12 > 2.9, p < 0.05). Hip movement angle in LC tended to differ from that in nLC (t12 = 2.1, p = 0.06). No significant differences were found between conditions in AD reaction time or arm movement duration (mean in both conditions: 185 ms and 498 ms, respectively). Preceding activations of postural muscles with respect to AD were found in ES and BF in nLC and in all postural muscles in LC (t12 > 5.6, p < 0.001) (Fig. 5). A significant interaction was found between condition and muscle for onset time of postural muscles (F3,48 = 36.0, p < 0.001). Onset times for ES, GcM and Sol were significantly earlier in LC than in nLC (p < 0.01). In nLC, ES and BF were activated significantly earlier than GcM and Sol (p < 0.001), while in LC, no significant differences in onset time were found for all postural muscles. For ES only, EMG mean amplitude just before S2 was significantly larger in LC (6.4 lV (SD = 5.4)) than in nLC (3.4 lV (1.8)) (t12 = 2.3, p < 0.05). Peak amplitude of BF was significantly smaller in LC (37.7 lV (28.6)) than in nLC (50.9 lV (35.6)) (t12 = 4.2, p < 0.01). Peak latency of GcM was significantly shorter in LC (75.5 ms (42.4)) than in nLC (99.3 ms (53.2)) (t12 = 2.5, p < 0.05). With regard to correlations between postural movement indices and onset times of postural muscles, significant correlations were found between ankle movement angle and Sol onset time, and between hip movement angle and BF onset time (p < 0.05) (Table 1). With regard to correlations between postural movement indices and EMG mean amplitude just before S2, ankle movement
***
***
Gastrocnemius
Soleus
no-limitation limitation
20 0
**
-20 -40 -60 -80
Erector spinae
Biceps femoris
Postural muscles Fig. 5. Means and standard deviations of onset times of postural muscles with respect to burst onset of anterior deltoid (AD) p < 0.01; p < 0.001. Significant differences between burst onsets of AD and each postural muscle (p < 0.001).
angle correlated with mean amplitudes of ES and Sol (p < 0.01), knee movement angle correlated with BF mean amplitude (p < 0.05), and hip movement angle correlated with mean amplitudes of ES and Sol (p < 0.01). CoPap displacement correlated with onset times of ES, GcM and Sol (p < 0.01), and with ankle movement angle (p < 0.01). 4. Discussion The present study tried to induce preceding activation of TS with respect to AD during bilateral shoulder flexion from the body side position. For that purpose, a condition limiting the anterior displacement range of CoPap caused by shoulder flexion was set using an inclination board. In experimental trials under LC after the practice trials, floor inclination was seen in 13% of trials, regardless of trial progress. By providing feedback information on inclination to subjects, CoPap anterior displacement largely reduced (12 mm). This showed that CoPap anterior displacement could be limited using the present method. In LC, clear preceding activation with respect to AD was found in TS, as well as in ES and BF. We will discuss this activation in comparison with that in nLC. In discussions about postural muscle activation, some limitations exist to evaluating global activity of each muscle. It has been reported that surface potentials are more localized in pinnate muscles, as the muscle fibers are more oblique to the skin (Mesin et al., 2011) and that bi-articular muscles play region-specific functional roles (Watanabe et al., 2012). Activation patterns of postural muscles should thus be discussed taking these limitations into consideration. Under nLC, the knee and hip significantly extended according to shoulder flexion, but the ankle did not move. This suggests that by backward inclination of the trunk with relatively high mass, postural disturbance would be moderated. In this case, the preceding activation of postural muscles with respect to AD was found in ES and BF, but not in TS. ES and BF activation would generate extension of the trunk and hip joint. For TS, stiffness of the contractile portion of muscle is reportedly higher than that of tendon at dorsiflexion below 0.5° and is not associated with knee movement (Loram et al., 2007). We consider that for TS under nLC, the focus of postural control might be on stiffness rather than preceding activation. On the other hand, under LC, the ankle and knee respectively plantarflexed and extended by 1.1°, with no hip movement. Equal movement angle of the ankle and knee indicates that thigh inclina-
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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Table 1 Significant correlations between each parameter. Onset time of postural muscles Sol Movement angle Ankle Knee Hip CoPap displacement
GcM
BF
EMG mean amplitude just before S2 ES
0.47
Sol
BF
0.58
Movement angle ES
Ankle
0.66 0.42
0.42 0.86
0.82
0.62 0.51
tion was maintained during shoulder flexion, as well as hip joint angle. Crenna et al. (1987) suggested that backward inclination of the whole body pivoting at the ankles is the postural movement pattern required to effectively translate the COG backward. Thus, the postural control strategy adopted under LC would be backward inclination of the whole body pivoting at the ankle to reduce CoPap anterior displacement. For this postural control strategy, TS was activated prior to AD activation and the onset time was almost the same as those of ES and BF. Onset time of TS correlated with CoPap displacement. For burst of GcM activation, peak amplitude showed no significant difference between conditions, while peak time under LC was clearly reduced. Fujiwara et al. (2011b) reported that peak times of BF and GcM were significantly shorter in a simple-reaction task that required a rapid response than in a self-timing task. These results indicate that in order to reduce CoPap anterior displacement, the focus of postural control would be on rapid activation of TS, and the ankle joint would then largely plantarflex. As mentioned above, movement angles of the ankle and knee are very small (about 1.1°). Gurfinkel’ et al. (1983) reported that the perceptual threshold in angular displacement of the ankle joint was extremely lower when standing (0.04–0.13°) than when sitting. In the present study, movement angles of the ankle and hip joints correlated with onset times of Sol and BF, respectively. These suggest that joint movements would be perceived with relatively higher sensitivity based on the integrated multiple sensory information, and would be controlled synergistically (Amblard et al., 1997). Clinical training of postural control should therefore be conducted with consideration of sensory integration via a sensory reference frame. The timing of preceding activation of ES was earlier under LC than under nLC. In our previous study, subjects who inclined the legs backward and the trunk forward did not show any clear preceding activation of ES (Fujiwara et al., 2007). As described above, under LC, the lower legs largely inclined backward, while the hip joint did not move. These findings suggest that under LC, the forward inclination of the trunk induced by inertia during backward inclination of the lower legs would be inhibited by the preceding activation of ES. For ES only, muscle activation just before S2 was significantly larger under LC than under nLC. This muscle activation correlated closely with movement angles of the ankle and hip. The increment in ES stiffness would also achieve a marked effect to inhibit forward inclination of the trunk. For BF, no significant difference was found between conditions in preceding onset time. The function of BF for the hip joint would be similar to that of ES for the trunk including the pelvis. The knees extended under both conditions, but the degree of extension was larger under LC than under nLC. The knee has a locking structure that prevents anterior rotation, which may be related to the lack of significant differences in muscle activation of BF just before S2 between conditions and the decrease in burst activity of BF under LC. Thus, by limiting CoPap anterior displacement, we demonstrated that clear preceding activation of TS could be induced for young adults, even with bilateral shoulder flexion from the body
0.60 0.53
side position. In future studies, we intend to use this limitation method to investigate whether preceding activation of TS can be induced for elderly individuals and whether changes can be obtained with muscle training of TS. Furthermore, we will examine transient floor translation with this limitation and investigate activation patterns of TS. 5. Conclusions By limiting CoPap anterior displacement, a postural control strategy of backward inclination of the entire body pivoting at the ankles is adopted and preceding activation of TS can be induced. Using this method, both the role of and the training effects on TS for anticipatory postural control during shoulder flexion may be able to be clearly investigated in the elderly. Conflict of interest We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. Acknowledgement This work was supported by Grant-in-Aid for Scientific Research (B) (23300238). References Amblard B, Assaiante C, Fabre JC, Mouchnino L, Massion J. Voluntary head stabilization in space during oscillatory trunk movements in the frontal plane performed in weightlessness. Exp Brain Res 1997;114(2):214–25. Belen’kiı˘ VE, Gurfinkel’ VS, Pal’tsev EI. Elements of control of voluntary movements. Biofizika 1967;12(1):135–41. Bouisset S, Zattara M. A sequence of postural movements precedes voluntary movement. Neurosci Lett 1981;22(3):263–70. Cordo PJ, Nashner LM. Properties of postural adjustments associated with rapid arm movements. J Neurophysiol 1982;47(2):287–302. Crenna P, Frigo C, Massion J, Pedotti A. Forward and backward axial synergies in man. Exp Brain Res 1987;65(3):538–48. Fujiwara K, Toyama H, Kunita K. Anticipatory activation of postural muscles associated with bilateral arm flexion in subjects with different quiet standing positions. Gait Posture 2003;17(3):254–63. Fujiwara K, Maeda K, Kunita K, Tomita H. Postural movement pattern and muscle action sequence associated with self-paced bilateral arm flexion during standing. Percept Mot Skills 2007;104(1):327–34. Fujiwara K, Toyama H, Asai H, Yaguchi C, Irei M, Naka M, et al. Effects of regular heel-raise training aimed at the soleus muscle on dynamic balance associated with arm movement in elderly women. J Strength Cond Res 2011a;25(9):2605–15. Fujiwara K, Yaguchi C, Shen X, Maeda K, Mammadova A. Activation timing of postural muscles during bilateral arm flexion in self-timing, oddball and simple-reaction tasks. J Electromyogr Kinesiol 2011b;21(4):595–601. Goshima K. Studies on items and normal ranges in stabilometry. Equilibrium Res 1986;45(4):368–87 [In Japanese with English Abstract]. Gurfinkel’ VS, Lipshits MI, Popov KE. Thresholds of kinesthetic sensation in the vertical posture. Hum Physiol 1983;8(6):439–45. Horak FB, Nashner LM. Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol 1986;55(6):1369–81. Horak FB, Shupert CL, Mirka A. Components of postural dyscontrol in the elderly: a review. Neurobiol Aging 1989;10(6):727–38.
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K. Fujiwara, C. Yaguchi / Journal of Electromyography and Kinesiology xxx (2013) xxx–xxx Lee WA, Buchanan TS, Rogers MW. Effects of arm acceleration and behavioral conditions on the organization of postural adjustments during arm flexion. Exp Brain Res 1987;66(2):257–70. Loram ID, Maganaris CN, Lakie M. The passive, human calf muscles in relation to standing: the non-linear decrease from short range to long range stiffness. J Physiol 2007;584(Pt 2):661–75. Mesin L, Merletti R, Vieira TM. Insights gained into the interpretation of surface electromyograms from the gastrocnemius muscles: a simulation study. J Biomech 2011;44(6):1096–103. Watanabe K, Kouzaki M, Moritani T. Task-dependent spatial distribution of neural activation pattern in human rectus femoris muscle. J Electromyogr Kinesiol 2012;22(2):251–8. Woollacott MH, Manchester DL. Anticipatory postural adjustments in older adults: are changes in response characteristics due to changes in strategy? J Gerontol 1993;48(2):M64–70.
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Chie Yaguchi received her PhD from Kanazawa University in 2012. She is an assistant professor at the Department of Physical Therapy, Faculty of Human Science, Hokkaido Bunkyo University (2011-Present). She is a member of the Society for Neuroscience. She is currently performing research into the relationship between anticipatory postural control and visuo-spatial attention.
Katsuo Fujiwara received his PhD from Tsukuba University in 1984. He is a professor at the Department of Human Movement and Health, Graduate School of Medical Science, Kanazawa University (2001-Present). He is a member of the International Society of Electrophysiological Kinesiology, the International Society of Posture and Gait Research, and the Society for Neuroscience. He serves as a president of the Japanese Society of Health and Behavior Science. He is now analyzing the anticipatory processes of postural control in the brain by using electromyograms, evoked potentials, eventrelated potentials, and cerebral blood flow.
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion Katsuo Fujiwara a,⇑, Chie Yaguchi b a b
Department of Human Movement and Health, Graduate School of Medical Science, Kanazawa University, 13-1 Takara-machi, Kanazawa 920-8640, Japan Department of Physical Therapy, Faculty of Human Science, Hokkaido Bunkyo University, 5-196-1, Kogane-chuo, Eniwa 061-1449, Japan
a r t i c l e
i n f o
Article history: Received 28 August 2012 Received in revised form 19 July 2013 Accepted 28 July 2013 Available online xxxx Keywords: Anticipatory postural control Arm movement Center of foot pressure Electromyogram Strategy
a b s t r a c t In bilateral shoulder flexion with the arms moving from the sides of the body to the horizontal level while standing, no preceding activation of the triceps surae (TS) with respect to focal muscles has been found. Considering that preceding activation would offer a useful indicator of anticipatory postural control, it was attempted to induce preceding activation by limiting the anterior displacement range of the center of foot pressure in the anteroposterior direction (CoPap). Subjects were 13 healthy young adults. The 50% anterior range of CoPap displacement caused by shoulder flexion was calculated, and the floor inclined by the subject’s weight when CoPap extended beyond that range. Subjects were instructed not to incline the floor during shoulder flexion. Under the limitation condition, the ankle and knee joints plantarflexed and extended at 1.1°, respectively, with no hip movement; that is, the whole body inclined backward by pivoting at the ankle. This limitation resulted in preceding muscle activation of TS as well as erector spinae and biceps femoris, and no significant differences in onset time were seen between these muscles. These results demonstrated that by limiting CoPap anterior displacement, preceding activation of TS could be induced with backward inclination of the whole body. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction With rapid movements of the arms while standing, the postural muscles of the legs and trunk are automatically activated before the focal muscles of the arms, to moderate any disturbances of posture and equilibrium caused by the arm movement (Belen’kiı˘ et al., 1967). Cordo and Nashner (1982) reported that the timing of postural muscle activation changes according to internal and external conditions. In addition, they proposed that the preceding muscle activation is clearly observed in those postural muscles playing the most important roles in balance maintenance. Marked preceding activation is found in the biceps femoris (BF), and the onset time was found to be earlier under conditions of rapid (Lee et al., 1987) and self-paced shoulder flexion (Fujiwara et al., 2011b), anterior initial position of the center of gravity (COG) (Fujiwara et al., 2003) and postural movement patterns in which the legs and trunk or trunk alone were inclined backward (Fujiwara et al., 2007). However, when shoulder flexion has been performed in previous studies with the arm moving from the side of the body to the horizontal level, preceding activation of the triceps surae (TS) has not been observed (Bouisset and Zattara, 1981). This ⇑ Corresponding author. Tel.: +81 76 265 2225; fax: +81 76 234 4219.
presumably results from a lack of task condition in which the preceding activation of TS is necessary for postural control. The present study was designed to provide useful background information in order to subsequently select tasks in which preceding activation of TS is recognized. For postural control during transient floor translation, a postural movement pattern focused on the hip joint (hip strategy) is adopted with a narrow base of support in the anteroposterior direction, while with a wide support base, the movement pattern focused on the ankle joint (ankle strategy) (Horak and Nashner, 1986). The muscles around the hip joint and the lower leg muscles are mainly activated in these hip and ankle strategies, respectively. These findings indicate that in transient floor translation with a wide support base, torque around the ankle starts to change earliest, so the focus of postural control is put on the lower leg muscles, while with a narrow support base, the focus is switched to the muscles around the hip joint. However, no studies have examined activation patterns of postural muscles during bilateral shoulder flexion on a stable platform when subjects try to keep the center of foot pressure in the anteroposterior direction (CoPap) within a restrictive range of the support base. We considered that with bilateral shoulder flexion from the body side position, preceding activation of TS might be induced by narrowing only the anterior range of the support base, while keeping a wide posterior range. In this case, to limit anterior displacement of CoPap, a strategy in which the center of body mass
E-mail address: [email protected] (K. Fujiwara). 1050-6411/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jelekin.2013.07.015
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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moves backward with the postural control focused on the ankle is adopted, and any preceding activation of TS would be clearly apparent. In the present study, the floor was inclined when CoPap extended beyond a determined anterior range. Based on the feedback information of floor inclination, the subjects were required to control their posture to avoid inclining the floor. A standing posture with the upper limbs at the side of the body is fundamental and arm movements from this position are frequently performed during daily life. In the elderly, decreased muscle strength of the lower legs leads to deterioration in balance function (Horak et al., 1989). Fujiwara et al. (2011a) reported that during shoulder flexion from hands at the side of the body, the soleus (Sol) activated slightly earlier following muscle training of TS, but clear preceding activation was not observed. If preceding activation of TS is able to be induced for young adults during shoulder flexion from this hand position, this task condition could be effectively applied for the elderly (Woollacott and Manchester, 1993). We therefore investigated the onset timing of TS and postural movement patterns by narrowing the anterior range of the support base, first in young adults. Our working hypothesis was that during bilateral shoulder flexion with limitation of CoPap anterior displacement, the preceding activation of TS would be induced, with backward inclination of the whole body pivoting at the ankles. 2. Methods 2.1. Subjects Subjects comprised 7 men and 6 women. Mean values (standard deviation (SD)) for age, height, weight, foot length and lower leg length were 24.8 (5.0) years, 165.5 (8.1) cm, 59.3 (8.1) kg, 24.5 (1.5) cm and 40.5 (2.3) cm, respectively. No subjects reported any history of neurological or orthopedic impairment. In accordance with the Declaration of Helsinki, all subjects provided informed consent after receiving an explanation of the experimental protocol, which was approved by our institutional ethics committee. 2.2. Apparatus To measure CoPap, a force platform (FPA34; Electro-design, Noda, Japan) was used. CoPap position was shown as a percentage of the distance from the heel in relation to foot length (%FL). CoPap electronic signals were sent simultaneously to three devices: a computer (PC9801BX; NEC, Tokyo, Japan) to determine CoPap position; another computer (Dimension E521; Dell Japan, Kawasaki, Japan) for analysis; and an oscilloscope (DS6612; Iwatsu, Tokyo, Japan) to monitor the results. The onset time of postural muscles is influenced by CoPap position just before shoulder flexion (Fujiwara et al., 2003). To control initial CoPap positions, the first computer, which received CoPap data via an analog-to-digital (A/D) converter (PIO9045; I/O-Data, Kanazawa, Japan) with a 20-Hz sampling rate and 12-bit resolution, generated a buzzing sound when CoPap was located within a range of ±1 cm of the quiet standing posture (QSP range). Since the SD for CoPap fluctuation during QSP for 60 s was approximately 0.5 cm for young healthy subjects (Goshima, 1986), the QSP range corresponds to ±2 SDs of the fluctuation. The 50% range of most anterior displacement of the CoPap caused by shoulder flexion was calculated. To limit the anterior displacement range of CoPap, we used a handmade inclination board on the force platform that underwent forward-inclination by 10° due to the subject’s weight when CoPap extended beyond that range (Fig. 1). Arm acceleration was recorded using a miniature unidirectional accelerometer (AS-5GB; Kyowa, Tokyo, Japan) placed on the dorsal
surface of the right wrist. To detect the beginning of arm movement, the axis of sensitivity before shoulder flexion was along the anteroposterior direction. To measure arm, trunk and leg motions in the sagittal plane during shoulder flexion, a position sensor system (C5949; Hamamatsu Photonics, Hamamatsu, Japan) was used. The sensor head was placed 4.0 m away from the right side of the subject. Lightemitting diode (LED) targets were placed over the following landmarks on the right side: the wrist; spinous process of C7; midpoint of the greater trochanter (GT); lateral epicondyle (LE); lateral malleolus (LM); and the fifth metatarsal head (MH) (Fig. 1). The x- and y-coordinates of LED targets were recorded at 0.3-mm resolution. A fixation point was presented at the center of an eye-trek facemounted display (FMD011F; Olympus, Tokyo, Japan). Warning (S1) and response (S2) signals were auditory stimuli delivered via earphones with frequency, intensity, duration and inter-stimulus interval of 2000 Hz, 35 dB above the auditory threshold, 100 ms and 2 s, respectively. Surface electrodes (30-mm diameter, 13-mm diameter capture area, P-00-S; Ambu, Ballerup, Denmark) were used in bipolar derivation to record electromyographic (EMG) activity of the following muscles: the anterior deltoid (AD) as a focal muscle for shoulder flexion; rectus abdominis (RA) at the level of the navel, erector spinae (ES) at the level of the iliac crest, rectus femoris (RF) at the midpoint between the anterior inferior iliac spine and upper border of the patella, long head of BF at the midpoint between the ischial tuberosity and head of the fibula, tibialis anterior (TA), medial head of gastrocnemius (GcM) and Sol as postural muscles (Fig. 1). Electrode locations for AD, TA, GcM and Sol were the midportion of the muscle belly. Electrodes were placed on the right side of the body with an inter-electrode (center-to-center) distance of about 3 cm. A ground electrode was placed over the right LM. These electrodes were fixed after shaving and cleaning the skin with alcohol. Inter-electrode impedance, as measured by an impedance tester, was reduced to below 5 kX. EMG signals from electrodes were amplified (4000) and band-pass filtered (5–500 Hz) using an analog amplifier (Biotop-6R12; NEC-Sanei, Tokyo, Japan; common mode rejection ratio, 86 dB; input impedance, >10 MX). All electrical signals, including CoPap, arm acceleration, x- and y-coordinates of each LED, S1 and S2 signals and each EMG, were sent to the computer for analysis via A/D converters (ADJ-98; Canopus, Kobe, Japan) with a 1000-Hz sampling rate and 16-bit resolution. 2.3. Procedure All measurements were performed on the force platform while standing barefoot with feet 10 cm apart and parallel, elbows extended, and hands positioned on the thigh anterior to GT (Fig. 1). Subjects were instructed to gaze at the fixation point during all measurements. First, after the experimenter told the subject to maintain a stabilized QSP and confirmed the stabilization, CoPap fluctuation for 10 s was measured and the mean position was calculated. The mean value of five measurements was adopted as the QSP position. Next, bilateral shoulder flexion trials were commenced. Subjects maintained CoPap position within the QSP range for at least 3 s while hearing the buzzing sound. S1 was randomly presented within 1–3 s after the experimenter stopped the buzzing sound, and then S2 was started 2 s after S1. In response to S2, subjects flexed the arms at maximum speed, stopped voluntarily at the shoulder level, and maintained this position for 3 s. Shoulder flexion trials were repeated 20 times on the flat floor (no-limitation condition, nLC), and the 50% range of most anterior displacement of the CoPap was calculated. Inclination axis of the floor was set
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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Face-mounted display
EMG C7
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Wrist Rectus abdominis
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Biceps femoris
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Rectus femoris Lateral epicondyle
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Fifth metatarsal head Position sensor camara
Fig. 1. Experimental set-up for measurement of EMG and postural movement during shoulder flexion and for limitation of CoPap anterior displacement.
at that range (mean position for 20 trials) (Fig. 1). Subjects were then instructed not to incline the floor during the shoulder flexion (limitation condition, LC). Shoulder flexion trials under LC were repeated 20 times. To familiarize subjects with the task, 10 practice trials for each condition were performed before the experimental trials. Under each condition, experimental trials in which CoPap position just before the shoulder flexion was beyond the QSP range were rejected. Furthermore, under LC, trials in which the subject failed to prevent inclination of the floor were also rejected. The experiment was conducted with a 30-s standing rest between each trial and a 3-min seated rest between conditions.
2.4. Data analysis Under LC, the percentage of inclined trials among all trials was calculated. All data were analyzed blinded to condition using signal-processing software (BIMUTAS II; Kissei Comtec, Matsumoto, Japan). We defined the first deviation in the accelerometer signal as the start point of arm movement (Fig. 2). The end of arm movement was defined as the end of the second burst of AD activity included in the envelop line that first deviated below the mean +2 SDs just before 500 ms of arm lowering, with reference to the curves of wrist position and arm acceleration. The interval between start point and endpoint of arm movement was defined as the arm movement duration. Mean CoPap positions were calculated for the periods from 300 to 150 ms with respect to the burst onset of AD (before arm movement period) and from 0 to +150 ms with respect to the endpoint of arm movement (after arm movement period) (Fig. 2). Differences between these mean positions were defined as CoPap displacements. Ankle (LE – LM – MH), knee (GT – LE – LM), and hip (C7 – GT – LE) angles in the sagittal plane were calculated using Excel 2010 software (Microsoft, Tokyo, Japan) based on x- and y-coordinates of LED targets (Fig. 2). For each angle, mean values were then calculated for the periods before and after arm movement. Differences in mean angles between the two time periods were calculated and defined as movement angles of the ankle, knee, and hip, respec-
tively (Fig. 2). Movement angles were considered positive for dorsiflexion of the ankle and flexion of the knee and hip. EMGs were analyzed as described below with reference to a previous study (Fujiwara et al., 2011b) (Fig. 2). To exclude electrocardiographic and movement artifacts, all EMGs were high-pass filtered at 40 Hz using a seventh-order Butterworth method and then full-wave rectified (rEMG). Mean and SD of the amplitude for background activity of each muscle was calculated during the period from 150 to 0 ms with respect to S2 onset for AD and from 300 to 150 ms with respect to burst onset of AD for postural muscles. Burst activation of each muscle was identified when onset was within +100 to +300 ms after S2 onset for AD and 150 to +100 ms with respect to burst onset of AD for postural muscles, and when the envelope line of the burst activity deviated more than the mean +2 SDs from background activity for at least 50 ms. Burst onset was defined as the time point at which the above deviation began in the EMG wave included in the envelope line. AD reaction time was defined as the time difference between S2 onsets and the AD burst. The onset time of postural muscles was defined as the time difference between burst onsets of postural muscles and AD, and presented as a negative value when burst onset of postural muscles preceded AD. Preceding EMG bursts of postural muscles were observed only in the dorsal muscles. Subsequently, activities of the frontal muscles (RA, RF and TA) sometimes or scarcely occurred between bimodal bursts in the dorsal muscles. As a result, only EMG bursts in the dorsal postural muscles were analyzed. To investigate EMG activity before S2, rEMG of each postural muscle from 500 ms before S1 to S2 was averaged for each condition. Then the averaged waveform was low-pass filtered at 40 Hz to detect the envelop line of the activity. In each averaged waveform, mean amplitude was calculated for 100 ms just before S2. To analyze the activity level for burst activation after arm movement, EMG of each muscle in the period from 300 to +200 ms with respect to burst onset of the muscle was averaged separately for each condition. The averaged EMG waveforms were then smoothed using a 40-Hz low-pass filter (Fujiwara et al., 2011b) to detect the envelop line of the averaged burst activity. EMG peak amplitude from baseline and latency with respect to burst onset were measured.
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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1.0 mV
Anterior deltoid Rectus abdominis Erector spinae Rectus femoris Biceps femoris Tibialis anterior Gastrocnemius Soleus
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onset -300 ms
onset -150ms
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Fig. 2. Representative waveforms of each measurement data under the limitation condition. Arrows with thin straight and dashed lines indicate onset of burst activation of postural muscles and start point of arm movement, respectively. Arrows with thick straight and dashed lines indicate CoPap displacement and each movement angle.
2.5. Statistical analysis 60
no-limitation limitation
***
55
CoPap position (%FL)
Shapiro-Wilk tests confirmed that all data satisfied the assumption of a normal distribution. A one-sample t-test was used to assess whether burst onset of the postural muscles and angles of the ankle, knee and hip after arm movement differed significantly from that of AD and those before arm movement, respectively. A paired t-test was used to assess differences between conditions in CoPap displacement, arm movement duration, each movement angle, AD reaction time, postural muscle activities before S2 and peak amplitudes and latencies of each muscle. Two-way analysis of variance was used to assess the effect of condition (nLC and LC) and muscle on onset time of postural muscles. When a significant interaction between these factors was shown, post-hoc multiple-comparison analyses using Tukey’s honestly significant difference test were performed to assess differences among muscles. Pearson correlations were used to evaluate the magnitude of correlation between each parameter. The alpha level was set at p < 0.05. All statistical analyses were performed using SPSS software (version 14.0J, SPSS Japan, Tokyo, Japan).
50
45
Limited position
40
35
30 start point
endpoint
Fig. 3. Means and standard deviations of CoPap position at the start point and endpoint of the arm movement. p < 0.001.
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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3. Results
60
4
Movement angle (degrees)
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no-limitation limitation
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*
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Fig. 4. Means and standard deviations of movement angles of the ankle, knee and hip p < 0.05; p < 0.001. Significant differences between before and after the arm movement (p < 0.05).
40
Onset time (ms)
Fig. 3 shows CoPap positions at the start point and endpoint of arm movement. Position at the endpoint of arm movement in LC was slightly posterior (2.9%FL (2.2)) to the determined position (4.7%FL (2.0) anterior to QSP position). CoPap displacement was significantly smaller in LC than in nLC (a decrease of 4.9%FL (2.7), i.e., 12.0 mm (6.7)) (t12 = 6.6, p < 0.001). No significant differences were found in the percentage of inclined trials between first and last halves of trials and the percentage of inclined trials among all trials was 13.4% (8.4). Fig. 4 shows movement angles of the ankle, knee, and hip. Angles of the ankle in LC, knee in both conditions and hip in nLC after arm movement were significantly larger in the plantarflexion and extension directions, respectively, than before arm movement (t12 > 2.3, p < 0.05). No significant differences were found between before and after arm movement in angles of ankle in nLC and hip in LC. Significant differences were found between conditions in movement angles of the ankle and knee (t12 > 2.9, p < 0.05). Hip movement angle in LC tended to differ from that in nLC (t12 = 2.1, p = 0.06). No significant differences were found between conditions in AD reaction time or arm movement duration (mean in both conditions: 185 ms and 498 ms, respectively). Preceding activations of postural muscles with respect to AD were found in ES and BF in nLC and in all postural muscles in LC (t12 > 5.6, p < 0.001) (Fig. 5). A significant interaction was found between condition and muscle for onset time of postural muscles (F3,48 = 36.0, p < 0.001). Onset times for ES, GcM and Sol were significantly earlier in LC than in nLC (p < 0.01). In nLC, ES and BF were activated significantly earlier than GcM and Sol (p < 0.001), while in LC, no significant differences in onset time were found for all postural muscles. For ES only, EMG mean amplitude just before S2 was significantly larger in LC (6.4 lV (SD = 5.4)) than in nLC (3.4 lV (1.8)) (t12 = 2.3, p < 0.05). Peak amplitude of BF was significantly smaller in LC (37.7 lV (28.6)) than in nLC (50.9 lV (35.6)) (t12 = 4.2, p < 0.01). Peak latency of GcM was significantly shorter in LC (75.5 ms (42.4)) than in nLC (99.3 ms (53.2)) (t12 = 2.5, p < 0.05). With regard to correlations between postural movement indices and onset times of postural muscles, significant correlations were found between ankle movement angle and Sol onset time, and between hip movement angle and BF onset time (p < 0.05) (Table 1). With regard to correlations between postural movement indices and EMG mean amplitude just before S2, ankle movement
***
***
Gastrocnemius
Soleus
no-limitation limitation
20 0
**
-20 -40 -60 -80
Erector spinae
Biceps femoris
Postural muscles Fig. 5. Means and standard deviations of onset times of postural muscles with respect to burst onset of anterior deltoid (AD) p < 0.01; p < 0.001. Significant differences between burst onsets of AD and each postural muscle (p < 0.001).
angle correlated with mean amplitudes of ES and Sol (p < 0.01), knee movement angle correlated with BF mean amplitude (p < 0.05), and hip movement angle correlated with mean amplitudes of ES and Sol (p < 0.01). CoPap displacement correlated with onset times of ES, GcM and Sol (p < 0.01), and with ankle movement angle (p < 0.01). 4. Discussion The present study tried to induce preceding activation of TS with respect to AD during bilateral shoulder flexion from the body side position. For that purpose, a condition limiting the anterior displacement range of CoPap caused by shoulder flexion was set using an inclination board. In experimental trials under LC after the practice trials, floor inclination was seen in 13% of trials, regardless of trial progress. By providing feedback information on inclination to subjects, CoPap anterior displacement largely reduced (12 mm). This showed that CoPap anterior displacement could be limited using the present method. In LC, clear preceding activation with respect to AD was found in TS, as well as in ES and BF. We will discuss this activation in comparison with that in nLC. In discussions about postural muscle activation, some limitations exist to evaluating global activity of each muscle. It has been reported that surface potentials are more localized in pinnate muscles, as the muscle fibers are more oblique to the skin (Mesin et al., 2011) and that bi-articular muscles play region-specific functional roles (Watanabe et al., 2012). Activation patterns of postural muscles should thus be discussed taking these limitations into consideration. Under nLC, the knee and hip significantly extended according to shoulder flexion, but the ankle did not move. This suggests that by backward inclination of the trunk with relatively high mass, postural disturbance would be moderated. In this case, the preceding activation of postural muscles with respect to AD was found in ES and BF, but not in TS. ES and BF activation would generate extension of the trunk and hip joint. For TS, stiffness of the contractile portion of muscle is reportedly higher than that of tendon at dorsiflexion below 0.5° and is not associated with knee movement (Loram et al., 2007). We consider that for TS under nLC, the focus of postural control might be on stiffness rather than preceding activation. On the other hand, under LC, the ankle and knee respectively plantarflexed and extended by 1.1°, with no hip movement. Equal movement angle of the ankle and knee indicates that thigh inclina-
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015
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K. Fujiwara, C. Yaguchi / Journal of Electromyography and Kinesiology xxx (2013) xxx–xxx
Table 1 Significant correlations between each parameter. Onset time of postural muscles Sol Movement angle Ankle Knee Hip CoPap displacement
GcM
BF
EMG mean amplitude just before S2 ES
0.47
Sol
BF
0.58
Movement angle ES
Ankle
0.66 0.42
0.42 0.86
0.82
0.62 0.51
tion was maintained during shoulder flexion, as well as hip joint angle. Crenna et al. (1987) suggested that backward inclination of the whole body pivoting at the ankles is the postural movement pattern required to effectively translate the COG backward. Thus, the postural control strategy adopted under LC would be backward inclination of the whole body pivoting at the ankle to reduce CoPap anterior displacement. For this postural control strategy, TS was activated prior to AD activation and the onset time was almost the same as those of ES and BF. Onset time of TS correlated with CoPap displacement. For burst of GcM activation, peak amplitude showed no significant difference between conditions, while peak time under LC was clearly reduced. Fujiwara et al. (2011b) reported that peak times of BF and GcM were significantly shorter in a simple-reaction task that required a rapid response than in a self-timing task. These results indicate that in order to reduce CoPap anterior displacement, the focus of postural control would be on rapid activation of TS, and the ankle joint would then largely plantarflex. As mentioned above, movement angles of the ankle and knee are very small (about 1.1°). Gurfinkel’ et al. (1983) reported that the perceptual threshold in angular displacement of the ankle joint was extremely lower when standing (0.04–0.13°) than when sitting. In the present study, movement angles of the ankle and hip joints correlated with onset times of Sol and BF, respectively. These suggest that joint movements would be perceived with relatively higher sensitivity based on the integrated multiple sensory information, and would be controlled synergistically (Amblard et al., 1997). Clinical training of postural control should therefore be conducted with consideration of sensory integration via a sensory reference frame. The timing of preceding activation of ES was earlier under LC than under nLC. In our previous study, subjects who inclined the legs backward and the trunk forward did not show any clear preceding activation of ES (Fujiwara et al., 2007). As described above, under LC, the lower legs largely inclined backward, while the hip joint did not move. These findings suggest that under LC, the forward inclination of the trunk induced by inertia during backward inclination of the lower legs would be inhibited by the preceding activation of ES. For ES only, muscle activation just before S2 was significantly larger under LC than under nLC. This muscle activation correlated closely with movement angles of the ankle and hip. The increment in ES stiffness would also achieve a marked effect to inhibit forward inclination of the trunk. For BF, no significant difference was found between conditions in preceding onset time. The function of BF for the hip joint would be similar to that of ES for the trunk including the pelvis. The knees extended under both conditions, but the degree of extension was larger under LC than under nLC. The knee has a locking structure that prevents anterior rotation, which may be related to the lack of significant differences in muscle activation of BF just before S2 between conditions and the decrease in burst activity of BF under LC. Thus, by limiting CoPap anterior displacement, we demonstrated that clear preceding activation of TS could be induced for young adults, even with bilateral shoulder flexion from the body
0.60 0.53
side position. In future studies, we intend to use this limitation method to investigate whether preceding activation of TS can be induced for elderly individuals and whether changes can be obtained with muscle training of TS. Furthermore, we will examine transient floor translation with this limitation and investigate activation patterns of TS. 5. Conclusions By limiting CoPap anterior displacement, a postural control strategy of backward inclination of the entire body pivoting at the ankles is adopted and preceding activation of TS can be induced. Using this method, both the role of and the training effects on TS for anticipatory postural control during shoulder flexion may be able to be clearly investigated in the elderly. Conflict of interest We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. Acknowledgement This work was supported by Grant-in-Aid for Scientific Research (B) (23300238). References Amblard B, Assaiante C, Fabre JC, Mouchnino L, Massion J. Voluntary head stabilization in space during oscillatory trunk movements in the frontal plane performed in weightlessness. Exp Brain Res 1997;114(2):214–25. Belen’kiı˘ VE, Gurfinkel’ VS, Pal’tsev EI. Elements of control of voluntary movements. Biofizika 1967;12(1):135–41. Bouisset S, Zattara M. A sequence of postural movements precedes voluntary movement. Neurosci Lett 1981;22(3):263–70. Cordo PJ, Nashner LM. Properties of postural adjustments associated with rapid arm movements. J Neurophysiol 1982;47(2):287–302. Crenna P, Frigo C, Massion J, Pedotti A. Forward and backward axial synergies in man. Exp Brain Res 1987;65(3):538–48. Fujiwara K, Toyama H, Kunita K. Anticipatory activation of postural muscles associated with bilateral arm flexion in subjects with different quiet standing positions. Gait Posture 2003;17(3):254–63. Fujiwara K, Maeda K, Kunita K, Tomita H. Postural movement pattern and muscle action sequence associated with self-paced bilateral arm flexion during standing. Percept Mot Skills 2007;104(1):327–34. Fujiwara K, Toyama H, Asai H, Yaguchi C, Irei M, Naka M, et al. Effects of regular heel-raise training aimed at the soleus muscle on dynamic balance associated with arm movement in elderly women. J Strength Cond Res 2011a;25(9):2605–15. Fujiwara K, Yaguchi C, Shen X, Maeda K, Mammadova A. Activation timing of postural muscles during bilateral arm flexion in self-timing, oddball and simple-reaction tasks. J Electromyogr Kinesiol 2011b;21(4):595–601. Goshima K. Studies on items and normal ranges in stabilometry. Equilibrium Res 1986;45(4):368–87 [In Japanese with English Abstract]. Gurfinkel’ VS, Lipshits MI, Popov KE. Thresholds of kinesthetic sensation in the vertical posture. Hum Physiol 1983;8(6):439–45. Horak FB, Nashner LM. Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol 1986;55(6):1369–81. Horak FB, Shupert CL, Mirka A. Components of postural dyscontrol in the elderly: a review. Neurobiol Aging 1989;10(6):727–38.
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Chie Yaguchi received her PhD from Kanazawa University in 2012. She is an assistant professor at the Department of Physical Therapy, Faculty of Human Science, Hokkaido Bunkyo University (2011-Present). She is a member of the Society for Neuroscience. She is currently performing research into the relationship between anticipatory postural control and visuo-spatial attention.
Katsuo Fujiwara received his PhD from Tsukuba University in 1984. He is a professor at the Department of Human Movement and Health, Graduate School of Medical Science, Kanazawa University (2001-Present). He is a member of the International Society of Electrophysiological Kinesiology, the International Society of Posture and Gait Research, and the Society for Neuroscience. He serves as a president of the Japanese Society of Health and Behavior Science. He is now analyzing the anticipatory processes of postural control in the brain by using electromyograms, evoked potentials, eventrelated potentials, and cerebral blood flow.
Please cite this article in press as: Fujiwara K, Yaguchi C. Effects of limiting anterior displacement of the center of foot pressure on anticipatory postural control during bilateral shoulder flexion. J Electromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.07.015