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    Journal of Electromyography and Kinesiology 14 (2004) 463474www.elsevier.com/locate/jelekin

    Spatio-temporal evaluation of neck muscle activationduring postural perturbations in healthy subjects

    D. Falla a,, A. Rainoldi b,c, R. Merletti b, G. Jull a

    a Division of Physiotherapy, The University of Queensland, Brisbane, Qld 4072, Australiab Centro di Bioingegneria, Dip. di Elettronica, Politecnico di Torino, Turin, Italy

    c Department of Physical Medicine and Rehabilitation, University of Tor Vergata and Fondazione Don Gnocchi, Rome, Italy

    Abstract

    The purpose of this study was to examine the spatio-temporal activation of the sternocleidomastoid (SCM) and cervical exten-sor (CE) muscles with respect to the deltoid muscle onset during rapid voluntary upper limb movement in healthy volunteers. Therepeatability and reliability of the spatio-temporal aspects of the myoelectric signals were also examined. Ten subjects performedbilateral and unilateral rapid upper limb flexion, abduction and extension in response to a visual stimulus. EMG onsets and nor-malised root mean square (nRMS) values were calculated for the SCM and CE muscles. Subjects attended three testing sessionsover non-consecutive days allowing the repeatability and reliability of these measures to be assessed. The SCM and CE musclesdemonstrated feed-forward activation (activation within 50 ms of deltoid onset) during rapid arm movements in all directions.The sequence and magnitude of neck muscle activation displayed directional specificity, however, the neck flexor and extensormuscles displayed co-activation during all perturbations. EMG onsets demonstrated high repeatability in terms of repeated mea-sure precision (nSEM in the range 1.95.7%). This was less evident for the repeatability of nRMS values. The results of this studyprovide a greater understanding of cervical neuromotor control strategies. During bilateral and unilateral upper limb perturba-tions, the SCM and CE muscles demonstrate feed-forward co-activation. It seems apparent that feed-forward activation of neckmuscles is a mechanism necessary to achieve stability for the visual and vestibular systems, whilst ensuring stabilisation and pro-tection of the cervical spine.# 2004 Elsevier Ltd. All rights reserved.

    Keywords:Neck muscle; Electromyography; Postural control; Feed-forward

    1. Introduction

    Perturbation studies have been used extensively toexplore the neural mechanisms underlying balance con-trol. Internal perturbations such as a rapid movementof the arm produce reactive compensatory forces

    opposing those produced by the arm movement [5].These forces are transferred to body segments elicitinga series of postural adjustments. The origin of the pos-tural adjustments is twofold. Firstly, the movementcauses a change in body geometry. This may result in ashift of the centre of gravity, which causes dis-equilibrium. Secondly, the forces generated to initiate amovement induce reaction forces[25].

    Detection of the spatio-temporal aspects of myo-electric signals during postural perturbations can beutilised to analyse muscle recruitment and enhance ourunderstanding of neuromotor control strategies. Feed-forward muscle activation is one central nervoussystem (CNS) strategy, which can be detected with

    analysis of the temporal aspects of the electromyo-graphic (EMG) signal. Feed-forward postural respon-ses are a mechanism employed by the CNS to regulatemotor control of muscles and contribute towards themaintenance of stability[1]. Extensive evidence of feed-forward activation of limb and trunk musculature inresponse to perturbations is available in the literature[7,8,12,1618]. However, there is a paucity of studiesthat have investigated spatio-temporal aspects of neckmuscle activation during postural perturbations.

    Gurfinkel et al. [13] demonstrated that backward accel-eration of the head precedes an internal perturbation

    Corresponding author. Tel.: +61-7-3365-4529; fax: +61-7-3365-2775.

    E-mail address:[email protected] (D. Falla).

    1050-6411/$ - see front matter # 2004 Elsevier Ltd. All rights reserved.doi:10.1016/j.jelekin.2004.03.003

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    of upper limb flexion, which coincides with an increase intrapezius and splenius capitus muscle activity. Theauthors suggested that this anticipatory muscle acti-vation provided generalised postural fixation of thecervical spine. This study was supported by the work ofvan der Fits et al. [25] which demonstrated primary

    activation of the dorsal postural muscles includingthe neck extensors, with rapid upper limb flexion.This result confirmed that the basic nature of thedirection-specific organisation of postural adjustments,readily identified in the lower limb and trunk muscles,is also present in the neck.

    The present study aimed to provide a more extensiveanalysis of neck muscle activation in response to inter-nal postural perturbations. This study sought to exam-ine the temporal and spatial response of thesternocleidomastoid (SCM) and the cervical extensor(CE) muscles during rapid voluntary upper limb move-ments in three directions (flexion, extension and abduc-

    tion) in healthy volunteers. Internal perturbations wereselected to assess neck muscle responses for the follow-ing two reasons. Firstly, internal perturbations allowidentification of the response to the perturbation that istemporally and spatially predictable by the CNS. Sec-ondly, internal perturbations allow evaluation of thefinal output of the motor command from the CNSwithout the influence of afferent information resultingfrom the perturbation[14].

    The second aim of this investigation was to examinethe repeatability and reliability of the spatio-temporalaspects of the EMG signals obtained from the SCM

    and CE muscles during rapid upper limb perturbations.

    2. Methods

    2.1. Subjects

    Ten right-handed healthy volunteers aged between25 and 35 years (mean 29.2, SD 3.4) participated inthis study. Subjects were included if they were free ofneck pain, had no past history of orthopaedic disordersaffecting the neck and no history of neurological dis-orders. Subjects attended three testing sessions over

    non-consecutive days.Ethical approval for the study was granted by the

    Institutional Medical Research Ethics Committee. Allstudies were conducted in accordance with the declar-ation of Helsinki.

    2.2. Instrumentation and measurements

    Visual commands to move were provided by lightemitting diodes (LED) fixed to an adjustable visual dis-play board positioned at the subjects eye level. A redLED provided the stimulus to move for bilateral

    shoulder movements. For the unilateral arm movementtask, a red and green LED provided the prompt for theright and left arm, respectively. The electrical signalproviding the stimulus to move was recorded simul-taneously with the EMG signals to generate the triggerinformation for further data reduction. The timebetween stimuli was randomly varied and controlled bythe investigator.

    Myoelectric signals were detected bilaterally from thesternal head of the SCM, CE, anterior, middle andposterior deltoid muscles using bipolar disposable elec-trodes (1 cm disc electrodes, inter-electrode distance2 cm) (Myotronics, Noromed) following careful skinpreparation[4]and using published guidelines for elec-trode placement. For the SCM muscles, the electrodeswere positioned at 1/3 the distance from the sternalnotch to the mastoid process at the distal end overlyingthe muscle belly[9]. For the CE muscles, the electrodeswere positioned over the distal half of the distance

    between the base of the occiput and the spinous pro-cess of the seventh cervical vertebra. For the anterior,middle and posterior deltoid electrodes were positionedin the lower half of the distance from the acromion tothe deltoid tuberosity[9,20]. The ground electrode wasplaced on the upper thoracic spine.

    Signals were amplified (gain 2000), passed througha 10450 Hz bandwidth filter (40 dB/decade slope oneach side) and sampled at 2048 Hz (ASE16-16 channelamplifier, LISiN Centro di Bioingegneria, Politecnicodi Torino, Italy). The samples were digitised by a 12 bitA/D converter and stored on a personal computer.

    2.3. Procedure

    Prior to commencement of experimental trials, EMGdata were collected for 10 s during standardised man-euvers for normalisation of the EMG amplitude. Withthe subject positioned in supine lying, the reference vol-untary contraction for the SCM involved a combinedmovement of cranio-cervical and cervical flexion to liftthe head so that it just cleared the bed and was heldisometrically[11]. For the CE muscles, the subject waspositioned in prone lying and performed an isometriccervical extension contraction so that the forehead just

    cleared the bed. Each reference voluntary contractionwas repeated three times with an interval of 1 minbetween repetitions.

    During the experimental trials, subjects performed aseries of unilateral and bilateral rapid shoulder flexion,abduction and extension movements keeping the elbowstraight, in the relaxed standing position with their feetplaced shoulder width apart. Subjects were instructedto move, upon the light command, as fast as possibleand to focus on the speed of movement rather than onthe distance. Rapid shoulder flexion and abductionwere performed to approximately 60

    v

    and shoulder

    464 D. Falla et al. / Journal of Electromyography and Kinesiology 14 (2004) 463474

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    extension to 40v

    [16]. Each subject initially performedtwo to three practice repetitions to allow EMG signalquality to be assessed and to ensure consistency of thespeed and distance of arm movement between repeti-tions. Each subject then performed three repetitions ineach direction in a randomised order. The experimental

    protocol was repeated over three non-consecutive days.

    2.4. Data management and statistics

    Previously developed software for muscle activitydetection from EMG signals was utilised to determinethe onoff timing of muscles (for a complete descrip-tion of the algorithm used, refer to the work of Merloet al. [19]). Several methods for onoff timing estima-tions are proposed in the literature. These methods arebased on the single-threshold method [24] or on thesignal envelope [6,15,23]. In this study, the recentmethod described by Merlo et al. [19] was adopted

    since it offers the best performance in terms of onsetdetection. This program is based on identifying singlemotor unit action potentials from the interferenceEMG signal using the continuous wavelet transform. Amanifestation variable is computed as the maximum ofthe outputs of a bank of matched filters at differentscales. A threshold is applied to the manifestation vari-able to detect EMG activity. With the method pro-posed by Merlo et al. [19], the SD of onset estimatereduces from 26 to 17 ms when the signal to noise ratiovaries from 2 to 8 dB, while the single thresholdapproach leads to a SD of onset estimate always great-

    er than 130 ms and results in the worst performance.Subsequent to identification of EMG onsets, two

    measures were calculated; (a) the reaction time of del-toid muscle, defined as the time from stimulus to theonset of deltoid muscle activity and (b) relative latencydefined as the latency between the onset of the agonist

    limb muscle and each of the neck muscles. Fig. 1 pre-sents an example of raw EMG traces recorded fromthe SCM, CE and deltoid muscles obtained from asubject performing left and right rapid unilateral upperlimb flexion movements. Fig. 2 illustrates identificationof the onoff timing of the CE and deltoid muscles dur-

    ing rapid unilateral upper limb flexion movements.Neck muscle latencies and deltoid reaction timeswere calculated for the three contractions for each con-dition. Any EMG onset occurring between 150 msbefore and 50 ms after the agonist arm muscle EMGonset was considered feed-forward activation[2,16].

    The data from subject 6 for all contractions on thethird day and data from subject 9 for the unilateralextension contractions on the third day were excludeddue to errors in data collection. As a consequence ofsuch data purging, all contractions from subject 6 andthe unilateral extension contractions from subject 9

    were omitted in the assessment of repeatability.To evaluate the EMG amplitude, root mean square

    (RMS) values were calculated for the EMG bursts(time interval between the on and off timing of amuscle) identified in the initial signal processing pro-cedure. For normalisation, RMS values obtained

    during the experimental trials were expressed as a per-centage of a maximum 1 s RMS value obtained acrossthe three repetitions of the reference voluntary contrac-tions for each muscle.

    The means and SD for the nRMS values, deltoidreaction times and SCM and CE relative latencies were

    calculated from the three repetitions performed by eachsubject for each muscle and each condition. TheWilcoxon non-parametric matched paired test was usedto verify whether significant differences existed betweenmuscles, contractions, and sides within the group ofsubjects. The significance level was set at p

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    2.5. Repeatability of amplitude and time variableestimates

    The repeatability of deltoid reaction times, relative

    latencies and nRMS values of the SCM and CE mus-

    cles were examined. For each condition, the subject

    performed three repetitions and the experimental pro-

    tocol was repeated three times over non-consecutive

    days. Repeatability estimates were obtained by evaluat-

    ing intraclass correlation coefficients (ICC) and the

    normalised standard error of the mean (nSEM). Pre-

    vious work examining sEMG repeatability has ident-

    ified the advantages of considering both the ICC andnSEM [21,22]. A low nSEM indicates a reliable esti-

    mate of the mean, that is, minimal experimental noise

    while analysis of variance (ANOVA) provides infor-

    mation about the factors contributing to the total vari-

    ance (days, trials, subjects, measurement conditions).

    In particular, ICC is the portion (in %) of variance due

    to subjects: its value indicates whether the variations of

    the measurements reflect subject-to-subject variations

    or random experimental noise introduced by different

    days or trials[9].

    3. Results

    3.1. Spatial and temporal characteristics

    When rapid movements of the arm were performedin response to a visual stimulus, the SCM and CE mus-cles were activated within 50 ms of the onset of thedeltoid muscle, thereby fulfilling the criterion forfeed-forward activation with movement. The neckflexor and extensor muscles demonstrated co-activationacross all conditions.

    Table 1 presents the means and SD for the deltoidreaction times. Deltoid reaction times were significantly

    greater for unilateral upper limb movements across allconditions compared to bilateral movements.

    Fig. 3 presents the means and SD of the relativelatencies recorded for the SCM and CE muscles in per-formance of rapid bilateral arm flexion, abduction andextension. For bilateral upper limb flexion, a trend waspresent to suggest onset of CE muscle activity (right9:3 18:7 ms, left 15:4 17:8 ms) prior to the SCM(right 22:0 14:3 ms, left 21:5 9:5 ms). During bilat-eral upper limb abduction, a similar trend was evidentto support activation of the CE muscles (right23:1 8:4 ms, left 30:8 5:3 ms) prior to the SCM

    Fig. 2. Raw EMG traces from the cervical extensor (CE) and deltoid (DELT) muscles obtained from a subject performing (A) right and (B) leftrapid unilateral upper limb flexion movements. Previously developed software [19]was utilised to determine the onoff timing of muscles. EMGamplitude, was calculated for the time interval between the on and off timing of each muscle.

    Table 1Reaction times (ms) for the deltoid muscles with each movement direction (mean SD). Differences between bilateral and unilateral movementsare also presented. Reaction times for unilateral contractions were significantly greater than bilateral. Wilcoxon paired test, N 54 for flexion andabduction andN 48 for extension

    Condition Flexion Abduction Extension

    Left Right Left Right Left Right

    Bilateral 215 29 215 29 196 36 198 36 202 32 205 33Unilateral 237 21 241 16 227 35 213 30 241 24 232 32Unilateralbilateral 22 12 25 15 31 32 15 22 38 22 22 22

    p < 0.01. p

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    (right 34:9 13:5 ms, left 29:5 18:3 ms). For bilateralupper limb extension, onset of the SCM muscles (right17:1 15:8 ms, left 18:5 15:2 ms) occurred prior to theCE muscles (right 24:1 14:4 ms, left 32:2 9:2 ms).

    Activation of the contralateral CE muscles was notdetected during the unilateral movement tasks in eightout of the 10 subjects. Fig. 4 presents the means andSD of the relative latencies recorded for the bilateralSCM and ipsilateral CE muscles in performance of uni-lateral flexion, abduction and extension movements.No differences in the relative latencies of the SCM andCE muscles were identified during unilateral flexionand abduction movements. For unilateral upper limbextension performed on the right side, the right SCM

    (18:2 7:7 ms) was activated prior to the right CEmuscle (28:6 14:7 ms). No significant difference wasidentified for the onset of left and right SCM musclesfor unilateral upper limb movements in all three direc-tions. EMG onsets for SCM and CE were comparedbetween bilateral and unilateral arm movements,revealing no difference.

    3.2. Signal amplitude behaviour

    Fig. 5 presents the nRMS values obtained for theSCM and CE muscles during each condition and

    Table 2 presents the significant differences betweenconditions. The main significant findings are sum-marised as follows.

    Overall, the SCM muscles demonstrated the greatestactivation during bilateral and unilateral upper limbflexion compared to bilateral and unilateral extensionand abduction. For the left SCM muscle, there was nodifference in the magnitude of activation during unilat-eral and bilateral arm flexion manoeuvres. This wasalso the case for the right SCM muscle for compar-isons between bilateral flexion and right unilateral flex-ion. However, for the right SCM, greater activation

    was evident during bilateral arm flexion compared withunilateral arm flexion performed on the left.

    Across all movements, both unilateral and bilateral,greatest nRMS values for the CE muscles wererecorded during bilateral arm abduction. For both theleft and right CE muscles, greater nRMS values wererecorded during unilateral flexion and abduction com-pared to extension (all p

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    precision identified for the detection of EMG onsetswas smaller for the estimation of nRMS values (nSEM

    between 3.8% and 25.1%).

    4. Discussion

    This study aimed to evaluate the temporal and

    amplitude parameters of neck muscle activation inassociation with rapid voluntary movement of the

    upper limb. With bilateral and unilateral upper limb

    movements in all directions, the SCM and CE musclesdemonstrated feed-forward activation (all relativelatencies

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    research [13,25,26]. Gurfinkel et al. [13] showed back-ward head acceleration 40:5 12:2 ms prior to unilat-eral upper limb flexion, which was associated withactivation of the splenius capitus and trapezius prior toactivation of the deltoid muscle. Although our resultsdid not demonstrate activation of neck muscles prior tothe onset of deltoid muscle, neck muscle activationoccurred within 50 ms of the deltoid onset indicatingthat their contraction cannot be reflexly mediated andmust be centrally initiated in a feed-forward manner[2,16]. Difficulty measuring the precise timing of EMGonsets and differences in the method of detecting EMG

    onsets is the most likely explanation for minor dissim-ilarities between results of different studies. Forexample, in the study conducted by Gurfinkel et al.[13], EMG onsets were determined by visual inspectionof the raw and rectified EMG signals, which precludesdirect comparison with our results.

    In addition to demonstrating feed-forward activationof neck muscles during unilateral upper limb flexion,the results of this study revealed the existence of feed-forward neck muscle activation with unilateral exten-sion, unilateral abduction and bilateral upper limbmovement in all three directions. Furthermore, the

    results highlight directional specificity of neck muscleactivation in response to moments imposed by the per-turbation. There is still uncertainty as to whether feed-forward neck muscle activity is contributing to stabilityof the neck or helping to control the position of thecentre of gravity. As suggested by Gurfinkel et al. [13],given that anticipatory postural movements measuredat the hip, ankle and knee serve to regulate position ofthe trunk, it seems unlikely neck muscle activity cancontribute substantially to minimise body movement.This hypothesis was substantiated by the results of vander Fits et al. [25] who demonstrated that position

    dependency of agonist activity was restricted to morecaudally located postural muscles. This suggests thatmuscles of the lower limb and trunk are especiallyinvolved in the maintenance of equilibrium, i.e. keepingthe centre of mass within the limits of the support sur-face. In contrast, neck muscle activation was inde-pendent of the starting position suggesting neck muscleactivity probably serves to oppose the reaction forcesinduced by arm movements[25].

    Interestingly, the results of our study demonstratedco-activation of the neck flexor and extensor musclesduring perturbations in all directions. Co-activation of

    Fig. 5. Normalised root mean square (nRMS) values (%) obtained for the sternocleidomastoid (SCM) and cervical extensors (CE) musclesduring left (L) and right (R) unilateral (U) and bilateral (B) upper limb flexion (FLE), extension (EXE) and abduction (ABD).

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    the cervical flexor and extensor muscles would seem

    essential to ensure adequate stabilisation of the head, a

    necessary function for vision. Since no analysis of head

    motion was involved in the current study, the extrapol-

    ation of our findings to head movement and the impli-

    cations for cervical stabilisation are potentially limited.

    However, in a previous study [25], 80% of subjects

    demonstrated less than 3v

    of head displacement with

    rapid upper limb flexion, which demonstrates minimal

    head movement with this type of postural perturbation.

    Feed-forward activation of neck muscles is most likely

    a mechanism employed to maintain stability of the ves-tibular system and visual field and offer protection tothe cervical spine, rather than acting as a compensationto the perturbation.

    4.1. Repeatability of EMG onsets and nRMS values

    Because of the low values of between-subject nSEM,results for the deltoid reaction times and relative laten-cies of the SCM and CE muscles, demonstratereliability that supports their use in clinical and

    Table 2Results of the Wilcoxon non-parametric matched paired test to detect differences in the normalised root mean square values obtained for the ster-nocleidomastoid (SCM) and cervical extensor (CE) muscles between bilateral (BI) and unilateral (UNI) rapid upper limb flexion (FLEX), abduc-tion (ABD) and extension (EXT) of the right (R) and left (L) arm. indicates significant difference p < 0:05, indicates significant differencep < 0:01. Refer toFig. 4for the normalised root mean square values obtained for the SCM and CE muscles during each condition

    BIFLEX BIABD BIEXT UNIFLEXR UNIFLEXL UNIABDR UNIABDL UNIEXTR UNIEXTL

    LSCMBIFLEX BIABD

    BIEXT UNIFLEXR

    UNIFLEXL

    UNIABDR UNIABDL UNIEXTR

    UNIEXTL

    RSCMBIFLEX

    BIABD

    BIEXT UNIFLEXR

    UNIFLEXL UNIABDR

    UNIABDL UNIEXTR

    UNIEXTL

    LCEBIFLEX

    BIABD BIEXT

    UNIFLEXRUNIFLEXL

    UNIABDRUNIABDL

    UNIEXTRUNIEXTL

    RCEBIFLEX BIABD

    BIEXT UNIFLEXR

    UNIFLEXLUNIABDR

    UNIABDLUNIEXTR

    UNIEXTL

    470 D. Falla et al. / Journal of Electromyography and Kinesiology 14 (2004) 463474

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    research evaluations. As previously documented[21,22], when the between-subject variability is compa-rable to (or less than) the within-subject variability, thedegree of repeatability defined by the ICC becomesmeaningless (very low or negative). The low valuesobtained in this study for both between- and within-subject nSEM for the deltoid reaction times and rela-tive latencies of the SCM and CE demonstrate thatthese variables could be estimated with very highrepeated measures precision. However, it also showsthat there was very little variation in the reaction timesand relative latencies obtained across subjects and

    trials, so the measure might not be able to detect differ-ences among uniform groups (such as asymptomaticsubjects). The EMG onsets of the SCM and CE mus-cles might therefore be best utilised in providing a ref-erence range for a uniform group of subjects (e.g.normative data).

    Several muscles displayed low estimates of the nSEMfor the nRMS values (seeTable 4), which are compara-ble with repeatability results of EMG amplitudeobtained from neck muscles during isometric con-ditions obtained in a previous protocol [10]. The lowestimates of the nSEM for the nRMS values offers

    Table 3Repeatability of deltoid (DELT) reaction times and relative latencies of the sternocleidomastoid (SCM) and cervical extensors (CE) during bilat-eral (BI) and unilateral (UNI) rapid upper limb flexion (FLEX), abduction (ABD) and extension (EXT). Intraclass correlation coefficient (ICC)reports variance due to subjects; variance contributions due to days and trials are reported from analysis of variance results. Normalised standarderror of the mean (nSEM) reports deviation within- and between-subjects

    Movement Muscle ICC Days Trials Within-subjectsnSEM

    Between-subjectsnSEM

    BIFLEX LSCM 29.6 43.4 27.0 3.7 3.8RSCM 31.6 40.6 27.8 4.0 4.1LCE 29.4 40.0 30.6 4.2 4.0RCE 39.7 31.9 28.4 5.0 5.5LDELT 23.8 44.5 31.7 4.6 4.0RDELT 24.9 38.7 36.4 4.4 3.8

    BIABD LSCM 36.9 14.8 48.3 5.1 4.7RSCM 24.7 13.5 61.8 4.8 3.7LCE 32.7 11.4 55.9 4.3 3.9RCE 30.1 17.3 52.6 4.9 4.1LDELT 28.6 17.0 54.4 5.6 4.6RDELT 30.1 6.8 63.1 5.3 4.4

    BIEXT LSCM 43.6 26.0 30.4 4.2 5.0RSCM 31.2 40.7 28.1 4.6 4.5LCE 40.1 24.2 35.7 3.8 4.2RCE 48.2 23.8 28.0 4.1 5.3LDELT 53.6 12.7 33.7 4.3 5.4RDELT 48.2 25.3 26.5 4.4 5.7

    UNIFLEXR LSCM 5.7 31.7 74.0 5.0 1.9RSCM 21.5 12.2 66.3 4.9 3.3RCE 38.2 6.8 55.0 4.3 4.0RDELT 25.0 12.5 62.5 4.9 3.6

    UNIFLEXL LSCM 9.2 12.6 78.2 4.3 2.3RSCM 18.7 27.0 54.3 4.3 3.2LCE 11.9 19.9 68.2 4.3 2.6LDELT 9.7 14.9 75.4 4.6 2.6

    UNIABDR LSCM 24.4 24.4 51.2 4.3 3.4RSCM 34.5 22.4 43.1 4.4 4.2RCE 27.9 24.4 47.7 4.6 3.8RDELT 38.4 11.5 50.1 4.3 4.1

    UNIABDL LSCM 45.5 6.0 60.5 4.7 5.2RSCM 46.3 10.4 43.3 4.7 4.9LCE 11.9 19.9 68.2 4.3 2.6LDELT 34.9 2.2 67.3 5.9 5.3

    UNIEXTR LSCM 16.4 36.1 47.5 4.4 3.4RSCM 33.2 20.4 46.4 4.5 4.1RCE 20.2 30.1 49.7 4.2 3.3RDELT 40.3 25.1 34.6 4.3 4.7

    UNIEXTL LSCM 38.3 1.9 59.8 4.2 4.0RSCM 30.0 6.0 64.0 4.9 4.0LCE 21.9 27.7 50.4 4.4 3.6LDELT 26.8 17.3 56.1 4.6 3.8

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    some support for their use in future clinical andresearch applications as providing a reference range for

    asymptomatic subjects. Further research is indicated to

    determine the utility of both EMG onsets and nRMS

    measures in demonstrating differences between asymp-

    tomatic and symptomatic subjects.

    5. Conclusion

    The results of this study provide a greater under-

    standing of cervical neuromotor control strategies and

    a reference framework to be used for comparison withsymptomatic subjects. During bilateral and unilateralupper limb perturbations, the SCM and CE musclesdemonstrate feed-forward activation. The temporalsequence and magnitude of this activation displayeddirectional specificity, however, the neck flexors andextensor muscles were co-activated during perturba-tions in all directions. It seems apparent that feed-for-ward activation of neck muscles is a mechanismnecessary to achieve head stability for the visual andvestibular systems, whilst ensuring stabilisation andprotection of the cervical spine.

    Table 4Repeatability of absolute root mean square values for the deltoid (DELT) muscles and normalised root mean square values for the sternocleido-mastoid (SCM) and cervical extensors (CE) during bilateral (BI) and unilateral (UNI) rapid upper limb flexion (FLEX), abduction (ABD) andextension (EXT)

    Movement Muscle ICC Days Trials Within-subjectsnSEM

    Between-subjectsnSEM

    BIFLEX LSCM 17.8 41.9 40.3 10.0 7.8RSCM 38.2 35.2 26.6 9.4 11.3LCE 47.5 19.7 32.8 8.5 10.8RCE 7.6 41.8 50.6 9.2 6.7LDELT 14.3 56.1 29.6 9.4 7.9RDELT 68.6 11.4 20.0 8.3 14.5

    BIABD LSCM 66.3 14.8 18.9 8.4 13.6RSCM 42.5 19.2 38.3 8.7 9.4LCE 54.5 26.4 19.1 9.1 12.2RCE 49.9 27.3 22.8 9.1 11.5LDELT 67.5 16.2 16.3 7.7 12.6RDELT 57.9 17.6 24.5 8.1 12.2

    BIEXT LSCM 57.3 23.9 18.8 8.5 12.6RSCM 51.9 11.8 36.3 8.2 10.6LCE 27.5 48.7 23.8 8.5 8.6RCE 24.9 39.3 35.8 9.0 7.6LDELT 13.0 85.7 27.3 13.9 6.6RDELT 16.3 68.3 15.4 10.8 10.2

    UNIFLEXR LSCM 57.0 22.2 20.8 9.4 15.2RSCM 31.5 20.1 38.4 9.9 11.2RCE 7.8 48.4 43.8 10.3 6.9RDELT 45.6 40.9 13.5 11.5 17.3

    UNIFLEXL LSCM 47.1 16.2 36.7 9.2 11.2RSCM 50.6 28.1 21.3 11.8 15.7LCE 23.1 35.6 41.3 9.1 7.1LDELT 38.4 12.2 49.4 9.4 8.9

    UNIABDR LSCM 81.5 2.0 20.5 7.7 16.5RSCM 39.6 18.5 41.9 9.4 10.1RCE 47.2 112.5 40.3 8.3 9.7RDELT 56.1 33.3 10.6 8.7 13.3

    UNIABDL LSCM 35.7 21.4 42.9 10.7 11.0RSCM 37.5 25.4 37.1 9.1 9.5LCE 21.4 46.4 32.2 9.9 9.2LDELT 65.1 21.8 13.1 8.7 13.6

    UNIEXTR LSCM 62.9 8.6 28.5 8.4 13.4RSCM 35.9 27.6 36.5 9.3 9.9RCE 45.6 16.0 38.4 1.0 8.5RDELT 19.5 51.4 29.1 13.3 15.9

    UNIEXTL LSCM 65.1 8.8 26.1 8.8 15.7RSCM 51.0 10.8 38.2 8.6 10.9LCE 25.6 28.6 45.8 8.1 7.7LDELT 36.9 39.8 23.3 10.8 13.5

    472 D. Falla et al. / Journal of Electromyography and Kinesiology 14 (2004) 463474

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    Acknowledgements

    The authors wish to thank A. Merlo and D. Farinafor providing the algorithms used for muscle activitydetection.

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    Deborah Falla received her Ph.D. in Physio-therapy from The University of Queensland,

    Australia in 2003. She is currently a researchofficer in the Cervical Spine and Whiplash

    Research Unit at The University of Queens-land. Her research focus involves the inte-

    gration of neurophysiological and clinicalresearch to evaluate the pathophysiology

    underlying muscle impairment in people witha history of neck pain. Her research also

    focuses on investigating the physiologicalmechanisms that underpin the efficacy of therapeutic exercise for the

    treatment of patients with neck pain.

    Alberto Rainoldi was born in Torino, Italy

    and graduated in Physics (1991) from Torino

    University. He obtained the Ph.D. in Physi-cal Medicine and Rehabilitation (2002) at

    the Faculty of Medicine, Universitadi RomaTor Vergata, Italy. Since 1996, he has

    been with the Laboratory for Neuromuscu-lar System Engineering and Motor Rehabili-

    tation at Politecnico di Torino, where hisresearch activity is focused on: the assess-

    ment of proper methodologies useful to

    increase the standardisation and the repeatability of EMG measures,allowing their clinical use; the feasibility study of a technique of mus-

    cle fiber type estimation based on surface EMG; the assessment of

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    EMG signal modification in different clinical pathologies. He is also ascientific consultant of the S. Maugeri Foundation (Pavia, Italy) forthe research projects in the field of muscle fatigue.

    Roberto Merletti graduated in ElectronicsEngineering from Politecnico di Torino,

    Italy, and obtained the M.S. and the Ph.D.in Biomedical Engineering from The OhioState University. Since 1984, he is AssociateProfessor of Biomedical Instrumentation atthe Department of Electronics of Politecnicodi Torino. From 1989 to 1994, he wasAssociate Professor at the Department ofBiomedical Engineering of Boston Universityand Research Associate at the Neuromuscu-

    lar Research Center of the same University. In 1996, he founded theLaboratory for Neuromuscular System Engineering at Politecnico di

    Torino, where he is currently Director. He is Coordinator of a pro-ject sponsored by the European Community and of a project spon-sored by the European Space Agency. His research focuses ondetection, processing and interpretation of surface EMG, on electri-cal stimulation and neuromuscular control.

    Gwendolen Jullis an Associate Professor and Head of the Division ofPhysiotherapy at The University of Queensland where she leads theCervical Spine and Whiplash Research Unit. Her particular researchand clinical interests are in establishing the pathophysiological pro-cesses involved in the pain and muscle systems of patients with neckdisorders, both of insidious and traumatic onset (whiplash), with thesubsequent development of research based physical therapy interven-tions. The research is also concerned with testing the efficacy of spe-cific exercise programs for the management of neck pain inrandomised controlled trials as well as investigating the physiologicalmechanisms of effect of therapeutic exercise for the cervico-brachialregion.

    474 D. Falla et al. / Journal of Electromyography and Kinesiology 14 (2004) 463474