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Journal of Back and Musculoskeletal Rehabilitation 27 (2014) 545–551 DOI 10.3233/BMR-140480 IOS Press
Normal postural responses preceding shoulder flexion: Co-activation or asymmetric activation of transverse abdominis? Sanaz Davariana, Nader Maroufib,∗ , Esmaeil Ebrahimib , Mohammad Parnianpourc,d and Farzam Farahmandc a
Faculty of Rehabilitation Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran Faculty of Rehabilitation, Iran University of Medical Sciences, Tehran, Iran c Department of Mechanical Engineering, Sharif University of Technology, Tehran, Iran d Information and Industrial Engineering, Hanyang University, Seoul, Korea b
Abstract. BACKGROUND AND OBJECTIVES: It is suggested that activation of the transverse abdominis muscle has a stabilizing effect on the lumbar spine by raising intra-abdominal pressure without added disc compression. However, its feedforward activity has remained a controversial issue. In addition, research regarding bilateral activation of trunk muscles during a unilateral arm movement is limited. The aim of this study was to evaluate bilateral anticipatory activity of trunk muscles during unilateral arm flexion. MATERIALS AND METHODS: Eighteen healthy subjects (aged 25 ± 3.96 years) participated in this study and performed 10 trials of rapid arm flexion in response to a visual stimulus. The electromyographic activity of the right anterior deltoid (AD) and bilateral trunk muscles including the transverse abdominis/internal oblique (TA/IO), superficial lumbar multifidus (SLM) and lumbar erector spine (LES) was recorded. The onset latency and anticipatory activity of the recorded trunk muscles were calculated. RESULTS: The first muscle activated in anticipation of the right arm flexion was the left TA/IO. The right TA/IO activated significantly later than all other trunk muscles (P < 0.0005). In addition, anticipatory activity of the right TA/IO was significantly lower than all other trunk muscles (P < 0.0005). There was no significant difference in either onset latency or anticipatory activity among other trunk muscles (P > 0.05). CONCLUSION: Healthy subjects showed no bilateral anticipatory co-activation of TA/IO in unilateral arm elevation. Further investigations are required to delineate normal muscle activation pattern in healthy subjects prior to prescribing bilateral activation training of transverse abdominis for subjects with chronic low back pain. Keywords: Anticipatory postural adjustments, motor control, low back, stability, self-induced perturbation
1. Introduction A motor action is composed of a focal and postural component [1–3]. The former refers to the body segments that are related to the goal of movement and ∗ Corresponding author: Nader Maroufi, Physical Therapy, Faculty of Rehabilitation, Iran University of Medical Sciences, Tehran, Iran. Tel.: +98 2122228051; E-mail: [email protected].
the latter refers to the other body segments [1–3]. Postural adjustments are those motor commands that are sent to the postural component and can precede (anticipatory postural adjustments (APAs)), accompany (synchronous postural adjustments (SPAs)) and follow (consecutive postural adjustments (CPAs)) the movement [3]. It is not a new finding that in upper limb tasks, the activity of trunk and leg muscles precedes the movement [4–8]. Some studies have shown that feedforward
c 2014 – IOS Press and the authors. All rights reserved ISSN 1053-8127/14/$27.50
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contraction of transverse abdominis (TA), unlike other superficial trunk muscles, is not direction-specific [7– 10]. However, recent studies have revealed that TA acts asymmetrically and its anticipatory activation is directionally specific [11,12]. Controversy regarding feedforward activation of TA is one of the concerns of the literature, in that bilateral contraction of this muscle has been suggested as the basis for an exercise called “abdominal hollowing” which is one of the main parts of core stabilization exercises [13]. In addition, majority of the research concerning feedforward muscle activation during rapid arm flexion in healthy subjects have recorded trunk muscles unilaterally [4,7–9]. Information regarding bilateral activation of trunk muscles during unilateral limb movement may help us better understand the strategies that the central nervous system (CNS) uses to encounter a specific self-induced perturbation. Allison et al. [11] and Morris et al. [12] recorded bilateral feedforward activation of TA; however, they used a small sample size of seven and six participants, respectively. In addition, in the study of Morris et al., 2 of 6 participants showed a large amount of co-contraction of TA and only 4 subjects demonstrated reciprocal activation of TA. Another study that evaluated abdominal and lumbar muscle activation pattern bilaterally was performed by Silfies et al. [14], but since they did not find any significant difference in onset latency between ipsilatelaral and contralateral rectus abdominis, lumbar multifidus and erector spine muscles, they collapsed the data of both sides for these muscle groups. We hypothesized that pure stability function of TA (an increase in intra-abdominal pressure) predicts similar TA response bilaterally, but a more complex function may induce bilateral differences. In order to test our hypothesis we required monitoring of TA activity from both sides. Therefore, the aim of this study was to evaluate normal feedforward activation pattern of trunk muscles bilaterally during unilateral arm flexion.
2. Methods 2.1. Participants Eighteen healthy volunteers (13 female and 5 male; with age, weight, height and Body Mass Index (BMI) of 25 ± 3.96 years, 54 ± 7.81 Kg, 165 ± 8.78 cm and 20 ± 2.04 Kg/m2 , respectively) participated in this study after signing the informed consent. The exclusion criteria were spinal surgery/fracture/trauma,
major spinal deformity, lumbar disc herniation, pregnancy, cardio-vasculo-pulmonary diseases, vertigo and vestibular system disorders. In addition, all women were asked to participate when they were not menstruating. The study was approved by Tehran University of Medical Sciences ethics committee. 2.2. Testing protocol All participants were asked to stand in a relaxed position while their feet were 50% of shoulder’s width apart. The task was rapid unilateral shoulder flexion of the right upper limb up to approximately 90 degrees in response to a “green” visual stimulus. A rope which was horizontally attached to two vertical wooden bars was adjusted to the shoulder level for each subject to show the target shoulder flexion angle. It was placed in front of the subjects, 20 centimeters farther from their outstretched hand at 90 degrees of shoulder flexion in order for the task not to be interrupted by the rope. To decrease the predictability of movement, a “red” visual stimulus was designed and all participants were asked to avoid performing any movement whenever they saw the red light. The visual stimulus – whether the green or the red light – followed a verbal warning by 2–3.5 s in a random fashion. All subjects became familiarized with the task, verbal warning and visual stimuli prior to the testing phase. The order of appearance of green or red visual stimulus was randomized using a pre-designed 15repetition table. Therefore, each subject faced 15 random repetitions of visual stimuli with a 10-second rest between each trial; and 10 repetitions of rapid arm flexion in response to the green light were recorded for further analyses. 2.3. Instrumentation The electromyographic (EMG) activity of the right anterior deltoid (AD) and bilateral trunk muscles including transverse abdominis/internal oblique (TA/IO), superficial lumbar multifidus (SLM) and lumbar erector spine (LES) were recorded using bipolar surface electrodes (Biometrics Data Link, UK) with diameter and centre-to-centre distance of 10 mm and 20 mm, respectively. In order to eliminate the effect of intersubject variability on electrode placement, all the procedures of proper skin preparation, detecting bony landmarks and electrode placement were performed by one pre-trained examiner throughout the study. The electrodes were placed over the following sites; 2 cm
S. Davarian et al. / Normal postural responses preceding shoulder flexion
Fig. 1. Electrode placement for the recorded trunk muscles. TA/IO: transverse abdominis/internal oblique; SLM: superficial lumbar multifidus; LES: lumbar erector spine.
anterior and inferior to the right acromion for the right AD (15), 2 cm medial and inferior to the Anterior Superior Iliac Spine (ASIS) for the TA/IO (4), parallel to a line connecting the Posterior Superior Iliac Spine (PSIS) and L1-L2 interspinous space at the level of L5 for the SLM [16], and 3 cm lateral to the spinal process of L3 for the LES [17,18]. Figure 1 depicts the sites of electrode placement for the recorded trunk muscles. EMG signals were band-pass filtered between 20 and 450 Hz and sampled at 1000 Hz. An accelerometer (Biometrics, ACL300, UK) was attached to the dorsal aspect of the right wrist between the distal end of the radius and ulna and a goniometer (Biometrics, SG, UK) was placed over the right shoulder joint in order to record the acceleration of arm movement during the familiarization and testing phases. The data was sampled at 1000 Hz for the accelerometer and 50 Hz for the goniometer. 2.4. Reliability procedure
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Works, MA, USA). The onset of the EMG signal was detected using a combination of an algorithm (Approximated Generalized Likelihood Ratio (AGLR)) [19– 21] and visual inspection by a pre-trained examiner. The onset latency of the recorded muscles was defined as the time between the onset of each trunk muscle and the onset of the right AD. The period between 100 ms before and 50 ms after the onset of the right AD was considered to determine anticipatory postural adjustments of the recorded trunk muscles [6,18,22,23]. For calculating anticipatory EMG activity, all signals were full-wave rectified. Then, the EMG integral of the rectified signal was calculated for an individual trunk muscle during 100 ms before to 50 ms after the onset of the right AD (anticipatory period) as well as 500 to 450 ms before the onset of the right AD (background period). The anticipatory integrated EMG activity (IEMG) of each muscle in one trial was calculated using the following formula [6,24–26]: +50 |EMGij (t)|dt IEMGij = −100
−3
−450
−500
|EMGij (t)|dt
Where i and j represent ith muscle and j th trial, respectively. According to the previous studies, the anticipatory IEMG of a specific muscle in each trial, then, was normalized to the maximum absolute anticipatory IEMG across all 10 trials for that particular muscle [6,25,26]. IEMGnorm ij = IEMGij / max(|IEMGi1 |, |IEMGi2 |, . . . , |IEMGij |, |IEMGi10 |) j = 1, . . . , 10
Intrasession reliability of dependent variables including the onset latency and anticipatory activity of trunk muscles was calculated in all subjects. In addition, 10 participants were selected randomly for assessing intersession reliability of these variables.
Therefore, the range of anticipatory IEMG indices limited from −1 to +1; negative values indicated inhibition of muscle activation and positive values showed anticipatory activation [6,25,26].
2.5. Data analysis
2.6. Statistical analysis
The reaction time of arm elevation was defined as the time between the instant of green light occurrence and the onset of the right AD. When the reaction time was below 100 ms, the data of that trial was removed from further analyses due to the assumption that subject had initiated arm movement prior to observation of the stimulus. The onset and magnitude of muscle activation were calculated using MATLAB (version 7.10.0; Math-
In order to assess the relative and absolute reliability of the onset latency and anticipatory activity of the trunk muscles, the Intraclass Correlation Coefficient (ICC) and Standard Error of Measurement (SEM) were computed, respectively. The strength of ICCs was interpreted according to Munro’s classification [27]; an ICC value ranging between 0 and 0.25 indicates “little” correlation, 0.26 and 0.49 indicates “low” correlation, 0.50 and 0.69 indicates “moderate” correla-
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Fig. 2. Order of activation of trunk muscles during unilateral arm flexion. TA/IO: transverse abdominis/internal oblique; SLM: superficial lumbar multifidus; LES: lumbar erector spine; Vertical dashed line indicates the onset of the right anterior deltoid.; ∗ indicates significant difference (P < 0.0005) between the right TA/IO and other muscles.
tion, 0.70 and 0.89 indicates “high” correlation, and 0.90 and 1 indicates “very high” correlation. A Kolmogorov Smirnov (K-S) test was used to determine normal distribution of each variable. A repeated measures ANOVA with post hoc comparisons using Bonferroni test was performed to detect whether there was any difference in onset latency or anticipatory activity among trunk muscles.
Fig. 3. Anticipatory activity of trunk muscles during unilateral arm flexion. TA/IO: transverse abdominis/internal oblique; SLM: superficial lumbar multifidus; LES: lumbar erector spine; ∗ indicates significant difference (P < 0.0005) between the right TA/IO and other muscles.
tivariate partial eta squared = 0.96). Post hoc comparisons using the Bonferroni test showed that the right TA/IO activated significantly later than all other trunk muscles (P < 0.0005). In addition, the left TA/IO was the first muscle activated, although there was not any significant difference in onset latency between left TA/IO and other trunk muscles (P > 0.05) except for the right TA/IO (P < 0.0005). Figure 2 depicts the order of activation of the recorded trunk muscles during arm flexion. 3.3. Anticipatory activity
3. Results The K-S test was not significant for any of the variables (P > 0.05), showing normal distribution for all variables. 3.1. Reliability Intra-session reliability of onset latency and anticipatory activity for individual muscles ranged from 0.83 to 0.94 and 0.59 to 0.91, respectively. Inter-session reliability ranged from 0.86 to 0.97 for muscle onset latency and 0.64 to 0.84 for anticipatory activity. ICC and SEM of dependent variables for individual muscles have been shown in Table 1. 3.2. Onset latency There was a significant effect for muscle (Wilks’ Lambda = 0.04, F (5, 13) = 56.75, P < 0.0005, mul-
There was a significant effect for muscle (Wilks’ Lambda = 0.14, F (5, 13) = 15.88, P < 0.0005, multivariate partial eta squared = 0.86). Post hoc comparisons using the Bonferroni test showed that anticipatory activity of the right TA/IO was significantly lower than all other trunk muscles (P < 0.0005). There was no significant difference among other trunk muscles (P > 0.05). Figure 3 represents the anticipatory activity of the recorded trunk muscles during arm flexion.
4. Discussion 4.1. Reliability According to Munro’s classification [27], the onset latency demonstrated high to very high and the anticipatory activity showed moderate to very high intra- and inter-session reliability (Table 1). High intrasession ICC values of onset latency can show that the method
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Table 1 Intra-session and inter-session reliability of onset latency and anticipatory activity of individual muscles Variable Onset latency
Muscle
Intra-session reliability ICC SEM∗
Inter-session reliability ICC SEM∗
Right TA/IO§ Left TA/IO Right SLM† Left SLM Right LES‡ Left LES
0.94 0.83 0.93 0.88 0.94 0.90
14.47 18.79 14.90 15.01 12.48 11.74
0.86 0.93 0.97 0.90 0.97 0.95
10.87 6.87 6.05 6.55 4.90 3.90
Right TA/IO Left TA/IO Right SLM Left SLM Right LES Left LES
0.91 0.65 0.79 0.75 0.59 0.65
0.34 0.19 0.24 0.21 0.26 0.12
0.84 0.64 0.73 0.82 0.69 0.70
0.23 0.06 0.09 0.05 0.06 0.05
Anticipatory activity
∗ The
unit of measurement for SEM of onset latency is ms. There is no unit of measurement for SEM of anticipatory activity, since it is a normalized value. § transverse abdominis/internal oblique; † superficial lumbar multifidus; ‡ lumbar erector spine.
of onset detection used in this study (which was a combination of AGLR algorithm and visual inspection by a pre-trained examiner) was a reliable technique. Moreover, a pre-trained examiner took all the measures of skin preparation, detecting bony landmarks and electrode placement in two subsequent days which resulted in high inter-session reliability of the dependent variables. The number of trials used for data analysis is another important factor related to relative reliability. Increasing the number of trials enhances relative reliability of a specific outcome measure [28,29]. This fact is more critical when the outcome measure of a survey is obtained from an inherently variable data such as EMG signal. In addition, moderate reliability of anticipatory activity may be due to the method of normalization used in this study. However, we did not have any comparison of different normalization techniques. The second explanation may result from the rationale that muscle activity is dependent on temporal and spatial summation of motor units; therefore, variation in the recruitment of motor units in different trials may increase variability of response and, consequently, reduce reliability. 4.2. Feedforward activation of TA/IO In the present study, the contralateral TA/IO was the first muscle activated in anticipation of unilateral arm flexion which is in accordance with previous reports [7,8,30]. The ipsilateral TA/IO activated later than all other trunk muscles and even the prime mover (AD) which is also consistent with previous reports regarding feedforward activation of TA [4,11,14].
Furthermore, the ipsilateral TA/IO showed significant lower anticipatory activity compared to the contralateral TA/IO which is in agreement with the study of Allison et al. that evaluated this muscle bilaterally [11]. Although studying feedforward activation of TA is not a new topic, the direction-specificity of this muscle is one of the challenges among researchers. Hodges et al. carried out several studies in which feedforward activity of trunk muscles contralateral to the side of perturbation was evaluated during unilateral arm movements in different directions and demonstrated that contralateral TA precedes other trunk muscles regardless of the direction of movement [7,8,30]. They interpreted that activation of TA, unlike other superficial trunk muscles, is not direction-specific [7,8,30]. In contrast, Allison et al. [11] and Morris et al. [12] interpreted that TA acts asymmetrically and its anticipatory activation is directionally specific. The results of our study revealed that during anticipatory period of unilateral arm flexion, ipsilateral TA/IO activated later with lower magnitude than contralateral TA/IO, showing bilateral asymmetry in anticipatory activation of TA, which were similar to the findings of Allison et al. and Morris et al. [11,12]. Asymmetry in onset latency and anticipatory activity of TA/IO shows that the purpose of the activation of this muscle may not be a pure stability function by increasing the intra-abdominal pressure, but may be a more complex function. Morris et al. [12] proposed a new theoretical model for feedforward activation of TA and stated that this muscle acts as part of a synergy of muscles to counteract the rotary torques. Previous findings have shown that during left arm flexion, a flexion [7], left lateral flexion [7] and
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anticlockwise rotation [7,12] torque is imposed on the trunk. According to the findings of our study and previous research [7,8,11,12,30], it is obvious that the inconsistency regarding normal feedforward control of TA is not due to the discrepancies in the findings of different studies, but as Allison et al. [11] have mentioned, results from various interpretations. The human body specifically the trunk region has a complex nature with a great amount of redundancy at muscles [31]. Therefore, multiple muscles perform a similar function. Meanwhile, an individual muscle may have multiple actions in a complex system. Therefore, although TA may provide segmental control of the spine via increasing intra-abdominal pressure, it also acts as part of a muscle synergy [12] to counterbalance the anticipatory rotary torques. In addition, based upon previous studies concerning non-direction specific activation of TA in anticipation of any unilateral arm movement [7,8,30] as well as in vivo animal findings that showed bilateral activation of TA was very important in spinal segmental control [32], an exercise called “abdominal hollowing” was created and prescribed for patients who suffer from chronic low back pain (CLBP) or athletes and healthy individuals who are vulnerable to back pain [13]. The point is that these research evaluated trunk muscles on the contralateral side of the arm movement. However, our study showed that TA/IO did not co-activate bilaterally in anticipation of a unilateral task such as right shoulder flexion which is in accordance with previous reports [11,12]. Therefore, prescription of abdominal hollowing prior to limb movements for CLBP patients may be under question and it seems that prior to establishing a treatment technique, further studies are required to detect normal muscle activation pattern. 4.3. Feedforward activation of SLM and LES Posterior trunk muscles activated before the prime mover (right AD), significantly sooner with higher anticipatory activity than right TA/IO. However, they did not show any bilateral difference in onset latency or anticipatory activity. Anticipatory activity of LES and SLM in shoulder forward flexion has been reported in previous studies [7–9,14]. Activation of posterior trunk muscles prior to the prime mover in shoulder forward flexion is aimed at controlling perturbation produced by the movement. Hodges et al. [7] evaluated preparatory
trunk motion along with EMG recording of trunk muscles (including abdominal muscles and LES) in upper limb movements and showed that in upper limb flexion, activation of LES preceded the preparatory trunk extension. Anticipatory activity of these muscles may produce a secondary perturbation which should be controlled by other postural muscles. Unwanted accompanying torques from activated agonist muscles should be counterbalanced efficiently by activation of proper synergists to provide optimum postural stability. In addition, lack of bilateral difference in SLM and LES muscular response means that rotary perturbation of unilateral arm flexion may not elicit additional activity of these muscle groups. One limitation of our study was that we were not able to record TA using fine-wire electrodes. Surface EMG did not show the pure activity of TA because of an overlap between this muscle and the internal oblique in lower abdominal region. The electrode placement for TA/IO in this study was according to the survey of Marshal and Murphy [4] which showed that surface EMG can replicate intramuscular recordings for this muscle. Nevertheless, we cannot conclude that the observed muscle activation is solely due to TA. However, intramuscular EMG recording has also its own limitation which is the pick-up area of fine wire is much smaller that cannot be a representative of the whole muscle [12]. The second limitation of our study was that we could not assess kinematic variables along with kinetic data. Finally, it was not possible to record multiple muscles synchronously due to limited channels of the EMG device.
5. Conclusion Healthy subjects did not show bilateral anticipatory co-activation of TA/IO in unilateral arm elevation. This finding is of high importance since therapeutic exercises for CLBP patients are focusing on bilateral activation of TA. There is a need to perform further research to evaluate normal muscle activation pattern in healthy subjects. Furthermore, anticipatory activity of posterior trunk muscles is important to control the perturbation of arm flexion.
Acknowledgement This research was financially supported by Tehran University of Medical Sciences.
S. Davarian et al. / Normal postural responses preceding shoulder flexion
Conflict of interest
[16]
The authors declare no conflict of interest. [17]
References [1]
[2]
[3] [4]
[5]
[6]
[7]
[8]
[9]
[10]
[11]
[12]
[13]
[14]
[15]
Yiou E, Hamaoui A, Bozec SL. Influence of base of support size on arm pointing performance and associated anticipatory postural adjustments. Neuroscience Letters 2007; 423: 29-34. Nana-Ibrahim S, Vieilledent S, Leroyer P, Viale F, Zattara M. Target size modifies anticipatory postural adjustments and subsequent elementary arm pointing. Experimental Brain Research 2008; 184: 255-60. Bouisset S, Do MC. Posture, dynamic stability, and voluntary movement. Clinical Neurophysiology 2008; 38: 345-62. Marshall P, Murphy B. The validity and reliability of surface EMG to assess the neuromuscular response of the abdominal muscles to rapid limb movement. Journal of Electromyography and Kinesiology 2003; 13(5): 477-89. Allison GT, Henry SM. The influence of fatigue on trunk muscle responses to sudden arm movements, a pilot study. Clinical Biomechanics 2002; 17: 414-7. Kanekar N, Santos MJ, Aruin AS. Anticipatory postural control following fatigue of postural and focal muscles. Clinical Neurophysiology 2008; 119: 2304-13. Hodges P, Cresswell A, Daggfeldt K, Thorstensson A. Three dimensional preparatory trunk motion precedes asymmetrical upper limb movement. Gait and Posture 2000; 11(2): 92-101. Hodges P, Richardson C. Feedforward contraction of transversus abdominis is not influenced by the direction of arm movement. Experimental Brain Research 1997; 114(2): 362-70. Hodges P, Cresswell A, Thorstensson A. Preparatory trunk motion accompanies rapid upper limb movement. Experimental Brain Research 1999; 124(1): 69-79. Crommert ME, Ekblom MM, Thorstensson A. Activation of transversus abdominis varies with postural demand in standing. Gait and Posture 2011; 33: 473-7. Allison GT, Morris SL, Lay B. Feedforward responses of transversus abdominis are directionally specific and act asymmetrically: implications for core stability theories. Journal of Orthopaedic and Sports Physical Therapy 2008; 38(5): 22837. Morris SL, Lay B, Allison GT. Corset hypothesis rebutted – Transversus abdominis does not co-contract in unison prior to rapid arm movements. Clinical Biomechanics 2012; 27(3): 249-54. Richardson C, Hodges P, Hides J. Therapeutic exercise for lumbopelvic stabilization. A motor control approach for the treatment and prevention of low back pain. London: Churchill Livingstone, 2004. Silfies SP, Mehta R, Smith SS, Karduna AR. Differences in feedforward trunk muscle activity in subgroups of patients with mechanical low back pain. Archives of Physical Medicine and Rehabilitation 2009; 90(7): 1159-69. Sjödahl J, Kvist J, Gutke A, Öberg B. The postural response of the pelvic floor muscles during limb movements: A methodological electromyography study in parous women without lumbopelvic pain. Clinical Biomechanics 2009; 24(2): 183-9.
[18]
[19]
[20]
[21]
[22]
[23]
[24]
[25]
[26]
[27] [28]
[29]
[30]
[31]
[32]
551
O’Sullivan P, Dankaerts W, Burnett A, Farrell G, Jefford E, Naylor C, et al. Effect of different upright sitting postures on spinal-pelvic curvature and trunk muscle activation in a painfree population. Spine 2006; 31(19): E707-E12. Grenier SG, McGill S. Quantification of lumbar stability by using 2 different abdominal activation strategies. Archives of Physical Medicine and Rehabilitation 2007; 88: 54-62. Morris SL, Allison GT. Effects of abdominal muscle fatigue on anticipatory postural adjustments associated with arm raising. Gait and Posture 2006; 24: 342-8. Staude G, Flachenecker C, Daumer M, Wolf W. Onset detection in surface electromyographic signals: A systematic comparison of methods. Journal on Applied Signal Processing 2001; 2(1): 67-81. Staude G, Kafka V, Wolf W. Determination of premotor silent periods from surface myoelectric signals. Biomedical Techniques 2000; 45(2): 228-32. Staude G, Wolf W. Objective motor response onset detection in surface myoelectric signals. Medical Engineering and Physics 1999; 21(6-7): 449-67. Hodges PW, Richardson CA. Altered trunk muscle recruitment in people with low back pain with upper limb movement at different speeds. Archives of Physical Medicine and Rehabilitation 1999; 80: 1005-12. Strang AJ, Berg WP. Fatigue-induced adaptive changes of anticipatory postural adjustments. Experimental Brain Research 2007; 178: 49-61. Santos MJ, Kanekar N, Aruin AS. The role of anticipatory postural adjustments in compensatory control of posture: 1. Electromyographic analysis. Journal of Electromyography and Kinesiology 2010; 20(3): 388-97. Li X, Aruin AS. The effect of short-term changes in body mass distribution on feed-forward postural control. Journal of Electromyography and Kinesiology 2009; 19(5): 931-41. Li X, Aruin AS. The effect of short-term changes in the body mass on anticipatory postural adjustments. Experimental Brain Research 2007; 181(2): 333-46. Domholdt E. Rehabilitation research: principles and applications. 3rd ed. Philadelphia: Elsevier Saunders, 2005. Pinsault N, Vuillerme N. Test-retest reliability of centre of foot pressure measures to assess postural control during unperturbed stance. Medical Engineering & Physics 2009; 31(2): 276-86. Monaghan K, Delahunt E, Caulfield B. Increasing the number of gait trial recordings maximises intra-rater reliability of the CODA motion analysis system. Gait & Posture 2007; 25(2): 303-15. Hodges PW, Richardson CA. Transversus abdominis and the superficial abdominal muscles are controlled independently in a postural task. Neuroscience Letters 1999; 265(2): 91-4. Hodges PW. Pain and motor control: from the laboratory to rehabilitation. Journal of Electromyography and Kinesiology 2011; 21(2): 220-8. Hodges P, Kaigle Holm A, Holm S, Ekström L, Cresswell A, Hansson T, et al. Intervertebral stiffness of the spine is increased by evoked contraction of transversus abdominis and the diaphragm: In vivo porcine studies. Spine 2003; 28(23): 2594-601.
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Journal of Back and Musculoskeletal Rehabilitation 27 (2014) 545–551 DOI 10.3233/BMR-140480 IOS Press
Normal postural responses preceding shoulder flexion: Co-activation or asymmetric activation of transverse abdominis? Sanaz Davariana, Nader Maroufib,∗ , Esmaeil Ebrahimib , Mohammad Parnianpourc,d and Farzam Farahmandc a
Faculty of Rehabilitation Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran Faculty of Rehabilitation, Iran University of Medical Sciences, Tehran, Iran c Department of Mechanical Engineering, Sharif University of Technology, Tehran, Iran d Information and Industrial Engineering, Hanyang University, Seoul, Korea b
Abstract. BACKGROUND AND OBJECTIVES: It is suggested that activation of the transverse abdominis muscle has a stabilizing effect on the lumbar spine by raising intra-abdominal pressure without added disc compression. However, its feedforward activity has remained a controversial issue. In addition, research regarding bilateral activation of trunk muscles during a unilateral arm movement is limited. The aim of this study was to evaluate bilateral anticipatory activity of trunk muscles during unilateral arm flexion. MATERIALS AND METHODS: Eighteen healthy subjects (aged 25 ± 3.96 years) participated in this study and performed 10 trials of rapid arm flexion in response to a visual stimulus. The electromyographic activity of the right anterior deltoid (AD) and bilateral trunk muscles including the transverse abdominis/internal oblique (TA/IO), superficial lumbar multifidus (SLM) and lumbar erector spine (LES) was recorded. The onset latency and anticipatory activity of the recorded trunk muscles were calculated. RESULTS: The first muscle activated in anticipation of the right arm flexion was the left TA/IO. The right TA/IO activated significantly later than all other trunk muscles (P < 0.0005). In addition, anticipatory activity of the right TA/IO was significantly lower than all other trunk muscles (P < 0.0005). There was no significant difference in either onset latency or anticipatory activity among other trunk muscles (P > 0.05). CONCLUSION: Healthy subjects showed no bilateral anticipatory co-activation of TA/IO in unilateral arm elevation. Further investigations are required to delineate normal muscle activation pattern in healthy subjects prior to prescribing bilateral activation training of transverse abdominis for subjects with chronic low back pain. Keywords: Anticipatory postural adjustments, motor control, low back, stability, self-induced perturbation
1. Introduction A motor action is composed of a focal and postural component [1–3]. The former refers to the body segments that are related to the goal of movement and ∗ Corresponding author: Nader Maroufi, Physical Therapy, Faculty of Rehabilitation, Iran University of Medical Sciences, Tehran, Iran. Tel.: +98 2122228051; E-mail: [email protected].
the latter refers to the other body segments [1–3]. Postural adjustments are those motor commands that are sent to the postural component and can precede (anticipatory postural adjustments (APAs)), accompany (synchronous postural adjustments (SPAs)) and follow (consecutive postural adjustments (CPAs)) the movement [3]. It is not a new finding that in upper limb tasks, the activity of trunk and leg muscles precedes the movement [4–8]. Some studies have shown that feedforward
c 2014 – IOS Press and the authors. All rights reserved ISSN 1053-8127/14/$27.50
546
S. Davarian et al. / Normal postural responses preceding shoulder flexion
contraction of transverse abdominis (TA), unlike other superficial trunk muscles, is not direction-specific [7– 10]. However, recent studies have revealed that TA acts asymmetrically and its anticipatory activation is directionally specific [11,12]. Controversy regarding feedforward activation of TA is one of the concerns of the literature, in that bilateral contraction of this muscle has been suggested as the basis for an exercise called “abdominal hollowing” which is one of the main parts of core stabilization exercises [13]. In addition, majority of the research concerning feedforward muscle activation during rapid arm flexion in healthy subjects have recorded trunk muscles unilaterally [4,7–9]. Information regarding bilateral activation of trunk muscles during unilateral limb movement may help us better understand the strategies that the central nervous system (CNS) uses to encounter a specific self-induced perturbation. Allison et al. [11] and Morris et al. [12] recorded bilateral feedforward activation of TA; however, they used a small sample size of seven and six participants, respectively. In addition, in the study of Morris et al., 2 of 6 participants showed a large amount of co-contraction of TA and only 4 subjects demonstrated reciprocal activation of TA. Another study that evaluated abdominal and lumbar muscle activation pattern bilaterally was performed by Silfies et al. [14], but since they did not find any significant difference in onset latency between ipsilatelaral and contralateral rectus abdominis, lumbar multifidus and erector spine muscles, they collapsed the data of both sides for these muscle groups. We hypothesized that pure stability function of TA (an increase in intra-abdominal pressure) predicts similar TA response bilaterally, but a more complex function may induce bilateral differences. In order to test our hypothesis we required monitoring of TA activity from both sides. Therefore, the aim of this study was to evaluate normal feedforward activation pattern of trunk muscles bilaterally during unilateral arm flexion.
2. Methods 2.1. Participants Eighteen healthy volunteers (13 female and 5 male; with age, weight, height and Body Mass Index (BMI) of 25 ± 3.96 years, 54 ± 7.81 Kg, 165 ± 8.78 cm and 20 ± 2.04 Kg/m2 , respectively) participated in this study after signing the informed consent. The exclusion criteria were spinal surgery/fracture/trauma,
major spinal deformity, lumbar disc herniation, pregnancy, cardio-vasculo-pulmonary diseases, vertigo and vestibular system disorders. In addition, all women were asked to participate when they were not menstruating. The study was approved by Tehran University of Medical Sciences ethics committee. 2.2. Testing protocol All participants were asked to stand in a relaxed position while their feet were 50% of shoulder’s width apart. The task was rapid unilateral shoulder flexion of the right upper limb up to approximately 90 degrees in response to a “green” visual stimulus. A rope which was horizontally attached to two vertical wooden bars was adjusted to the shoulder level for each subject to show the target shoulder flexion angle. It was placed in front of the subjects, 20 centimeters farther from their outstretched hand at 90 degrees of shoulder flexion in order for the task not to be interrupted by the rope. To decrease the predictability of movement, a “red” visual stimulus was designed and all participants were asked to avoid performing any movement whenever they saw the red light. The visual stimulus – whether the green or the red light – followed a verbal warning by 2–3.5 s in a random fashion. All subjects became familiarized with the task, verbal warning and visual stimuli prior to the testing phase. The order of appearance of green or red visual stimulus was randomized using a pre-designed 15repetition table. Therefore, each subject faced 15 random repetitions of visual stimuli with a 10-second rest between each trial; and 10 repetitions of rapid arm flexion in response to the green light were recorded for further analyses. 2.3. Instrumentation The electromyographic (EMG) activity of the right anterior deltoid (AD) and bilateral trunk muscles including transverse abdominis/internal oblique (TA/IO), superficial lumbar multifidus (SLM) and lumbar erector spine (LES) were recorded using bipolar surface electrodes (Biometrics Data Link, UK) with diameter and centre-to-centre distance of 10 mm and 20 mm, respectively. In order to eliminate the effect of intersubject variability on electrode placement, all the procedures of proper skin preparation, detecting bony landmarks and electrode placement were performed by one pre-trained examiner throughout the study. The electrodes were placed over the following sites; 2 cm
S. Davarian et al. / Normal postural responses preceding shoulder flexion
Fig. 1. Electrode placement for the recorded trunk muscles. TA/IO: transverse abdominis/internal oblique; SLM: superficial lumbar multifidus; LES: lumbar erector spine.
anterior and inferior to the right acromion for the right AD (15), 2 cm medial and inferior to the Anterior Superior Iliac Spine (ASIS) for the TA/IO (4), parallel to a line connecting the Posterior Superior Iliac Spine (PSIS) and L1-L2 interspinous space at the level of L5 for the SLM [16], and 3 cm lateral to the spinal process of L3 for the LES [17,18]. Figure 1 depicts the sites of electrode placement for the recorded trunk muscles. EMG signals were band-pass filtered between 20 and 450 Hz and sampled at 1000 Hz. An accelerometer (Biometrics, ACL300, UK) was attached to the dorsal aspect of the right wrist between the distal end of the radius and ulna and a goniometer (Biometrics, SG, UK) was placed over the right shoulder joint in order to record the acceleration of arm movement during the familiarization and testing phases. The data was sampled at 1000 Hz for the accelerometer and 50 Hz for the goniometer. 2.4. Reliability procedure
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Works, MA, USA). The onset of the EMG signal was detected using a combination of an algorithm (Approximated Generalized Likelihood Ratio (AGLR)) [19– 21] and visual inspection by a pre-trained examiner. The onset latency of the recorded muscles was defined as the time between the onset of each trunk muscle and the onset of the right AD. The period between 100 ms before and 50 ms after the onset of the right AD was considered to determine anticipatory postural adjustments of the recorded trunk muscles [6,18,22,23]. For calculating anticipatory EMG activity, all signals were full-wave rectified. Then, the EMG integral of the rectified signal was calculated for an individual trunk muscle during 100 ms before to 50 ms after the onset of the right AD (anticipatory period) as well as 500 to 450 ms before the onset of the right AD (background period). The anticipatory integrated EMG activity (IEMG) of each muscle in one trial was calculated using the following formula [6,24–26]: +50 |EMGij (t)|dt IEMGij = −100
−3
−450
−500
|EMGij (t)|dt
Where i and j represent ith muscle and j th trial, respectively. According to the previous studies, the anticipatory IEMG of a specific muscle in each trial, then, was normalized to the maximum absolute anticipatory IEMG across all 10 trials for that particular muscle [6,25,26]. IEMGnorm ij = IEMGij / max(|IEMGi1 |, |IEMGi2 |, . . . , |IEMGij |, |IEMGi10 |) j = 1, . . . , 10
Intrasession reliability of dependent variables including the onset latency and anticipatory activity of trunk muscles was calculated in all subjects. In addition, 10 participants were selected randomly for assessing intersession reliability of these variables.
Therefore, the range of anticipatory IEMG indices limited from −1 to +1; negative values indicated inhibition of muscle activation and positive values showed anticipatory activation [6,25,26].
2.5. Data analysis
2.6. Statistical analysis
The reaction time of arm elevation was defined as the time between the instant of green light occurrence and the onset of the right AD. When the reaction time was below 100 ms, the data of that trial was removed from further analyses due to the assumption that subject had initiated arm movement prior to observation of the stimulus. The onset and magnitude of muscle activation were calculated using MATLAB (version 7.10.0; Math-
In order to assess the relative and absolute reliability of the onset latency and anticipatory activity of the trunk muscles, the Intraclass Correlation Coefficient (ICC) and Standard Error of Measurement (SEM) were computed, respectively. The strength of ICCs was interpreted according to Munro’s classification [27]; an ICC value ranging between 0 and 0.25 indicates “little” correlation, 0.26 and 0.49 indicates “low” correlation, 0.50 and 0.69 indicates “moderate” correla-
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Fig. 2. Order of activation of trunk muscles during unilateral arm flexion. TA/IO: transverse abdominis/internal oblique; SLM: superficial lumbar multifidus; LES: lumbar erector spine; Vertical dashed line indicates the onset of the right anterior deltoid.; ∗ indicates significant difference (P < 0.0005) between the right TA/IO and other muscles.
tion, 0.70 and 0.89 indicates “high” correlation, and 0.90 and 1 indicates “very high” correlation. A Kolmogorov Smirnov (K-S) test was used to determine normal distribution of each variable. A repeated measures ANOVA with post hoc comparisons using Bonferroni test was performed to detect whether there was any difference in onset latency or anticipatory activity among trunk muscles.
Fig. 3. Anticipatory activity of trunk muscles during unilateral arm flexion. TA/IO: transverse abdominis/internal oblique; SLM: superficial lumbar multifidus; LES: lumbar erector spine; ∗ indicates significant difference (P < 0.0005) between the right TA/IO and other muscles.
tivariate partial eta squared = 0.96). Post hoc comparisons using the Bonferroni test showed that the right TA/IO activated significantly later than all other trunk muscles (P < 0.0005). In addition, the left TA/IO was the first muscle activated, although there was not any significant difference in onset latency between left TA/IO and other trunk muscles (P > 0.05) except for the right TA/IO (P < 0.0005). Figure 2 depicts the order of activation of the recorded trunk muscles during arm flexion. 3.3. Anticipatory activity
3. Results The K-S test was not significant for any of the variables (P > 0.05), showing normal distribution for all variables. 3.1. Reliability Intra-session reliability of onset latency and anticipatory activity for individual muscles ranged from 0.83 to 0.94 and 0.59 to 0.91, respectively. Inter-session reliability ranged from 0.86 to 0.97 for muscle onset latency and 0.64 to 0.84 for anticipatory activity. ICC and SEM of dependent variables for individual muscles have been shown in Table 1. 3.2. Onset latency There was a significant effect for muscle (Wilks’ Lambda = 0.04, F (5, 13) = 56.75, P < 0.0005, mul-
There was a significant effect for muscle (Wilks’ Lambda = 0.14, F (5, 13) = 15.88, P < 0.0005, multivariate partial eta squared = 0.86). Post hoc comparisons using the Bonferroni test showed that anticipatory activity of the right TA/IO was significantly lower than all other trunk muscles (P < 0.0005). There was no significant difference among other trunk muscles (P > 0.05). Figure 3 represents the anticipatory activity of the recorded trunk muscles during arm flexion.
4. Discussion 4.1. Reliability According to Munro’s classification [27], the onset latency demonstrated high to very high and the anticipatory activity showed moderate to very high intra- and inter-session reliability (Table 1). High intrasession ICC values of onset latency can show that the method
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Table 1 Intra-session and inter-session reliability of onset latency and anticipatory activity of individual muscles Variable Onset latency
Muscle
Intra-session reliability ICC SEM∗
Inter-session reliability ICC SEM∗
Right TA/IO§ Left TA/IO Right SLM† Left SLM Right LES‡ Left LES
0.94 0.83 0.93 0.88 0.94 0.90
14.47 18.79 14.90 15.01 12.48 11.74
0.86 0.93 0.97 0.90 0.97 0.95
10.87 6.87 6.05 6.55 4.90 3.90
Right TA/IO Left TA/IO Right SLM Left SLM Right LES Left LES
0.91 0.65 0.79 0.75 0.59 0.65
0.34 0.19 0.24 0.21 0.26 0.12
0.84 0.64 0.73 0.82 0.69 0.70
0.23 0.06 0.09 0.05 0.06 0.05
Anticipatory activity
∗ The
unit of measurement for SEM of onset latency is ms. There is no unit of measurement for SEM of anticipatory activity, since it is a normalized value. § transverse abdominis/internal oblique; † superficial lumbar multifidus; ‡ lumbar erector spine.
of onset detection used in this study (which was a combination of AGLR algorithm and visual inspection by a pre-trained examiner) was a reliable technique. Moreover, a pre-trained examiner took all the measures of skin preparation, detecting bony landmarks and electrode placement in two subsequent days which resulted in high inter-session reliability of the dependent variables. The number of trials used for data analysis is another important factor related to relative reliability. Increasing the number of trials enhances relative reliability of a specific outcome measure [28,29]. This fact is more critical when the outcome measure of a survey is obtained from an inherently variable data such as EMG signal. In addition, moderate reliability of anticipatory activity may be due to the method of normalization used in this study. However, we did not have any comparison of different normalization techniques. The second explanation may result from the rationale that muscle activity is dependent on temporal and spatial summation of motor units; therefore, variation in the recruitment of motor units in different trials may increase variability of response and, consequently, reduce reliability. 4.2. Feedforward activation of TA/IO In the present study, the contralateral TA/IO was the first muscle activated in anticipation of unilateral arm flexion which is in accordance with previous reports [7,8,30]. The ipsilateral TA/IO activated later than all other trunk muscles and even the prime mover (AD) which is also consistent with previous reports regarding feedforward activation of TA [4,11,14].
Furthermore, the ipsilateral TA/IO showed significant lower anticipatory activity compared to the contralateral TA/IO which is in agreement with the study of Allison et al. that evaluated this muscle bilaterally [11]. Although studying feedforward activation of TA is not a new topic, the direction-specificity of this muscle is one of the challenges among researchers. Hodges et al. carried out several studies in which feedforward activity of trunk muscles contralateral to the side of perturbation was evaluated during unilateral arm movements in different directions and demonstrated that contralateral TA precedes other trunk muscles regardless of the direction of movement [7,8,30]. They interpreted that activation of TA, unlike other superficial trunk muscles, is not direction-specific [7,8,30]. In contrast, Allison et al. [11] and Morris et al. [12] interpreted that TA acts asymmetrically and its anticipatory activation is directionally specific. The results of our study revealed that during anticipatory period of unilateral arm flexion, ipsilateral TA/IO activated later with lower magnitude than contralateral TA/IO, showing bilateral asymmetry in anticipatory activation of TA, which were similar to the findings of Allison et al. and Morris et al. [11,12]. Asymmetry in onset latency and anticipatory activity of TA/IO shows that the purpose of the activation of this muscle may not be a pure stability function by increasing the intra-abdominal pressure, but may be a more complex function. Morris et al. [12] proposed a new theoretical model for feedforward activation of TA and stated that this muscle acts as part of a synergy of muscles to counteract the rotary torques. Previous findings have shown that during left arm flexion, a flexion [7], left lateral flexion [7] and
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anticlockwise rotation [7,12] torque is imposed on the trunk. According to the findings of our study and previous research [7,8,11,12,30], it is obvious that the inconsistency regarding normal feedforward control of TA is not due to the discrepancies in the findings of different studies, but as Allison et al. [11] have mentioned, results from various interpretations. The human body specifically the trunk region has a complex nature with a great amount of redundancy at muscles [31]. Therefore, multiple muscles perform a similar function. Meanwhile, an individual muscle may have multiple actions in a complex system. Therefore, although TA may provide segmental control of the spine via increasing intra-abdominal pressure, it also acts as part of a muscle synergy [12] to counterbalance the anticipatory rotary torques. In addition, based upon previous studies concerning non-direction specific activation of TA in anticipation of any unilateral arm movement [7,8,30] as well as in vivo animal findings that showed bilateral activation of TA was very important in spinal segmental control [32], an exercise called “abdominal hollowing” was created and prescribed for patients who suffer from chronic low back pain (CLBP) or athletes and healthy individuals who are vulnerable to back pain [13]. The point is that these research evaluated trunk muscles on the contralateral side of the arm movement. However, our study showed that TA/IO did not co-activate bilaterally in anticipation of a unilateral task such as right shoulder flexion which is in accordance with previous reports [11,12]. Therefore, prescription of abdominal hollowing prior to limb movements for CLBP patients may be under question and it seems that prior to establishing a treatment technique, further studies are required to detect normal muscle activation pattern. 4.3. Feedforward activation of SLM and LES Posterior trunk muscles activated before the prime mover (right AD), significantly sooner with higher anticipatory activity than right TA/IO. However, they did not show any bilateral difference in onset latency or anticipatory activity. Anticipatory activity of LES and SLM in shoulder forward flexion has been reported in previous studies [7–9,14]. Activation of posterior trunk muscles prior to the prime mover in shoulder forward flexion is aimed at controlling perturbation produced by the movement. Hodges et al. [7] evaluated preparatory
trunk motion along with EMG recording of trunk muscles (including abdominal muscles and LES) in upper limb movements and showed that in upper limb flexion, activation of LES preceded the preparatory trunk extension. Anticipatory activity of these muscles may produce a secondary perturbation which should be controlled by other postural muscles. Unwanted accompanying torques from activated agonist muscles should be counterbalanced efficiently by activation of proper synergists to provide optimum postural stability. In addition, lack of bilateral difference in SLM and LES muscular response means that rotary perturbation of unilateral arm flexion may not elicit additional activity of these muscle groups. One limitation of our study was that we were not able to record TA using fine-wire electrodes. Surface EMG did not show the pure activity of TA because of an overlap between this muscle and the internal oblique in lower abdominal region. The electrode placement for TA/IO in this study was according to the survey of Marshal and Murphy [4] which showed that surface EMG can replicate intramuscular recordings for this muscle. Nevertheless, we cannot conclude that the observed muscle activation is solely due to TA. However, intramuscular EMG recording has also its own limitation which is the pick-up area of fine wire is much smaller that cannot be a representative of the whole muscle [12]. The second limitation of our study was that we could not assess kinematic variables along with kinetic data. Finally, it was not possible to record multiple muscles synchronously due to limited channels of the EMG device.
5. Conclusion Healthy subjects did not show bilateral anticipatory co-activation of TA/IO in unilateral arm elevation. This finding is of high importance since therapeutic exercises for CLBP patients are focusing on bilateral activation of TA. There is a need to perform further research to evaluate normal muscle activation pattern in healthy subjects. Furthermore, anticipatory activity of posterior trunk muscles is important to control the perturbation of arm flexion.
Acknowledgement This research was financially supported by Tehran University of Medical Sciences.
S. Davarian et al. / Normal postural responses preceding shoulder flexion
Conflict of interest
[16]
The authors declare no conflict of interest. [17]
References [1]
[2]
[3] [4]
[5]
[6]
[7]
[8]
[9]
[10]
[11]
[12]
[13]
[14]
[15]
Yiou E, Hamaoui A, Bozec SL. Influence of base of support size on arm pointing performance and associated anticipatory postural adjustments. Neuroscience Letters 2007; 423: 29-34. Nana-Ibrahim S, Vieilledent S, Leroyer P, Viale F, Zattara M. Target size modifies anticipatory postural adjustments and subsequent elementary arm pointing. Experimental Brain Research 2008; 184: 255-60. Bouisset S, Do MC. Posture, dynamic stability, and voluntary movement. Clinical Neurophysiology 2008; 38: 345-62. Marshall P, Murphy B. The validity and reliability of surface EMG to assess the neuromuscular response of the abdominal muscles to rapid limb movement. Journal of Electromyography and Kinesiology 2003; 13(5): 477-89. Allison GT, Henry SM. The influence of fatigue on trunk muscle responses to sudden arm movements, a pilot study. Clinical Biomechanics 2002; 17: 414-7. Kanekar N, Santos MJ, Aruin AS. Anticipatory postural control following fatigue of postural and focal muscles. Clinical Neurophysiology 2008; 119: 2304-13. Hodges P, Cresswell A, Daggfeldt K, Thorstensson A. Three dimensional preparatory trunk motion precedes asymmetrical upper limb movement. Gait and Posture 2000; 11(2): 92-101. Hodges P, Richardson C. Feedforward contraction of transversus abdominis is not influenced by the direction of arm movement. Experimental Brain Research 1997; 114(2): 362-70. Hodges P, Cresswell A, Thorstensson A. Preparatory trunk motion accompanies rapid upper limb movement. Experimental Brain Research 1999; 124(1): 69-79. Crommert ME, Ekblom MM, Thorstensson A. Activation of transversus abdominis varies with postural demand in standing. Gait and Posture 2011; 33: 473-7. Allison GT, Morris SL, Lay B. Feedforward responses of transversus abdominis are directionally specific and act asymmetrically: implications for core stability theories. Journal of Orthopaedic and Sports Physical Therapy 2008; 38(5): 22837. Morris SL, Lay B, Allison GT. Corset hypothesis rebutted – Transversus abdominis does not co-contract in unison prior to rapid arm movements. Clinical Biomechanics 2012; 27(3): 249-54. Richardson C, Hodges P, Hides J. Therapeutic exercise for lumbopelvic stabilization. A motor control approach for the treatment and prevention of low back pain. London: Churchill Livingstone, 2004. Silfies SP, Mehta R, Smith SS, Karduna AR. Differences in feedforward trunk muscle activity in subgroups of patients with mechanical low back pain. Archives of Physical Medicine and Rehabilitation 2009; 90(7): 1159-69. Sjödahl J, Kvist J, Gutke A, Öberg B. The postural response of the pelvic floor muscles during limb movements: A methodological electromyography study in parous women without lumbopelvic pain. Clinical Biomechanics 2009; 24(2): 183-9.
[18]
[19]
[20]
[21]
[22]
[23]
[24]
[25]
[26]
[27] [28]
[29]
[30]
[31]
[32]
551
O’Sullivan P, Dankaerts W, Burnett A, Farrell G, Jefford E, Naylor C, et al. Effect of different upright sitting postures on spinal-pelvic curvature and trunk muscle activation in a painfree population. Spine 2006; 31(19): E707-E12. Grenier SG, McGill S. Quantification of lumbar stability by using 2 different abdominal activation strategies. Archives of Physical Medicine and Rehabilitation 2007; 88: 54-62. Morris SL, Allison GT. Effects of abdominal muscle fatigue on anticipatory postural adjustments associated with arm raising. Gait and Posture 2006; 24: 342-8. Staude G, Flachenecker C, Daumer M, Wolf W. Onset detection in surface electromyographic signals: A systematic comparison of methods. Journal on Applied Signal Processing 2001; 2(1): 67-81. Staude G, Kafka V, Wolf W. Determination of premotor silent periods from surface myoelectric signals. Biomedical Techniques 2000; 45(2): 228-32. Staude G, Wolf W. Objective motor response onset detection in surface myoelectric signals. Medical Engineering and Physics 1999; 21(6-7): 449-67. Hodges PW, Richardson CA. Altered trunk muscle recruitment in people with low back pain with upper limb movement at different speeds. Archives of Physical Medicine and Rehabilitation 1999; 80: 1005-12. Strang AJ, Berg WP. Fatigue-induced adaptive changes of anticipatory postural adjustments. Experimental Brain Research 2007; 178: 49-61. Santos MJ, Kanekar N, Aruin AS. The role of anticipatory postural adjustments in compensatory control of posture: 1. Electromyographic analysis. Journal of Electromyography and Kinesiology 2010; 20(3): 388-97. Li X, Aruin AS. The effect of short-term changes in body mass distribution on feed-forward postural control. Journal of Electromyography and Kinesiology 2009; 19(5): 931-41. Li X, Aruin AS. The effect of short-term changes in the body mass on anticipatory postural adjustments. Experimental Brain Research 2007; 181(2): 333-46. Domholdt E. Rehabilitation research: principles and applications. 3rd ed. Philadelphia: Elsevier Saunders, 2005. Pinsault N, Vuillerme N. Test-retest reliability of centre of foot pressure measures to assess postural control during unperturbed stance. Medical Engineering & Physics 2009; 31(2): 276-86. Monaghan K, Delahunt E, Caulfield B. Increasing the number of gait trial recordings maximises intra-rater reliability of the CODA motion analysis system. Gait & Posture 2007; 25(2): 303-15. Hodges PW, Richardson CA. Transversus abdominis and the superficial abdominal muscles are controlled independently in a postural task. Neuroscience Letters 1999; 265(2): 91-4. Hodges PW. Pain and motor control: from the laboratory to rehabilitation. Journal of Electromyography and Kinesiology 2011; 21(2): 220-8. Hodges P, Kaigle Holm A, Holm S, Ekström L, Cresswell A, Hansson T, et al. Intervertebral stiffness of the spine is increased by evoked contraction of transversus abdominis and the diaphragm: In vivo porcine studies. Spine 2003; 28(23): 2594-601.
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