Journal of Electromyography and Kinesiology 24 (2014) 72–77

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Journal of Electromyography and Kinesiology

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The effect of fatigued internal rotator and external rotator muscles of theshoulder on the shoulder position sense

1050-6411/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.jelekin.2013.10.008

⇑ Corresponding author. Address: West 17, South 1, Chuo-ku, Sapporo City, Japan.Tel.: +81 11 611 2111.

E-mail address: f-kaneko@sapmed.ac.jp (F. Kaneko).

Naoya Iida a,b, Fuminari Kaneko c,⇑, Nobuhiro Aoki c, Eriko Shibata a

a Graduate School of Health Sciences, Sapporo Medical University, Japanb Department of Rehabilitation, Hakodate Goryoukaku Hospital, Japanc Second Division of Physical Therapy, School of Health Science, Sapporo Medical University, Japan

a r t i c l e i n f o a b s t r a c t

Article history:Received 13 November 2012Received in revised form 14 September2013Accepted 15 October 2013

Keywords:Position senseMuscle fatigueShoulder joint rotation

The purpose of this study was to investigate which muscle group, the agonist or antagonist, contributesmost to the shoulder position sense (SPS). The SPS was tested under 2 conditions: fatigued shoulder inter-nal rotator (IR) muscles (pectoralis major and latissimus dorsi) and fatigued external rotator (ER) muscles(infraspinatus). In each condition, the SPS was measured before and after a fatiguing task involving the IRor ER muscles by repeating shoulder joint rotation. SPS was measured using a method in which subjectsreproduced a memorized shoulder joint rotation angle. The position error values in all conditions (fati-gued IR and ER muscles) and measurement periods (before- and after-fatigue task) were compared using2-way analysis of variance with repeated measures (IR/ER � before/after). Position error increased signif-icantly after both fatigue tasks (before- vs. after-fatigue: IR muscle, 2.68� vs. 4.19�; ER muscle, 2.32� vs.4.05�). In other words, SPS accuracy decreased when either the agonist or antagonist muscle was fati-gued. This finding indicated that SPS may be affected by an integrated information of the afferent signalsin the agonist and antagonist muscles.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Different receptors convey each somatosensory informationconsists of the pain, temperature, and tactile sensations as wellas conscious proprioception (Riemann and Lephert, 2002a,b). Rie-mann and Lephert (2002a,b) described that proprioception con-sisted of 3 submodalities (joint position sense, kinesthesia, andthe sense of tension). The position sense test measures the accu-racy of position replication and can be conducted actively (activeposition sense) or passively (passive position sense) in both openand closed kinetic chain positions (Riemann and Lephert, 2002a,b).

The mechanisms of the production of the position sense havebeen investigated using a tendon vibration and muscle fatigue inthe wrist and elbow joints. As the result of studies on a tendonvibration, it was indicated that joint position is determined bythe integration of afferent signals from the muscle spindles of 2antagonistic muscles (Figuière et al., 1999; Gilhodes et al., 1986).Furthermore, it was suggested that the position sense decreasedeven if the shortening muscle during the position sense measure-ment involved muscle fatigue (Allen et al., 2007, 2010; Allen and

Proske, 2006; Fortier et al., 2010; Walsh et al., 2004). Thus, thesestudies support the theory that the integration of afferent signalsfrom the muscle spindles of the 2 antagonistic muscles is impor-tant in the production of the position sense.

In the shoulder joint, when the internal and external rotatormuscles are concurrently fatigued, shoulder position sense (SPS)decreases (Myers et al., 1999; Voight et al., 1996). Moreover, mus-cle fatigue of shoulder horizontal flexion and extension leads toproprioceptive deficit of the shoulder joint (Björklund et al.,2000; Pedersen et al., 1999). However, it has not been clarifiedwhether fatigue of the agonist or the antagonist muscle has agreater effect on SPS. In the elbow joint, position sense accuracyis decreased even when the shortening muscle is fatigued duringposition sense measurement (Allen et al., 2007, 2010; Allen andProske, 2006; Fortier et al., 2010; Walsh et al., 2004); however,to our knowledge, no study of this kind has been performed forthe shoulder joint.

The purpose of this study was to investigate which musclegroup, the internal rotator or the external rotator, contributes mostto the position sense in the shoulder joint rotation using separatefatigue tasks for these muscles. We hypothesized that accuracyof the position sense of the shoulder is decreased like the elbowjoint even when the shortening muscle is fatigued during positionsense measurements.

N. Iida et al. / Journal of Electromyography and Kinesiology 24 (2014) 72–77 73

2. Methods

2.1. Subjects

Fifteen healthy male college students participated in thepresent study (mean age, 22.1 ± 3.4 years; mean height,174.4 ± 6.7 cm; mean body mass, 73.2 ± 11.9 kg). Subjects whohad a history of orthopedic or neurological problems, or playingoverhead sports were excluded from the study. Each subject’sdominant shoulder, the one used to throw the ball, was tested.All subjects provided written informed consent prior to participat-ing in the experiments, which were approved by the Sapporo Med-ical University Ethical Committee, and the study’s ethical aspectsconformed to the Declaration of Helsinki.

2.2. Instruments

An isokinetic dynamometer (Biodex System3; Biodex MedicalSystem, Inc., Shirley, NY, USA) was used for measuring of the SPS,fatigue confirmation and fatigue tasks. The long axis of each sub-ject’s humerus was matched to the rotation axis of the arm ofthe dynamometer. To eliminate the compensatory movementcaused by trunk flexion, extension and rotation, each subject’strunk was fixed to the chair with a belt (Fig. 1).

A 3-dimensional miniature and wireless motion capture device(i4 Motion; TECHNO CONCEPT, Inc., Mane, France) was used to cal-culate the angle of the shoulder joint rotation. Angle data (in de-grees) from the motion capture device were sampled at 100 Hzand stored on a personal computer. In the present study, the angleof the gradient of the forearm changes as the shoulder joint rotatessince the shoulder joint rotation was performed at 90� of abduc-tion. Therefore, the motion capture device was attached to the dis-tal and dorsal aspects of the forearm with a belt. The angle of thegradient of the forearm, which was calculated using the motioncapture device, was defined as the angle of the shoulder joint rota-tion in the present study. To eliminate the pronation and supina-tion movement of the forearm, the distal and ventral aspects ofthe forearm and palm were placed on a board attached to thearm of the dynamometer and fixed to the board with a belt (Fig. 1).

A surface electromyography (EMG) system (EMG TelemeterSystem; Harada Electronics Industry Ltd., Sapporo, Japan) was usedto obtain EMG data in the fatigue confirmation task. For the inter-nal rotator muscles, the surface EMG electrodes were placed at thepectoralis major muscle (PM) and the latissimus dorsi muscle (LD).For the external rotator muscles, the electrode was placed at theinfraspinatus muscle (ISP). Electrode placement was made as pre-viously published (Kelly et al., 1996; Paton and Brown, 1994). Thesignals were recorded using surface Ag/AgCl electrodes (10 mm indiameter) at an interelectrode distance of 20 mm.

dynamometer

motion capture device

Fig. 1. The SPS, fatigue confirmation task, and fatigue task were measured in thesitting position with the shoulder positioned at 90� of abduction and the elbowpositioned at 90� of flexion. Each subject performed internal and external rotationof the shoulder joint in that posture.

2.3. Procedures

2.3.1. Experimental protocolEach subject’s SPS was tested under 2 conditions: fatigued

shoulder internal rotator muscles and fatigued shoulder externalrotator muscles. Measurements under each condition were con-ducted 1 week apart. The 15 subjects were randomly divided into2 groups: those who previously had fatigued shoulder internalmuscles and those who had previously had fatigued shoulderexternal muscles. In each condition, the shoulder range of motion(ROM) was measured first, followed by SPS. Subsequently, the fati-gue confirmation task of the shoulder rotator muscles (internal orexternal) was performed. After the fatigue confirmation task wascompleted, a shoulder fatigue task was performed, and the SPSwas measured again.

2.3.2. Measurement of ROMPassive ROM was measured using the motion capture device for

the shoulder joint rotation to define the target angle and the start-ing angle. The target angle was defined as the angle halfway be-tween full internal rotation and full external rotation. Thestarting angle was defined as the angle halfway between the mid-dle of the target angle and full internal rotation (Fig. 2).

2.3.3. Measurement of position senseSPS was measured with each subject in the sitting position with

the shoulder positioned at 90� of abduction and the elbow posi-tioned at 90� of flexion (Fig. 1). To eliminate visual and auditorycues, the subjects kept their eyes closed and wore earplugs. SPSwas measured in the present study by the method in which sub-jects actively (active positioning task) or passively (passive posi-tioning task) reproduce a memorized angle of the shoulder jointrotation.

In the active positioning task, all movements were active. Theisokinetic mode of the dynamometer at 5�/s was used. Before eachmeasurement, each subject performed an isokinetic rotation of theshoulder joint using the dynamometer for a few minutes as awarm-up exercise. The subject then actively performed externalrotation of the shoulder from the starting angle to the target angleand actively maintained the target angle for 3 s. During this period,the subject attempted to memorize the target angle. After that, thesubject internally rotated his shoulder to the starting angle. Thesubject then actively reproduced the target angle. When the sub-ject perceived that he had reached the target angle, he pushedthe stop button and stopped moving the arm of the dynamometer.The angle at which the arm was stopped was defined as the repro-duced angle. This measurement was performed five times. More-over, we confirmed using EMG that the ISP activated and the PMand LD were not activated during the active positioning task.

full external rotation

full internal rotation

The target angle (the angle halfway between full internal rotation and full external rotation)

The starting angle (the angle halfway between the middle and full internal rotation)

Fig. 2. The target angle was defined as the angle halfway between the full internalrotation and the full external rotation. The starting angle was defined as the anglehalfway between the middle of the target angle and the full internal rotation.

74 N. Iida et al. / Journal of Electromyography and Kinesiology 24 (2014) 72–77

In the passive positioning task, all movements were passive.The passive mode of the dynamometer (5�/s) was used. The proce-dures of the passive positioning task were almost the same asthose of the active positioning task. First, the shoulder of thesubject was externally rotated from the starting angle to the targetangle, and the subject passively maintained the target angle for 3 s.The subject’s shoulder was then internally rotated to the startingangle. The subject then passively reproduced the target angle. Fur-thermore, we confirmed using EMG that the ISP, PM and LD werenot activated during the passive positioning task.

2.3.4. Fatigue confirmation taskTo confirm the presence of muscle fatigue, the fatigue confirma-

tion task was performed using the dynamometer and EMG. First,the peak torque (PT) of the shoulder rotation during maximal vol-untary isometric contraction (MVIC) was measured at the targetangle with the subject in the sitting position with the shoulderpositioned at 90� of abduction and the elbow positioned at 90� offlexion. Subsequently, the EMG data during the performance of50% of the PT before the fatigue task were recorded for 3 s whilevisually confirming the torque output by watching the liquid crys-tal display of the Biodex (the 50% PT task). At the same time as wevisually confirmed that the subjects output the target torque, westarted recording the EMG. Each measurement was performed induplicate.

2.3.5. Fatigue taskThe isokinetic mode of the dynamometer (180�/s) was used in

the fatigue task. Subjects were seated in the Biodex with the shoul-der positioned at 90� of abduction and the elbow positioned at 90�of flexion. In the condition of ‘‘fatigued shoulder internal rotatormuscles,’’ the subject performed a concentric contraction of inter-nal rotation from the angle halfway of total shoulder joint rotationto full internal rotation at maximal effort.

As previously described (Myers et al., 1999; Voight et al., 1996),the isokinetic peak torque of internal rotation was determined be-fore the fatigue task, and the subject exercised until the isokinetictorque decreased three times in a row by 40% of the peak torque.The fatigue task was then discontinued. The subject was not in-structed to voluntarily contract the external rotator muscles, andthe tester returned the arm to the angle halfway of total shoulderjoint rotation because the internal rotator muscles had becomeselectively fatigued. In the condition of ‘‘fatigued shoulder externalrotator muscles,’’ the subject performed a concentric contraction ofexternal rotation from the angle halfway of total shoulder jointrotation to full external rotation at maximal effort until the torqueof external rotation decreased three times in a row by 40% of thepeak torque. The subject was not instructed to voluntarily contractthe internal rotator muscles, and the tester returned the arm to theangle halfway of total shoulder joint rotation because the externalrotator muscles had become selectively fatigued.

2.4. Assessment parameters

To evaluate the direction and magnitude of the position error,the following parameters were calculated: (1) the constant errorof the joint angle (defined as the reproduced angle minus thememorized angle) and (2) the absolute error of the joint angle (de-fined as the absolute difference between the memorized angle andthe reproduced angle). To minimize parameters variability, themaximum and minimum values obtained in the five trials were ex-cluded from the analysis. The mean value of the remaining threetrials was used for the statistical analysis.

To assess the presence of muscle fatigue, the median power fre-quency (MDF) and the integrated EMG (IEMG) during the 50% PTtask was calculated. It has generally been found that the EMG

frequency decreases after sustained muscular contraction so thatthe MDF decreases (Gerdle and Elert, 1994; Komi and Tesch,1979). Signals from the surface EMG were sampled at 1000 Hzand stored on a personal computer. All of the EMG signals wereprocessed offline using custom software (Labview 8.6; NationalInstruments Corp., Austin, TX, USA). The EMG data were band-passfiltered from 10 to 500 Hz through a 4th-order Butterworth filterand full-wave rectified. The signals collected within the first andlast second of each 3 s isometric contraction was not used for anal-ysis. Therefore, the middle 1 s window of 3 s of EMG signals wasused for analysis. A power spectral analysis was performed onthe 1 s window for each muscle. A Fast Fourier Transformation of1000 points (Hanning window processing) was performed for each1 s contraction and the MDF was determined. The MDF was calcu-lated by the following formula.Z MDF

0Pðf Þdf ¼

Z 1

MDFPðf Þdf

Moreover, the IEMG during the 50% task was standardized forthe IEMG during MVIC before the fatigue task as 100%. For thePT, the larger value of 2 trials was used for the statistical analysis.For the MDF and the IEMG during the 50% PT task, the mean valueof two trials was used for the statistical analysis.

2.5. Statistical analysis

All data were analyzed with statistical software (SPSS; SPSS Inc.,Chicago, IL, USA). The PT, MDF, IEMG, constant error and absoluteerror in all conditions (fatigued internal rotator muscles, fatiguedexternal rotator muscles) and measurement periods (before andafter the fatigue task) were compared using 2-way analysis of var-iance (ANOVA) with repeated measures (internal rotator muscles/external rotator muscles � before/after). If there was an interactionbetween condition and measurement period, a simple main effecttest was used. The level of significance was set at p < 0.05.

3. Results

3.1. PT, MDF and IEMG

The ANOVA results showed significant interactions of the PT(internal rotation: F = 12.107, p = 0.004; external rotation:F = 14.051, p = 0.001), MDF (PM: F = 33.509, p < 0.0005; LD: F =30.977, p < 0.0005; ISP: F = 10.666, p = 0.006) and IEMG (PM:F = 12.047, p = 0.004; LD: F = 7.367, p = 0.018; ISP: F = 8.197,p = 0.013) between the conditions and measurement periods. Posthoc test revealed that the PT of the internal rotation (p = 0.001), theMDF of the PM (p < 0.0005) and LD (p < 0.0005) significantly de-creased only after the fatigue task for the internal rotator muscles,and the PT of the external rotation (p < 0.0005) and the MDF of theISP (p = 0.002) significantly decreased only after the fatigue task forthe external rotator muscles (Table 1). Furthermore, post hoc testshowed the IEMG of the PM (p < 0.0005) and LD (p = 0.002) signif-icantly increased only after the fatigue task for the internal rotatormuscles, and the IEMG of the ISP (p = 0.002) significantly increasedonly after the fatigue task for the external rotator muscles (Table 1).Therefore, the PT and each EMG data indicated that internal rotatormuscles fatigued only after the fatigue task for the internal rotatormuscle, and external rotator muscles fatigued only after the fatiguetask for the external rotator muscles.

3.2. Position sense

The ANOVA results showed significant interactions of theconstant error in the active (F = 10.063, p = 0.007, g2 = 0.436) and

Table 1PT (in Nm [Mean ± SD]), MDF (in Hz [Mean ± SD]) and IEMG (in% [Mean ± SD]).

Before the fatigue taskof the IR muscle

After the fatigue taskof the IR muscle

Before the fatigue taskof the ER muscle

After the fatigue taskof the ER muscle

PT of the IR 36.4 ± 9.5 29.5 ± 7.4a 34.7 ± 10.1 36.0 ± 9.9PT of the ER 27.6 ± 5.3 27.1 ± 6.8 27.9 ± 6.1 22.8 ± 6.5b

MDF of the PM 51.2 ± 10.4 45.4 ± 10.1a 48.8 ± 12.5 51.1 ± 14.0MDF of the LD 55.6 ± 10.0 49.7 ± 11.8a 48.0 ± 7.3 50.0 ± 8.2MDF of the ISP 80.9 ± 28.2 80.6 ± 24.3 84.8 ± 26.4 73.8 ± 23.6b

IEMG of the PM 40.8 ± 15.6 62.5 ± 18.8c 36.2 ± 15.5 39.9 ± 16.2IEMG of the LD 33.4 ± 10.2 48.4 ± 18.1c 26.1 ± 12.4 26.5 ± 13.3IEMG of the ISP 46.5 ± 17.7 48.3 ± 16.1 43.7 ± 11.5 54.3 ± 14.7d

PT, peak torque; IR, internal rotation; ER, external rotation; MDF, median power frequency; IEMG, integrated electromyography; PM, pectoralis major muscle; LD, latissimusdorsi muscle; ISP, infraspinatus muscle.

a Significantly lower than the value before the fatigue task of the IR muscle.b Significantly lower than the value before the fatigue task of the ER muscle.c Significantly higher than the value before the fatigue task of the IR muscle.d Significantly higher than the value before the fatigue task of the ER muscle.

Con

stan

t erro

r (de

g)IR

ER

IRER

: p < 0.01

: p < 0.05

*

*

**

*

*

*

IR muscle

ER muscle

Before the fatigue task

After the fatigue task

Con

stan

t erro

r (de

g)

Before the fatigue task

After the fatigue task

Active positioning task Passive positioning task

: p < 0.05IR muscle

ER muscle* *

**

Fig. 3. IR, internal rotation; ER, external rotation. Constant error (mean ± SD) of the position sense before and after the fatigue task of the IR muscle (continuous line) and ERmuscle (dashed line).

Abso

lute

erro

r (de

g)

*

Before the fatigue task

After the fatigue task

Active positioning task**

Abso

lute

erro

r (de

g)

Before the fatigue task

After the fatigue task

Passive positioning task

IR muscle

ER muscle

IR muscle

ER muscle* : p < 0.05 : p < 0.01**

Fig. 4. IR, internal rotation; ER, external rotation. Absolute error (mean ± SD) of the position sense before and after the fatigue task of the IR muscle (continuous line) and ERmuscle (dashed line).

N. Iida et al. / Journal of Electromyography and Kinesiology 24 (2014) 72–77 75

passive (F = 9.616, p = 0.008, g2 = 0.425) positioning tasks betweenconditions and measurement periods (Fig. 3). In both the activeand passive positioning tasks, a post hoc test revealed the constanterror significantly increased in the direction of the external rota-tion after the fatigue task for the internal rotator muscles (active:p = 0.034, g2 = 0.302; passive: p = 0.014, g2 = 0.384). Moreover, posthoc test showed that the constant error increased significantly inthe direction of the internal rotation after the fatigue task for theexternal rotator muscles (active: p = 0.046, g2 = 0.272; passive:p = 0.046, g2 = 0.273).

ANOVA revealed that there was no significant interaction of theabsolute error in the active (F = 0.035, p = 0.855) or passive(F = 0.604, p = 0.451) positioning tasks between conditions andmeasurement periods (Fig. 4). However, there was a significantmain effect between measurement periods in which the absolute

error increased significantly after the fatigue task in both the active(F = 7.120, p = 0.019, g2 = 0.354) and passive (F = 40.868, p < 0.0005,g2 = 0.759) positioning tasks. In other words, the accuracy of theSPS decreased when either the internal rotator or the external rota-tor muscle was fatigued. Therefore, it was indicated that both theagonist and antagonist muscle contribute to the SPS.

4. Discussion

In the present study, the fatigue confirmation task was per-formed to objectively confirm the presence of muscle fatigue,and it was revealed that the targeted muscle was selectivelyfatigued. It has generally been found that the EMG frequencydecreases after sustained muscular contraction, so that the MDF

76 N. Iida et al. / Journal of Electromyography and Kinesiology 24 (2014) 72–77

decreases (Gerdle and Elert, 1994; Komi and Tesch, 1979). The PTof the internal rotation and the MDF of the PM and LD decreasedafter the fatigue task for the internal rotator muscles, and the PTof the external rotation and the MDF of the ISP decreased afterthe fatigue task for the external rotator muscles. Moreover theIEMG of the PM and LD increased after the fatigue task for theinternal rotator muscles, and the IEMG of the ISP increased afterthe fatigue task for the external rotator muscles. However, no alter-ation of the PT of the internal rotation and each EMG data of thePM and LD was observed before and after the fatigue task for theexternal rotator muscles, while no alteration of the PT of the exter-nal rotation and each EMG data of the ISP was observed before andafter the fatigue task for the internal rotator muscles. Therefore,the results of the present study show that the internal rotator mus-cles were fatigued only after the fatigue task for internal rotatormuscles, and the external rotator muscles were fatigued only afterthe fatigue task for external rotator muscles. In other word, theinternal and external rotator muscles were selectively fatiguedafter the fatigue task in which the muscle group was targeted.

In the elbow joint, position sense accuracy has been shown todecrease even when the shortening muscle during position sensemeasurement was fatigued (Allen et al., 2007, 2010; Allen andProske, 2006; Fortier et al., 2010; Walsh et al., 2004). Our impor-tant findings here show that, in contrast, when the shorteningmuscle during the position sense measurement in the shoulderjoint was fatigued, position sense accuracy decreased. Since posi-tion sense was measured during external rotation in the presentstudy, the external rotator muscles were the shortening muscleand the internal rotator muscles were the extending muscle duringposition sense measurement. If the joint position was perceivedonly on the basis of the muscle spindles that were extended duringthe joint movement, the position sense accuracy would not de-crease after external rotator fatigue. However, when the externalrotator muscles, which were shortened during the position sensemeasurements, were fatigued, the absolute error increased. Rolland Vedel (1982) reported that when a single muscle group was vi-brated, a kinesthetic illusion was induced in which the subjectsperceived lengthening of the vibrated muscle. Vibrating the same2 antagonistic muscles at different frequencies induced a kines-thetic illusion in the direction of a movement lengthening the mus-cle that was vibrated at the higher frequency (Figuière et al., 1999;Gilhodes et al., 1986). These reports suggest that joint position isdetermined by the integration of afferent signals from the musclespindles of 2 antagonistic muscles. In other words, it was indicatedthat not only extending muscle but also shortening muscle duringthe position sense measurement affects the position sense. In thepresent study, position sense accuracy decreased in the shoulderjoint when the shortening muscle was fatigued during the positionsense measurement. On the basis of above studies using a tendonvibration, the present results using a fatigue task indicated thatthe joint position of the shoulder was perceived as the result ofthe integration of afferent signals from the muscle spindles of 2antagonistic muscles.

Moreover, the constant error increased in the direction of exter-nal rotation after the fatigue task for the internal rotator muscles.In the case of external rotator muscle fatigue, the constant error in-creased in the direction of internal rotation. In other words, posi-tion error increased in the direction that fatigued muscle wasmore extended than before the muscle fatigue. On the basis ofthe theory that joint position was perceived as the result of theintegration of afferent signals from the muscle spindles of 2 antag-onistic muscles, the current results are reasonable when wehypothesize that the impulse of the muscle spindles decrease thanbefore the muscle fatigue. In the case of the external rotator musclefatigue, if the muscle fatigue decreased the muscle spindle im-pulse, the muscle spindle impulse of the external rotator muscle

decrease, while there is no change of the muscle spindle impulseof the internal rotator muscle. Thus, as the result of the integrationof afferent signals from the muscle spindles of two antagonisticmuscles, the subjects may misunderstand that external rotatormuscles do not extend more than before fatigue at the target angle.Then, the subjects may attempt to internally rotate their shoulderjoint. Therefore, the constant error increased in the direction ofinternal rotation after the fatigue task for the external rotator mus-cles. However, the effect of muscle fatigue on the sensitivity of themuscle spindles was not clarified in previous studies. Several stud-ies indicated that the muscle spindle impulses decrease after themuscle fatigue (Fukami, 1988; Nelson and Hutton, 1985). On theother hand, Fischer and Schafer (2005) suggested that the musclespindle impulses increase after the muscle fatigue. In the presentstudy, when it was hypothesized that the muscle spindle impulsesof the targeted muscles decreases after the muscle fatigue, the rea-son for the current result was consistently elucidated. However,this discussion is a matter of speculation because we did not mea-sure muscle spindle impulses.

The limitation of present study was as follows. It is impossibleto confirm the fatigue of all muscles that were activated duringthe shoulder joint rotation, although many muscles contribute toshoulder joint rotation. A wire electrode should be used to assessthe activation of the subscaplaris, teres minor and supraspinatus.However, such invasive intervention may cause muscle pain andaffect position sense. Therefore, we did not use the wire electrode;rather, we confirmed the fatigue of as many as possible muscles byusing the surface electrodes. Furthermore, we did not confirm theactivity of the accessory muscle of the shoulder joint rotation. Inthe trunk muscle, substitution of muscle has known during fatiguefrom low back exercise (Ng et al., 2003). Such phenomenon mayoccur also in shoulder joint. Therefore, accessory muscle integra-tion may contribute to SPS more heavily after the muscle fatigue.Finally, EMG and kinematics data were not perfectly synchronizedin the present study. Thus, there may be small time lag betweencorrect window during performance of targeted torque and ana-lyzed window. It was known that a reaction time to visual stimulustakes about 200 milliseconds in healthy subjects (Ando et al., 2009;Kaneko et al., 2002). Therefore, there may be the time lag for about200 ms from visual confirming of torque output to starting a recordof EMG in the present study. However, the signals collected withinthe first and last second of each 3 s isometric contraction was notused, and the middle 1 s window of 3 s of EMG signals was used foranalysis in the present study. Therefore, such small time lag willnot become a big problem for the current results. It is a fact thatthere are several important limitations in the present study. How-ever, the current results clarified that SPS during the shoulderexternal rotation was affected when either the agonist or antago-nist muscle was fatigued.

5. Conclusion

We observed here that position sense accuracy decreased in theshoulder joint when either the agonist or antagonist muscle duringthe position sense measurement was fatigued. This finding possi-bly indicated that the position of the shoulder joint was perceivedas a result of the integration of afferent signals from the musclespindles of 2 antagonistic muscles.

Conflict of interest

None declared.

N. Iida et al. / Journal of Electromyography and Kinesiology 24 (2014) 72–77 77

Acknowledgment

We thank all of the volunteers who participated in the project.This work was supported by a Grant-in-Aid for Scientific ResearchB (23300202).

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Naoya Iida received the PT from Sapporo Medical Uni-versity, Japan in 2010, and the MS degree in physicaltherapy science from Graduate School of Health Sci-ences, Sapporo Medical University, Japan in 2012. Hecurrently works as the PT at Hakodate GoryoukakuHospital, Japan. His major research interests focus onthe relationship muscle fatigue and proprioception inthe shoulder joint.

Fuminari Kaneko received his PT from Sapporo Medi-cal University, Japan in 1992, and PhD degree in healthscience from Graduate School of Medical Sciences,Hiroshima University, Japan in 2001. He worked asvisiting research fellow at NeuroMuscular ResearchCenter, Boston University, USA in 2001. Since 2001 hehad worked as scientific researcher in National Instituteof Advanced industrial Science and Technology, andcurrently he has been associate professor and chair-person of Sensorimotor Science and Sports Neurosci-ence Laboratory in Sapporo Medical University, Japan.Since 2010 to 2011, he worked as visiting researcher atPerception et controle du mouvement humain Labora-

toire de Neuroscience Integrative et Adaptative, Universite de Provence, France. Hismain research interest is the neuroscientific study on sensorimotor system anddevelopment of rehabilitation intervention based on neuroscience research.

Nobuhiro Aoki received the PT from Ibaraki PrefecturalUniversity of Health Sciences, Japan in 2004, and the MSdegree in physical therapy science from GraduateSchool of Health Sciences, Ibaraki Prefectural Universityof Health Sciences, Japan in 2009. He is currentlyassistant professor of Second Division of Physical Ther-apy in School of Health Science, Sapporo Medical Uni-versity, Japan. His main interest is electromyographicanalysis of function of hamstrings.

Eriko Shibata received PT from Sapporo Medical Uni-versity, Japan in 2008, and the MS degree in physicaltherapy science from Graduate School of Health Sci-ences, Sapporo Medical University, Japan in 2010. She iscurrently a PhD-student at the Sensorimotor Scienceand Sports Neuroscience Laboratory, Sapporo MedicalUniversity, Japan. She currently works as the PT atShinoro Orthopedic Hospital, Japan. Her main interest iskinesthetic perception by tendon vibration.