Effects of abdominal muscle fatigue on anticipatory postural adjustments associated with arm raising

Gait & Posture 24 (2006) 342–348 www.elsevier.com/locate/gaitpost

Effects of abdominal muscle fatigue on anticipatory postural adjustments associated with arm raising S.L. Morris *, G.T. Allison The Centre for Musculoskeletal Studies School of Surgery and Pathology, The Faculty of Medicine and Dentistry, The University of Western Australia, Level 2 Medical Research Foundation Building, Rear 50 Murray Street, Perth, WA 6000, Australia Received 11 February 2005; received in revised form 11 October 2005; accepted 20 October 2005

Abstract Anticipatory postural adjustments (APAs) are postulated to ameliorate the effects of the disturbance to posture caused by voluntary movement. The primary hypothesis tested in our study was that the magnitude of anticipatory trunk muscle activity is altered by abdominal muscle fatigue. A subsidiary aim of the present study was to examine the directional nature of APAs and use this information to elucidate the central or peripheral nature of changes in postural muscle activity associated with abdominal muscle fatigue. The present study was a within subject design, where abdominal muscle fatigue was induced by a static abdominal curl. Surface EMG was used to assess postural muscle activity in the following trunk muscles; rectus abdominis, erector spinae and internal oblique. Following abdominal muscle fatigue, the magnitude of muscle activity during APAs was significantly reduced by 20% in both the rectus abdominis (fatigued muscle) and the erector spinae (not fatigued) indicating a central rather than peripheral fatigue effect on muscle activity. Abdominal muscle fatigue also induced a 30% increase in the baseline muscle activity of the internal oblique. The changes in magnitude of APA muscle activity may reflect a change in system gain or a change in postural control perhaps related to a change in perceived postural stability. An increase in baseline muscle activity in the internal oblique may compensate partially for the reduction in APAs. # 2005 Elsevier B.V. All rights reserved. Keywords: Anticipatory postural adjustments; Trunk control; Fatigue; Abdominal muscles

1. Introduction Anticipatory postural adjustments (APAs) are modifications to posture which occur immediately prior to predictable postural perturbations including voluntary movements [1–3]. APAs are thought to pre-empt and counteract the anticipated disturbing effects of movement and are dependent on both the expected magnitude and direction of the perturbation to posture [1,3,4]. This is consistent with reports associating the peak arm acceleration with the size of the EMG signals in the postural muscles during APAs [5–7]. In addition to a dependence on the expected task constraints, there is a variety of research supporting Cordo and Nashner’s assertion that APAs depend on the postural set, that is ‘‘the * Corresponding author. Tel.: +61 8 6488 3630; fax: +61 8 9224 0204. E-mail address: [email protected] (S.L. Morris). URL: http://www.cms.uwa.edu.au/ 0966-6362/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2005.10.011

individual’s perception of their steady-state postural equilibrium and quality of external support’’ [8]. Unstable surfaces, altered configurations of base of support, altered orientation of the body and haptic cues have all been reported to influence the anticipatory control of posture [6,9–11]. Postural muscle fatigue has been reported to alter APA muscle activity in trunk muscles [12] and in lower limb muscles [13]. Muscle fatigue induces changes in internal body state which have both peripheral and central components [14]. The main hypothesis to be tested in this study is that muscle fatigue induced by a fatiguing static abdominal curl is associated with a change in the magnitude of anticipatory trunk muscle activity. A subsidiary aim of the present study was to examine the directional nature of APAs and use this information to elucidate the central or peripheral nature of changes in muscle activity after fatigue. Baseline muscle activity occurring prior to the onset of the APA is generally used as a reference point which is either

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subtracted or actively minimized in the assessment of the APA [6,7,10,11,15–17]. Independent examination of tonic or baseline muscle activity associated with APAs has rarely been discussed in the literature. Aruin [7] reported larger baseline muscle activity in the erector spinae and biceps femoris prior to APAs while bending forwards compared with upright standing. Slijper and Latash [11] reported increases in baseline muscle activity prior to APAs in the rectus femoris when standing on an unstable board. Since baseline muscle activity is likely to influence postural set, the present study includes an assessment of the effect of direction of arm movement and abdominal muscle fatigue on baseline muscle activity.

2. Methods 2.1. Subjects Seven right arm dominant subjects (six men), mean age 32.4 years, range 18–44, participated in two sessions of testing each 2 weeks apart. The subjects had no diagnosis of any pathological condition, had never experienced surgery to the trunk or abdomen, had no history of serious injury to the shoulder, were not using medication regularly, had not experienced pain requiring medical attention or which altered the activities of daily living for at least the past year and reported normal health at the time of testing. While all subjects were fit for exercise, none were trained athletes. Informed consent was obtained and the experiment was approved by the University of Western Australia’s Human Research Ethics Committee in accordance with the ethical standards defined by the 1964 Declaration of Helsinki. 2.2. Apparatus Electromyographic activity (EMG) was recorded using bipolar Ag/AgCl surface electrodes placed on the following trunk muscle sites contralateral to the side of arm movement;

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left rectus abdominis (RA) – 3 cm lateral to the umbilicus (according to Juker et al. [18]); left lumbar erector spinae (ES) – 3 cm lateral to the L3 spinous process; both aligned along the trunk axis (according to Juker et al. [18]) and left internal oblique (IO) – approximately 15 cm lateral to the umbilicus and just superior to the inguinal ligament and aligned transverse to the trunk axis (adapted from Juker et al. [18]). The right sides of each of the three trunk muscles were also recorded during the static abdominal curl. Surface electrodes were also placed on the right anterior and posterior deltoid. A ground electrode was placed over the right clavicle. EMG data were amplified (5000), analog filtered at 10– 1000 Hz (Grass series seven amplifiers) and digitally sampled at 2000 Hz, during arm movements and sampled at 1000 Hz, during the static abdominal curl using a 16 bit National Instruments DAQ card. Signals were digitally bandpass filtered between 15 and 400 Hz using a fourth order, zero lag butterworth filter. EMG gain was calibrated to the peak amplitude of muscle activity for each muscle during the practice trials. A Grass SPA1 single plane accelerometer, sensitivity 8G, was attached to the upper arm and used to record the acceleration of the arm. 2.3. Procedure The experimental protocol depicted in Fig. 1 contained three sets of procedures. Arm raising movements were used to invoke APAs (Fig. 1A, C and E). Each subject stood 3 m from a pair of lights located in the centre of their visual field. The subjects’ foot position was their self-selected normal standing posture and an outline of foot position was recorded. Subjects maintained this foot position for testing in both sessions. The initial position of the arm was held loosely at the side with thumb facing forwards. During each trial, subjects were required to raise their arm (either backwards or forwards) rapidly in quick response to a ‘‘go’’ light (simple reaction time mode). Subjects were told the direction of arm movement and a warning light was provided at random intervals between 2 and 5 s prior to the ‘‘go’’ light.

Fig. 1. Experimental design. The following protocol was undertaken: (A) 30 rapid arm forwards and 30 rapid arm backwards movements alternating direction of movement (pre-fatigue 1)—for each direction of arm movement, early referred to the first 10, middle to the second 10 and late to the third 10; followed by (B) a relaxed sit on the floor then (C) get up quickly to undertake 10 rapid arm forwards and 10 rapid arm backwards movements alternating direction of movement (pre-fatigue 2 early). Following this (D) a static abdominal curl to fatigue and then (E) get up quickly to undertake 30 rapid arm forwards and 30 rapid arm backwards movements alternating direction of movement (post-fatigue 1)—early (first 10), middle (second 10) and late (third 10). Steps D and E were repeated (post-fatigue 2)—early (first 10), middle (second 10) and late (third 10).

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Subjects underwent a set of 10 practice trials in each direction of arm movement prior to the beginning of the each session of testing. The intervention conditions were of two types. A control condition involving a relaxed sit and rise quickly to standing for testing was included in order to control for the effect of the experimental procedure on APAs (Fig. 1B and C). The sit was a similar position to that of the static abdominal curl but with minimal muscle use. The second and active intervention condition was the static abdominal curl (bent knees) during which subjects were directed to hold the position (Fig. 1D) for as long as possible. Subjects were required to maintain the position without reclining or sitting up further until fatigue. Fatigue was determined as the point at which the subject could no longer hold the posture due to muscle weakness. Following the static abdominal curl, subjects were requested to rise quickly to standing to begin APA testing. Fig. 1 describes the experimental protocol. 2.4. Data analysis In order to derive a variable reflecting the degree of muscle fatigue during the static abdominal curl, the first 5 s of each signal was cropped, the signal demeaned and the median frequency (the frequency at which the power of the FFT (Hamming window) derived power spectrum is halved) was calculated in a moving window of 2000 data points with a 1000 point slide. All signals were time normalised to 20 points and the averaged in tertiles. The derived variable change in median frequency was the percentage change between the initial and final tertile as a percentage of the initial tertile. Changes in median frequency were averaged bilaterally to aid reliability [18]. Each EMG signal for each muscle in a trial was examined visually. Trials were rejected because of outlier reaction time (10% of cases) or heart rate artifact in APA window of the signal (25% of cases). Derived variables associated with APAs were calculated in relation to the time of the onset of the deltoid muscle during the arm movement. T0 was defined as the onset of the deltoid muscle associated with the focal movement (anterior deltoid for arm forwards and posterior deltoid for arm backwards). The reaction time was the time from the ‘‘go’’ light to T0. Baseline muscle activity was determined by calculating the integrated EMG amplitude R ( EMG) in seven 50 ms blocks from 600 to 250 ms prior to T0 (EMG signals reflecting APA activity never occurred prior to 250 ms before T0 in any of the postural muscles). Baseline muscle activity was defined as the median R of the seven blocks. APA muscle activity was defined as the EMG of the postural muscle from 100 to +50 ms with respect to T0 (the APA window) minus the baseline muscle activity for the trial (50 R ms  3 = 150 ms) [3]. Focal muscle activity was the EMG of deltoid muscle associated with the focal movement calculated in the same way as APA muscle activity. Peak acceleration of the arm was determined as the absolute peak signal value in the first 100 ms of arm movement.

R

EMG was averaged in epochs of 10 consecutive trials in the same direction of arm movement. Trial rate was 1 trial every 30 s which was set by the data acquisition system. Hence the first epoch in either direction represented trials occurring in the first 10 min of testing, middle epoch 10–20 min into testing and late epoch last 10 min of testing (20–30 min). Data for APA muscle activity, baseline muscle activity and peak acceleration were skewed left. To meet the assumption of normality, baseline muscle activity and peak acceleration data were transformed using the natural logarithm while APA muscle activity was transformed using the natural logarithm of the raw data +30 to account for negative values. 2.5. Statistical analysis Analyses were carried out on reaction time, focal muscle activity, APA muscle activity and baseline muscle activity using the Linear Mixed Models in SPSS (version 11.5) – repeated measures (seven subjects) over two sessions with a two tailed test of significance (a = 0.05). Peak acceleration of the arm was included as a covariate to control for the magnitude of the perturbation to posture.

3. Results 3.1. Static abdominal curl Examination of the change in median frequency during the static abdominal curls supports the expectation that the rectus abdominis was the most consistently fatigued muscle and the erector spinae was the least fatigued muscle (Fig. 2). 3.2. Arm raising In an analysis of pre-fatigue trials only, baseline muscle activity was not significantly different according to the

Fig. 2. Box plot of the median and interquartile range of change in median frequency (n = 7 subjects  2 sessions  2 curls) for rectus abdomini (RA), internal oblique (IO) and erector spinae (ES) (pooled bilaterally). Change in median frequency was the percentage change in median frequency (MF) from the initial MF ((final MF initial MF)/initial MF).

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direction of arm movement for rectus abdominis (F = 0.319, p = 0.573), erector spinae (F = 0.062, p = 0.804) or internal oblique (F = 0.060, p = 0.807) (Fig. 3). In contrast, APA muscle activity was significantly dependent on the direction of arm movement for the rectus abdominis (F = 363.432, p < 0.001), the erector spinae (F = 663.644, p < 0.001) and the internal oblique (F = 32.658, p < 0.001). The effect was larger in the erector spinae and rectus abdominis in comparison with the internal oblique (Fig. 3). The internal oblique demonstrated a greater relative proportion of baseline to APA muscle activity in comparison to the rectus abdominis or erector spinae (Fig. 3). The rectus abdominis was most active in the arm backwards movements whereas the erector spinae and internal oblique were most active during the arm forwards movement. Inhibition of erector spinae baseline muscle activity by APA activity was evident in 25–50% of arm forwards trials (Fig. 3). In subsequent analyses data for arm forwards and arm backwards movements were analyzed separately due to the confirmed directional dependence of APA muscle activity. Within pre-fatigue 1 (Fig. 1A), there was no significant difference between epochs (early, middle or late) for APA or baseline muscle activity in arm forwards or arm backwards movements (F < 1.877, p > 0.174). This finding suggests muscle activity was consistent within the pre-fatigue 1 period. There were no significant differences in muscle activity between pre-fatigue 1 (Fig. 1A) and pre-fatigue 2 (Fig. 1C) (F < 1.889, p > 0.183) for either baseline or APA muscle activity. Subsequent differences in APA and baseline muscle activity are thus likely to be associated with the fatiguing static abdominal curl and not the process of sitting and getting up quickly to begin the arm raising protocol. Subsequent analyses compared all pre-fatigue data with specific post-fatigue epochs.

R Fig. 3. Box plot of the median and interquartile range of EMG of each muscle (rectus abdominis, internal oblique and erector spinae) for baseline and APA activity in all subjects in all pre-fatigue trials during arm forwards (checked) and arm backwards (white) movements. Negative values indicate inhibition of the baseline muscle activity during the APA. Probabilities of significant difference between arm forwards and arm backwards movements are included.

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No significant difference before and immediately following abdominal fatigue (post-fatigue early—first 10 min) was observed for reaction time in arm forwards (F = 0.009, p = 0.923) and arm backwards (F = 0.791, p = 0.378) movements or for focal muscle activity of the anterior deltoid (F = 0.009, p = 0.923) or the posterior deltoid (F = 0.791, p = 0.378). These findings indicate that the activity of the focal muscle was not systematically altered by abdominal fatigue. Significant reductions in APA muscle activity immediately following abdominal fatigue (post-fatigue early—first 10 min) were observed in both the rectus abdominis in arm backwards movements (F = 5.440, p = 0.027) and the erector spinae in arm forwards movements (F = 5.379, p = 0.025). Median reductions in APA muscle activity were approximately 20% (Fig. 4A). No significant differences in APA muscle activity were observed in a parallel comparison of rectus abdominis in arm forwards (F = 0.246, p = 0.622), erector spinae in arm backwards (F = 1.699, p = 0.198) or internal oblique in arm forwards (F = 2.655, p = 0.109) or arm backwards (F = 1.914, p = 0.173) movements. The findings indicate that the fatigue effect was correlated with the directional activity of the muscles during the APA.

Fig. 4. Box plot of the median and interquartile range of (A) change in APA muscle activity (ma) following fatigue for the rectus abdominis in arm forwards movements and erector spinae in arm backwards movements and (B) change in baseline muscle activity following fatigue for the rectus abdominis, erector spinae and internal oblique (direction of movement pooled) for early (up to 10 min after curl up), middle (10–20 min after curl up) and late (20–30 min after curl up) epochs. Data for the first and second post-fatigue periods were pooled within epoch. Calculation of the change score was (((post-fatigue epoch score average of all pre-fatigue trials)/ average of all pre-fatigue trials)  100). *Significant difference from baseline at p < 0.05.

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No significant changes in baseline muscle activity in arm forwards or arm backwards movements immediately following abdominal fatigue (post-fatigue early—first 10 min) were observed in the rectus abdominis (F < 0.137, p > 0.713) or the erector spinae (F < 0.307, p > 0.582). Baseline muscle activity in the internal oblique was significantly altered immediately following abdominal fatigue (post-fatigue early—first 10 min) in both arm forwards (F = 6.306, p = 0.016) and arm backwards (F = 6.900, p = 0.011) movements. The changes both reflected a 30% increase in baseline muscle activity in the internal oblique (Fig. 4B). Fig. 5 demonstrates an example of changes in rectus abdominis and internal oblique signals before and after abdominal fatigue for one subject during two equivalent arm backwards movements.

APA activity in the rectus abdominis in arm backwards movements and the erector spinae in arm forwards were significantly different before and 20–30 min after abdominal fatigue (late epoch) (arm backwards; F = 4.547, p = 0.044, arm forwards; F = 6.682, p = 0.012) indicating that APA muscle activity in these muscles had not recovered to prefatigue levels during this time period (Fig. 4A). Recovery was more evident in the internal oblique baseline muscle activity which was not significantly different before and 20– 30 min after abdominal fatigue (late epoch) in both arm forwards and arm backwards movements (F = 0.012, p = 0.915; F = 0.003, p = 0.956) (Fig. 4B).

4. Discussion Consistent with previous reports, the present study demonstrated that APA muscle activity was dependent on the direction of movement of the arm [3,15]. The central nervous system is thought to inhibit or enhance muscle activity during APAs depending on the direction of the perturbation to posture [6,7]. Inhibition of antagonist activity is obvious when APA activity falls below evident baseline muscle activity and this occurred in a small number of trials in the erector spinae during arm backwards movements. Evidence of the APA as inhibitory has been reported previously [7]. In the present study, baseline muscle activity was not affected by the direction of arm movement in all the recorded postural muscles suggesting an equivalent trunk and lower limb posture during both arm forwards and arm backwards movements. 4.1. The effect of abdominal muscle fatigue

Fig. 5. Plots of arm acceleration and raw EMG signals of rectus abdominis (RA) and internal oblique (IO) immediately prior to arm backwards movements (rectus abdominis most active in this direction) taken from one subject: (A) a pre-fatigue trial (B) a post-fatigue trial. Peak accelerations of the arm for both trials were within 5%. The APA window is 100 ms before to 50 ms after the onset of the deltoid and is indicated. The scale for each trace type is equivalent between trials. Note the larger APA activity for RA prefatigue vs. post-fatigue and the larger baseline for IO post-fatigue.

During a fatiguing isometric contraction, physiological processes result in a decline in the median frequency of the power spectrum of the EMG signal. The rate of decline in median frequency through an isometric contraction has been extrapolated to reflect the magnitude of muscle fatigue [19– 21]. In our study, the rectus abdominis demonstrated the greatest and most systematic reduction in median frequency of the power spectrum of the EMG signal during the static abdominal curl compared to that of the internal oblique and especially the erector spinae muscles. This finding supports the expectation that the static abdominal curl induced the greatest peripheral fatigue effects in the rectus abdominis muscles and the least peripheral fatigue effects in the erector spinae. Our primary hypothesis, that abdominal muscle fatigue induced a change in muscle activity during APAs, was supported by the findings of the study. Following abdominal muscle fatigue there was a decrease in muscle activity during the APA window. This was consistent with the findings of Vuillerme et al. [13] who reported significant reductions in the integrated EMG of the ipsilateral semitendinosis following calf muscle fatigue. The force or torque a fatigued muscle can produce is less than a fresh

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muscle for the same level of activation [22]. If fatigue influenced APA muscle activity in a simple manner, then it might be expected that muscle activity during the APA would be increased post-fatigue to compensate for relative muscle weakness. The sustained reduction of muscle activity during the APA window lasting more than 20 min suggests that changes in muscle fibre conduction rate were not responsible since these should ameliorate within 10 min [23]. It is possible that a change in performance of the fatigued muscle existed even 20 min post-exercise independent of changes in fibre conduction [33] and it may be that perception of a change in perceived performance influenced the observed response in APAs. A subsidiary aim of the present study was to examine the directional nature of APAs and use this information to elucidate the central or peripheral nature of changes in muscle activity during the APA window associated with fatigue. The findings of our study indicated that fatigue of the anterior muscles of the trunk resulted in reductions in APA muscle activity of equivalent magnitude in both the anterior and posterior aspects of the trunk despite the difference in muscle state (the rectus abdomini were fatigued and the erector spinae were not). This finding supports earlier mentioned evidence that the alteration in APA muscle activity post-fatigue was a centrally mediated rather than peripherally mediated event. A reduction in the magnitude of trunk muscle activity during APAs has been described previously. Standing (with eyes open) closer to the limits of support, inclined standing or bending at the waist and balancing on an unstable board have been reported to result in smaller amplitudes of APA muscle activity in the rectus abdomini, erector spinae and lower limb muscles [6,7,10,11]. Reductions were greatest when the direction of instability and perturbation were aligned [6,16]. APA suppression has also been reported in conditions where there was a threat to posture but no actual instability [24]. One difficulty with interpretation of the findings of the latter study in relation to the present study is the lack of clear separation of the postural and focal task and the changing characteristics of the focal task with ‘‘fear’’. APAs are thought to arise out of the prediction and counteraction of the anticipated disturbing effects of movement [1,3,4]. In upper limb raising activities the APA may control intersegmental orientation rather than stabilising the centre of mass [15,26,27]. It has also been hypothesized that APAs contribute to movement initiation [28,29]. Aruin, Latash and colleagues have hypothesized that in some conditions of postural instability ‘‘the central nervous system may suppress APAs as a protection against their possible destabilising effects’’ [6]. In arm raising after abdominal muscle fatigue, suppression of APA muscle activity may occur to reduce excessive postural or intersegmental movement. The difference between the present study and previous studies of unstable standing is that abdominal fatigue is likely to influence perceptions of body state before influencing postural equilibrium. It is proposed that changes in body scheme [25] result in an altered perception of body state through an influence postural set [8] and that this results

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in a reduction in APA muscle activity in muscles important in dynamic trunk stability. A difficulty with the proposition that APA suppression is adaptive is that without a corresponding alternative adaptation following abdominal fatigue, the body would be vulnerable to the destabilising effects of the perturbation. The suppression of APA muscle activity in the present study did not extend to the internal oblique muscle. The internal oblique also demonstrated a larger ratio of baseline to APA activity and smaller directional specificity compared with the rectus abdominis. These findings suggest that the internal oblique may have a relatively smaller role during the APA compared with rectus abdominus which is consistent with the smaller potential for the development of a directional torque. Interestingly, increases in baseline muscle activity in the internal oblique muscle were observed post-fatigue. Post hoc examination of data for the right side indicated that increases in baseline activity were bilateral. Increases in baseline muscle activity post-fatigue have been reported previously in the trunk muscles after fatiguing isometric back extensions [17] and in the dorsal neck muscles after fatiguing isometric neck flexion [30]. Bilateral elevation of baseline muscle activity of the internal oblique may compensate for relative muscle weakness following fatigue through splinting of the trunk. Regarding the changes in baseline and APA muscle activity associated with the first 10 min following fatigue, it might be suggested that the increase in baseline oblique muscle activity was the compensation that counteracted the effect of APA suppression in the rectus abdominis and erector spinae. Perhaps a more conservative postural strategy was induced reducing dynamic responses and increasing postural stiffness following fatigue. Alternatively the increase in internal oblique activity may reflect central changes other than those induced by changes in motor control such as changes in respiration following fatigue [31]. Spinal stiffness and trunk muscle EMG have been reported to increase with respiration above and below tidal volume [32]. The increase in baseline muscle activity of the obliques may have increased trunk stiffness and altered postural set within the first 10 min after the fatiguing exercise. Subsequent changes in the APA may have followed this. Further research has been undertaken to clarify the effects of fatigue on tonic muscle activity in the internal obliques and the relationship between these changes, respiration and trunk segmental movement. The findings of this study provide insights into the control mechanisms underlying the trunk muscles APAs and open an avenue into the understanding of the changes observed in individuals with spinal pain syndromes.

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