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Exp Brain Res (2014) 232:3515–3524DOI 10.1007/s00221-014-4040-8

RESEARCH ARTICLE

Pain reported during prolonged standing is associated with reduced anticipatory postural adjustments of the deep abdominals

Paul W. M. Marshall · Rick Romero · Cristy Brooks

Received: 12 June 2013 / Accepted: 9 July 2014 / Published online: 25 July 2014 © Springer-Verlag Berlin Heidelberg 2014

Introduction

Anticipatory postural adjustments (APAs) are involuntary and automatic adjustments in muscle activation that occur prior to a predictable perturbation (Belen’kii et al. 1967; Aruin and Latash 1995). APAs of the transversus abdominis (TA) muscle have received particular interest for the research of postural control in low back pain (LBP). Nearly 20-years ago, delayed onsets of TA during rapid shoulder movements in patients with chronic LBP were first reported (Hodges and Richardson 1996). This delay was sufficiently late to not be classed as anticipatory or feedforward activa-tion [muscle onset <50 ms after the prime mover (Hodges and Richardson 1996)]. While other abdominal and lumbar muscles also exhibited delays, the onset of TA was the most consistent difference across shoulder movement directions between people with and without chronic LBP (Hodges and Richardson 1996, 1999; Hodges 2001). Subsequent research in asymptomatic participants suggested that the early onset of TA, as compared to other trunk muscles, was not influenced by different upper or lower limb movement directions (Hodges and Richardson 1997a, b). Thus, it was summarized that in the presence of LBP, the onset of TA becomes a reflex to the movement of the limb rather than part of a feedforward postural control strategy (Hodges 2001). A limitation within initial research into TA APAs was the measurement only of contra-lateral TA onsets to a unilateral limb movement. Subsequent research using surface and fine-wire electromyography (EMG) (Marshall and Murphy 2003, 2006; Allison et al. 2008; Mannion et al. 2008; Brooks et al. 2012; Masse-Alarie et al. 2012), and Doppler imaging methods (Mannion et al. 2008; Gubler et al. 2010) provided evidence that the bilateral onsets of TA during a rapid unilateral shoulder movement were not symmetrical, and were influenced by the direction of limb

Abstract Within the context of low back pain, the meas-urement of deep abdominal anticipatory postural adjust-ments (APAs) during rapid limb movement has received much interest. There is dispute about the association between APAs and back pain. Moreover, there is limited evidence examining compensatory postural adjustments (CPAs) in back pain. This study examined the relation-ship between APAs and CPAs with pain reported in the low back during 2 h of prolonged standing. Twenty-six partici-pants with no history of severe back pain performed 2-h prolonged standing. APAs and CPAs of the deep abdomi-nal muscles (transverse abdominis/internal obliques) were measured by surface electromyography during rapid shoul-der flexion and extension. APAs and CPAs measured pre-standing revealed symmetrical anticipatory activity, but an asymmetry between the different sides of the abdominal wall for CPAs. APAs and CPAs measured pre-standing were not associated with pain reported during standing. For the whole group, APA amplitudes were reduced post-standing during shoulder flexion (p = 0.005). Pain reported during standing was associated with the changes in APA ampli-tudes post-standing (rs = 0.43, p = 0.002). These findings support previous research using hypertonic saline injections to induce back pain that showed reduced APA amplitudes, and extends findings to suggest pain does not effect com-pensatory postural adjustments.

Keywords Anticipatory motor activation · Compensatory postural adjustment · Transversus abdominis · Prolonged standing · Back pain

P. W. M. Marshall (*) · R. Romero · C. Brooks School of Science and Health, University of Western Sydney, Locked Bag 1797, Sydney, NSW 2751, Australiae-mail: p.marshall@uws.edu.au

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movement. Moreover, not all individuals with chronic LBP appear to exhibit delayed TA onsets during rapid shoulder movements (Silfies et al. 2009; Gubler et al. 2010; Tsao et al. 2010; Brooks et al. 2012; Vasseljen et al. 2012). Con-fusion about the anticipatory control of TA in the context of back pain may, in part, be explained by different collec-tion, onset detection and analysis methods, and a focus on exploring heterogenous chronic LBP populations. Exami-nation of the control of TA during an experimental situation likely to elicit pain reporting in the low back in asympto-matic individuals, such as prolonged standing, may provide unique insight into the relationship between anticipatory control of TA and back pain, and how the nervous system alters dynamic postural stability following maintenance of a prolonged upright posture.

Within an experimental context, it has been observed that 2 h of prolonged standing elicits reporting of pain in the low back for between 40 and 60 % of young, previ-ously asymptomatic individuals (Gregory et al. 2008; Greg-ory and Callaghan 2008). Increased bilateral coactivation of gluteus medius is evident at the start of the prolonged standing task in participants who subsequently report pain in the low back during standing (Nelson-Wong et al. 2008; Nelson-Wong and Callaghan 2010a, b; Marshall et al. 2011). Thus, it has been suggested that muscle activation strategies associated with postural control may be a predis-posing factor in the development of LBP during prolonged standing. No study has examined the relationship between TA APAs and the pain reported in the low back during pro-longed standing.

One study observed changes in the recruitment of TA during rapid limb movement following experimentally induced back pain using hypertonic saline in previously asymptomatic individuals (Hodges et al. 2003). These changes were manifested as a delayed APA in terms of onset timing and reduced strength of APA measured from the EMG amplitude (Hodges et al. 2003). EMG amplitude analysis during rapid limb movement is absent from most research examining TA APA function. EMG amplitude analysis allows examination of both the APA and com-pensatory postural adjustment (CPA). CPAs are initiated by sensory feedback signals and serve as a mechanism for restoration of body position after the perturbation has occurred (Henry et al. 1998; Park et al. 2004; Alexandrov et al. 2005). Currently, no research examining TA APAs has also measured the concomitant CPA in the time inter-val from 50 to 350 ms post onset of the limb prime mover. CPAs are of interest for this research considering findings which showed patients with mild chronic LBP exhibited a greater time to regain normal standing posture in response to a rapid bilateral shoulder flexion task compared to healthy individuals (Mok et al. 2011). Thus, it is reason-able to believe that in the presence of acute pain provoked

during prolonged standing, the timing and amplitude of the APA as well as the CPA will be reduced.

The aims of this study were to examine (1) APAs (tim-ing and amplitude) and CPAs of the ipsi-lateral and con-tra-lateral TA during rapid unilateral shoulder flexion and extension before and after 2 h of prolonged standing, (2) the relationship between APAs and CPAs pre-standing and pain reported during prolonged standing, and (3) whether pain reported in the low back was associated with changes in TA APAs and CPAs measured after 2-h standing. It was hypothesized that the during rapid unilateral shoulder flex-ion, contra-lateral TA onsets would be earlier and have a greater APA amplitude and lower CPA amplitude compared to the ipsi-lateral (sides reversed for shoulder extension). It was also hypothesized that pain in the low back reported during 2-h prolonged standing would be associated with later TA onsets and reduced APA and CPA amplitudes measured after the standing period.

Methods

Participants

This study included 26 healthy young adults (10 men and 16 women, age 24 ± 3 years, body-mass 62 ± 9.4 kg, height, 1.69 ± 0.07 m; mean ± SD). Participants were required to be between the ages of 18 and 30, have no lifetime history of severe LBP, do not work in an occupa-tion where prolonged standing was required (e.g., military, checkout operator at supermarket, bank teller), and were free from known metabolic and neuromuscular disease. Lifetime history of severe LBP was defined as any episode of LBP that required absence from work, sport, training or pain that required medication or treatment by a health care professional. Written informed consent was received from all participants. Ethical approval was received for this study from the University Human Research Ethics Committee.

Procedures

Participants were tested before and after the 2-h prolonged standing protocol for measurement of trunk muscle APAs. After the 2-h prolonged standing, participants remained standing for APA measurements to be performed.

Electromyography

APAs were measured before and immediately after 2-h pro-longed standing using surface electromyography record-ings of the anterior and posterior deltoid, and the right and left transverse abdominis/internal obliques muscle sites. Following careful skin preparation to reduce impedance

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below 5 kΩ, pairs of Ag/AgCl surface electrodes (Maxen-sor, Medimax Global, Australia) with a contact diameter of 10 mm and center to center distance of 20 mm were applied to the skin parallel to the underlying muscle fibers of trans-verse abdominis/internal obliques (TA/IO). Electrodes were placed 2 cm medial and inferior to the anterior supe-rior iliac spine (Marshall and Murphy 2003). This site has previously been established to have good internal validity for the relevant anatomy in the region, not be influenced by significant crosstalk during low-intensity abdominal con-tractions, and good replication of APA findings from fine-wire and ultrasound-based detection techniques (Allison et al. 2008; Mannion et al. 2008). Pairs of electrodes were applied to the right anterior and posterior deltoid as the prime movers for the rapid right arm shoulder flexion and extension tasks used in this study, with electrodes aligned parallel to the direction of the muscle fibers.

The rapid shoulder task required participants to either rapidly flex or extend their right arm in response to a ver-bal command from the researcher (‘flex,’ ‘extend’). After familiarization with the protocol, ten repetitions each of right shoulder flexion and extension were performed in a randomized order. Shoulder flexion was performed to the height of the acromion, while shoulder extension was per-formed to 40° (as demonstrated pretesting to participants using a flexible goniometer). Participants were instructed to “breath and relax” between each trial. A random time period of between 5 and 10 s was allowed between each shoulder movement. A trial was not performed if the par-ticipant attempted to laugh, cough, talk, etc.

EMG signals were recorded using the ML138 BioAmp (common mode rejection ratio (CMRR) >85 dB @ 50 Hz, input impedance 200 MΩ) with 16-bit analog to digital con-version, sampled at 2,000 Hz (ADI instruments, Australia). Raw signals were initially filtered with a fourth-order Bes-sel filter between 20 and 500 Hz. Subsequent data process-ing was performed using MATLAB (MATLAB v7.1, The Mathworks Inc, Natwick, MA, USA). EMG signals were rectified and digitally filtered using a fourth-order, 100 Hz Savitsky–Golay low pass prior to onset determination. The difference between the onset of the right and left TA/IO with the right deltoid prime movers formed the basis of the APA analysis.

Muscle onset determination

Initially, signals were visually inspected by enlarging the collection screen to a resolution of 25 ms epochs to determine that onsets were not obscured by signal artifact introduced from cable movement or ECG contamination. A physiologically relevant analysis window from 150 ms pre-deltoid onset to 400 ms post-deltoid onset (window based on visual inspection of deltoid onset) was selected

for calculation of muscle onsets and signal amplitudes. In addition, a 50 ms baseline epoch preceding the analysis window was selected to perform a computer-based verifica-tion of signal-to-noise ratios and for normalization of sig-nal amplitudes.

An initial algorithm was used to verify that an onset was present in the analysis window. The mean and SD for the 50 ms baseline epoch were calculated, and a threshold of 5 SD above this mean was established as a minimum signal-to-noise ratio for computer-based verification that a muscle onset was present within the analysis window. Of the 1,040 abdominal muscle trials recorded, 201 (19.3 %) were dis-carded from prescreening of the signal for a verifiable onset based on a combination of the initial visual inspection and/or a signal-to-noise ratio <5. Thus, some participants’ results were calculated from <10 trials. This is a compara-ble rejection rate to similar research (Mannion et al. 2008; Gubler et al. 2010).

For trials that were accepted after visual and computer inspection, the integrated profile method was used as an objective method of determining muscle onsets for the deltoid prime mover, and the right and left TA/IO. Briefly, the integrated profile method involves comparing the nor-malized integral of the muscle signal to a time normalized function to determine the point where there is a sudden increase in muscle activity (Allison 2003).

The onset time for the right and left TA/IO relative to the onset of deltoid prime mover (denoted as T0) was cal-culated as the difference in absolute onset time between the right and left TA/IO with the anterior or posterior deltoid. The average onset time for each muscle from the ten rep-etitions performed in each direction provided the basis for data analysis.

Muscle amplitude analysis

Integrals of the right and left TA/IO EMG signals during the rapid shoulder movement tasks were calculated for three different epochs in relation to T0 (Fig. 1). The time windows were (1) anticipatory amplitudes (APA), defined as the time from muscle onset of the right and left TA/IO to +50 ms post T0; (2) initial compensatory reactions (CPA1) from +50 to 200 ms; and (3) late compensatory reactions (CPA2) from +200 to 350 ms. The duration of the APA window was based on data suggesting that the fastest trunk muscle reflex response to a rapid limb move-ment cannot be earlier than +50 ms T0 (Bouisset and Zattara 1981; Aruin and Latash 1995). The processing of APA amplitude from the detected onset is a point of difference to previously described methods that analyzed the EMG signal from −100 to +50 ms T0 regardless of when the onset was identified (Santos et al. 2010). Since some trials may not exhibit a detectable onset within the

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APA window, it does not seem valid to always analyze the amplitude of the aforementioned APA window. The CPA time windows were chosen using literature on the tim-ing of corrective reactions observed in the trunk muscles in response to external perturbations (Henry et al. 1998; Santos et al. 2010). Division of the CPA window into the two subwindows differentiates the reflex responses (CPA1) from voluntary reactions (CPA2) (Latash 2008). To allow comparison of EMG activity before and after standing and between participants, time window integrals were normalized to the integral of the baseline 50 ms time window selected prior to the primary analysis win-dow (−500 to −450 ms T0). Deltoid muscle activity for each prime mover was also integrated in the time win-dow from T0 to +350 ms to provide a proxy indicator of

perturbation strength in the absence of kinematic tracking of shoulder movement.

Prolonged standing protocol

Participants were required to stand within a confined space of 0.5 m by 0.48 m situated adjacent to an adjustable height work bench (Gregory and Callaghan 2008; Nelson-Wong and Callaghan 2010b; Marshall et al. 2011; Raftry and Marshall 2012). The working bench was adjusted to a height 5 cm below the elbow where the participant was standing with the forearms at 90° of elbow flexion. At no time was the participant permitted to leave the test-ing area except in emergency circumstances or personal choice to withdraw participation from the experiment. At

Fig. 1 Representative rectified EMG traces of right anterior deltoid (PD), and the left and right transversus abdominis/internal obliques (TA/IO) muscle activity during rapid shoulder flexion, before and after 2-h prolonged standing. Time is expressed relative to the onset of anterior deltoid (0 ms onset of deltoid). The corresponding time

epochs for the anticipatory postural adjustment (APA; from muscle onset to +50 ms), and compensatory postural adjustments (CPA1; from +50 to +200 ms, and CPA2; from +200 to +350 ms) are indi-cated with dashed lines

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the initiation of the standing protocol, the participant was instructed how to stand throughout the duration of the task. Participants were allowed to adopt any comfortable stand-ing posture which they would regularly use while standing. At all times across the 2 h, the participant was restricted from resting their arms or legs on the work bench to sup-port their weight. The 2-h standing protocol was separated into four 30-min periods during which time participants performed a variety of tasks replicating those performed by many professions requiring periods of prolonged standing. Currency handling, card dealing, pen assembly, and mec-cano set assembly were randomised among participants to mitigate any order effects on pain development. Partici-pants rated their pain in the low back on a 100 mm visual analog scale (VAS) prior to the start of, every 15 min dur-ing, and at the end of the 2-h standing period (Huskisson 1974). The left end of the line was anchored with ‘no pain,’ and the right end of the line with ‘worst pain imaginable.’ The VAS has been found to have good construct valid-ity (Summers 2001) and reliability (Revill et al. 1976). A minimum clinically meaningful increase in VAS score is >10 mm (Kelly 1998).

Data analysis

Kolmogorov–Smirnov testing found that all depend-ent variables were normally distributed pre-standing, and therefore, parametric testing procedures were used. For all data analysis, the right TA/IO signal was coded as the ipsi-lateral (ipsi), and the left TA/IO the contra-lateral (contra) to describe the orientation of each muscle with respect to the right shoulder movement. Pre-standing APA and CPA variables were analyzed for main and interaction effects between movement direction (flexion, extension) and mus-cle (ipsi-lateral, contra-lateral) by univariate analysis of variance (ANOVA). A repeated-measures ANOVA was used to examine the change in dependent variables before and after standing (same ANOVA model but introduction of two levels of time: pre- and post-standing). If significant main or interaction effects were observed in the ANOVA models, post hoc tests using Bonferroni’s correction were used. Covariates in the ANOVA models were gender, age, and the integral of the deltoid prime mover for the respec-tive time epoch (APA, CPA1, CPA2). Differences identi-fied in the ANOVA were expressed as mean difference and 95 % confidence intervals (CIs).

VAS scores reported during prolonged standing were not normally distributed, and therefore, nonparametric cor-relation analyses (Spearman’s rank correlation coefficient; rs-value) were performed to examine whether dependent variables measured pre-standing were associated with VAS scores during standing. Correlation analyses were also per-formed to examine the relationship between VAS scores

during standing and that change in each dependent variable measured from the difference between the post- and pre-standing score.

The significance level for statistical analyses in this study was p < 0.05. Unless otherwise stated, data are mean ± SD.

Results

Pain reporting

Sixteen participants reported a clinically meaningful increase in back pain during prolonged standing (mean increase 33 ± 22 mm), while ten participants reported a mean increase of 5.6 ± 3.5. Four participants reported pain in the back >50 mm, and three reported pain between 30 to 50 mm. There were no demographic differences (age, height, weight) between participants who did and did not report a clinically meaningful increase in pain.

Muscle onsets

Pre-standing, a muscle × movement interaction was observed for TA/IO onset times (p < 0.001). During shoul-der flexion, the onset of contra-lateral TA/IO preceded anterior deltoid by 30 ± 67 ms, while the ipsi-lateral TA/IO was after deltoid by 15 ± 29 ms (mean difference = 46 ms, 95 % CI 21–54 ms, p < 0.001). During shoulder exten-sion pre-standing, the onset of the ipsi-lateral and contra-lateral TA/IO preceded posterior deltoid during exten-sion by 21 ± 25 and 16 ± 26 ms, respectively (p = 0.57). There was no difference between flexion and extension for the onset of contra-lateral TA/IO (p = 0.36). The onset of ipsi-lateral TA/IO was earlier during extension compared to flexion (mean difference = 36 ms, 95 % CI 5–24 ms, p < 0.001). No changes were observed following prolonged standing for latency times measured during shoulder flex-ion and extension. Pre-standing latency times were not associated with VAS scores during standing. VAS scores reported during standing were not associated with the change in latency times recorded post-standing.

APA amplitude analysis

Pre-standing, there was no difference between the ipsi-lat-eral and contra-lateral TA/IO for APA amplitudes. A main effect of direction was observed (Fig. 2; p < 0.001), with higher APA amplitudes recorded during extension com-pared to flexion (mean difference = 7.4, 95 % CI 3.7–11.1, p < 0.001). Pre-standing APA amplitudes did not predict VAS scores reported during standing. APA amplitudes were reduced post-standing during shoulder flexion only

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(collapsed for ipsi-lateral and contra-lateral TA/IO; mean difference = 2.4, 95 % CI 0.3–4.5, p = 0.005). VAS scores reported during standing were positively associated with the change in APA amplitudes post-standing during shoul-der flexion (Fig. 3; rs = 0.43, p = 0.002).

CPA amplitude analysis

For CPA1 amplitudes pre-standing (Fig. 4), a direction × side interaction was observed (p = 0.015). CPA1 ampli-tudes for ipsi-lateral TA/IO were greater than contra-lateral TA/IO during shoulder flexion (mean difference = 11.4,

95 % CI 4.4–18.4, p = 0.005). Also, contra-lateral TA/IO amplitudes were higher during shoulder extension com-pared to flexion (mean difference = 7.7, 95 % CI 3.4–12.1, p = 0.003). Pre-standing CPA1 amplitudes did not predict VAS scores reported during standing. Post-standing CPA1 amplitudes were not different from pre-standing values. There were no associations between VAS scores during standing and changes in CPA1 amplitudes post-standing.

For CPA2 amplitudes pre-standing, a main effect of side was observed with greater amplitudes recorded for ipsi-lat-eral TA/IO during both movement directions (Fig. 5; mean difference = 7.9, 95 % CI 2.0–13.8, p = 0.009). Pre-stand-ing CPA2 amplitudes did not predict VAS scores reported during standing. Post-standing CPA2 amplitudes were not different from pre-standing values. There were no associa-tions between VAS scores during standing and changes in CPA2 amplitudes post-standing.

Discussion

In this study, we observed symmetric anticipatory activity between the ipsi-lateral and contra-lateral TA/IO during the single arm shoulder flexion task, but asymmetric com-pensatory activity. Moreover, this is the first study to report reduced anticipatory TA/IO muscle activity following a period of prolonged standing, and a relationship between pain reported during standing and the change in anticipa-tory activity.

The results of this study suggest that despite differ-ences in onset time, which were both within the feedfor-ward onset window, the anticipatory muscle activity of the ipsi-lateral and contra-lateral TA/IO is symmetrical. Previ-ous research examining TA, or in the context of the surface

Fig. 2 APA amplitudes during shoulder flexion and extension meas-ured pre and post 2-h prolonged standing for all participants (n = 26). Data are collapsed for the ipsi- and contra-lateral TA/IO as no between-side differences were observed for APA amplitudes. Ampli-tudes during extension were greater than flexion (p < 0.001). Post-standing, APA amplitudes were reduced from pre during shoulder flexion only (**p = 0.005). Data are mean and 95 % CIs

Fig. 3 Relationship between changes in APA amplitudes post-standing for the ipsi- and contra-lateral TA/IO during shoulder flexion and the pain score (VAS, mm) reported during prolonged standing. A significant positive correla-tion was observed (rs = 0.43, p = 0.002)

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EMG method in this study TA/IO, anticipatory activity has solely relied on muscle onset times (Allison et al. 2008; Mannion et al. 2008; Marshall and Murphy 2010; Masse-Alarie et al. 2012). The amplitude of the EMG signal is influenced by factors including membrane excitability, sig-nal cancelation, and the inability to discriminate motor unit firing rate from the number of units recruited (Farina et al. 2004, 2008; Keenan et al. 2006). Notwithstanding these limitations, which also likely affect the ability to accurately determine onset time, the amplitude of the EMG signal probably provides a better estimate of gross central motor output and the net recruitment of muscle in the anticipa-tory window compared to onset time. Asymmetry between

the ipsi- and contra-lateral TA/IO was evident in the ampli-tude of the CPA, with greater activity for ipsi-lateral TA/IO during both movement directions. All together, these find-ings support and extend an alternative hypothesis proposed for the role of TA/IO during rapid limb movement (Alli-son et al. 2008; Masse-Alarie et al. 2012). This hypothesis proposed that activation of both muscles is anticipatory, but the earlier onset of the contra-lateral TA/IO during flexion was required to control the rotation torque (Allison et al. 2008; Masse-Alarie et al. 2012). The results of this study suggest that the relevance of the asymmetric onset does not relate to the anticipatory period, but to the compensatory period where sensory feedback and voluntary commands are integrated to provide a net response. During both shoul-der movement directions, the ipsi-lateral TA/IO had greater activity during the compensatory periods, which helps pro-vide a more informed hypothesis about the function of TA/IO activity. It would seem that the bilateral TA/IO activity is symmetrical in the anticipatory phase, but is asymmet-ric in the compensatory phase to control the rotation torque imparted on the trunk by the single limb movement.

This is the first study to report that anticipatory and CPAs of TA/IO measured before prolonged standing were not correlated with pain scores reported in the low back during the 2-h task. Previous research which has observed altered muscle recruitment strategies prior to pain reporting has analyzed bilateral co-activation patterns of hip, trunk, and abdominal muscles during the static standing task (Nel-son-Wong et al. 2008; Marshall et al. 2011). The measure-ment paradigm in this study could be considered an exami-nation of dynamic postural control, where the stability of the trunk is challenged by a rapid perturbation. Thus, while providing insight into underlying postural control strategies for a specific muscle, the measurement model of this study appears to have little utility in predicting pain reporting during a prolonged postural task.

The results of this study support and extend previous findings that showed acute pain provoked in the low back alters anticipatory muscle activity of the deep abdominals (Hodges et al. 2003). The absence of change in CPAs sup-ports this selective influence of pain on anticipatory mus-cle activity and suggests that the effect of pain is not medi-ated by alterations in feedback mechanisms or voluntary drive. While a positive relationship was observed, suggest-ing that higher pain scores were associated with increased APAs, inspection of the results (Fig. 3) shows this conclu-sion would be flawed. Indeed, the cluster of results below a pain reporting score of 40 mm shows that lower levels of self-rated back pain were associated with reduced APA amplitudes during flexion post-standing. The cluster of par-ticipants (n = 5) who reported pain above 50 mm tended to show no change. Thus, there is some support here for the hypothesis that in the presence of experimentally induced

Fig. 4 CPA1 amplitudes pre-standing for the ipsi- and contra-lat-eral TA/IO during shoulder flexion and extension. **A lower CPA1 amplitude for the contra-lateral TA/IO compared to the ipsi-lateral TA/IO during flexion (p = 0.005), and †a lower CPA1 amplitude for the contra-lateral TA/IO during flexion compared to extension (p = 0.003). Data are mean and 95 % CIs

Fig. 5 CPA2 amplitudes pre-standing for the ipsi- and contra-lateral TA/IO during shoulder flexion and extension. CPA2 amplitudes were lower for the contra-lateral TA/IO during flexion and extension (**for main effect of side, p = 0.009). Data are mean and 95 % CIs

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pain during prolonged standing, although only within a range of no pain to mild-to-moderate pain, anticipatory activity is reduced. The hypothesis of this research was based on evidence that induced acute back muscle pain using hypertonic saline injections (Hodges et al. 2003), and observed delayed onset times and reduced muscle ampli-tudes within the anticipatory period. The provocation of pain in this study, which was likely associated with creep-induced deformation of the posterior tissues in the lumbar spine as a more flexed posture is adopted (Gregory and Callaghan 2008; Nelson-Wong et al. 2008), appears to have similar effects on anticipatory muscle activity compared to the acute pain elicited from injection-based methods. Whether the reduced anticipatory activity is affecting the ability of participants to maintain normal standing posture during the rapid upper limb perturbation is not clear from this study. Future work should combine center-of-pressure and lumbar kinematics measures with the muscle analysis used in this study to provide understanding for the conse-quence of reduced anticipatory activity. Also, it is not clear why the observed reductions in anticipatory TA/IO ampli-tudes were not observed in the participants who reported pain over 50 mm. While this may reflect type II error, con-siderations for trunk stiffness strategies employed in the presence of higher pain levels should be considered, and thus, the lack of other measures (e.g., other trunk muscles, kinematics, and kinetics of the movement paradigm) is a weakness of this study for understanding potential implica-tions of this observation.

An interesting observation in this study was that the pain reported in the low back was correlated with reduced APAs during shoulder flexion, but not extension. It is unclear why reduced anticipatory activity following prolonged standing was direction specific. One difference that may explain this finding was that the range of motion was higher for shoul-der flexion compared to extension. Shoulder flexion was performed to the level of the acromion, approximately 90° of shoulder flexion, whereas extension was performed to approximately 40° only. The limitation on extension allows an isolated shoulder movement to occur, minimizing con-tribution from other joint movements and allowing valid comparison to the shoulder flexion movement. Despite the lower range of motion, APA and CPA1 amplitudes were higher for shoulder extension, suggesting that the reduced range of motion and resultant torque did not affect the mag-nitude of postural adjustments.

The difference in range of motion and resultant rota-tion torque of the shoulder flexion and extension move-ments may explain why asymmetries in onsets were only observed for the shoulder flexion movement. However, recent research using the rapid shoulder flexion method with lower range of motion to this study (45°–60°), which is comparable to the extension range of motion, has also

reported asymmetric onsets between the ipsi-lateral and contra-lateral TA/IO [surface (Lariviere et al. 2013) and fine-wire EMG methods (Morris et al. 2013)]. Thus, range of motion probably does not explain why onset times are different during flexion and not extension. Asymmetric onsets of TA/IO during shoulder flexion have been high-lighted as being relevant in research showing chronic side-specific adaptation in LBP patients (Marshall and Murphy 2008), as well as absent short-interval intracortical inhibi-tion of the ipsi-lateral TA/IO, which was associated with delayed muscle onsets in LBP patients (Masse-Alarie et al. 2012). While no evidence was observed in this study to link asymmetric onsets during flexion to pain reported in the low back during standing, the relevance of these asym-metries moving forward is of particular interest for under-standing postural control and how it is altered in the patho-logical state.

Several methodological aspects of this study must be discussed for contextualizing the generalizability of find-ings. The findings of this study have replicated previously observed patterns measured with tissue Doppler imaging (Mannion et al. 2008; Gubler et al. 2010) and intramuscular and surface EMG (Allison et al. 2008; Marshall and Mur-phy 2010) for asymmetric trunk muscle onsets during rapid shoulder flexion, with the left (contra-lateral side) abdomi-nals activating in advance of the right (ipsi-lateral). Thus, we are confident in the validity of results. Shoulder flex-ion results may lack accuracy, as it must be noted that most (131) of the 201 muscle onsets excluded from analysis were identified during the shoulder flexion task. This study should not be used to generalize findings to a chronic LBP population, where various chronic neuromuscular altera-tions are likely to alter both the resting and post-standing APAs and CPAs. Finally, this study has only presented data from a single muscle site. Examination of other trunk mus-cles may provide greater understanding and likely reveal a more complex and individual picture, of how dynamic pos-tural control is altered in response to pain provoked during a prolonged static postural task.

Conclusion

Anticipatory activity of TA/IO appears to be bilateral based on similarities in the amplitude of activity, despite differ-ences in the onset times during the shoulder flexion task. Indeed, the asymmetric activity of TA/IO which is prob-ably associated with reacting to and controlling the rotation torque of the trunk was manifested during the compensa-tory time periods. Prolonged standing induced reductions in the anticipatory muscle activity during shoulder flexion and was associated with pain reporting during standing. This supports previous research using hypertonic saline

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injections and extends on the findings to suggest that pain effects anticipatory activity only. Whether the changed anticipatory activity affects the ability to regain normal standing posture following limb perturbation is unclear from this study.

Acknowledgments The author acknowledges Dr. Simon Green and Dr. Jason Siegler for their comments on the manuscript.

Conflict of interest The author declares no financial relationship relevant to this article and no conflict of interest.

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