1996;497;291-298 J. Physiol. S P Magnusson, E B Simonsen, P Aagaard, H Sørensen and M Kjaer A mechanism for altered flexibility in human skeletal muscle. This information is current as of July 15, 2008 after publication unless article is open access. This version of the article may not be posted on a public website for 12 months http://jp.physoc.org/cgi/content/abstract/497/Pt_1/291 This is the final published version of this article; it is available at: [email protected]of Blackwell Publishing: permission 12 months after publication. No part of this article may be reproduced without the articles are free The Journal of Physiology Online . http://jp.physoc.org/subscriptions/ go to: The Journal of Physiology Online been published continuously since 1878. To subscribe to is the official journal of The Physiological Society. It has The Journal of Physiology Online
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1996;497;291-298 J. Physiol.
S P Magnusson, E B Simonsen, P Aagaard, H Sørensen and M Kjaer
A mechanism for altered flexibility in human skeletal muscle.
This information is current as of July 15, 2008
after publication unless article is open access. This version of the article may not be posted on a public website for 12 months
This is the final published version of this article; it is available at:
[email protected] Blackwell Publishing: permission12 months after publication. No part of this article may be reproduced without the
articles are freeThe Journal of Physiology Online. http://jp.physoc.org/subscriptions/go to: The Journal of Physiology Onlinebeen published continuously since 1878. To subscribe to
is the official journal of The Physiological Society. It hasThe Journal of Physiology Online
A mechanism for altered flexibility in human skeletal muscle
S. Peter Magnusson, Erik B. Simonsen, Per Aagaard, Henrik S0rensenand Michael Kjaer
Team Danmark Test Center, Copenhagen Muscle Research Center, Universityof Copenhagen, Rigshospitalet Afsnit 2001, Blegdamsvej 9, 2100 Copenhagen, Denmark
1. We investigated the effect of a long-term stretching regimen on the tissue properties andstretch tolerance of human skeletal muscle.
2. Resistance to stretch was measured as torque (in N m) offered by the hamstring musclegroup during passive knee extension while electromyographic (EMG) activity, knee jointangle and velocity were continuously monitored during a standardized stretch manoeuvre.
Seven healthy subjects were tested before and after a 3 week training period using twoseparate protocols. Protocol 1 consisted of a slow stretch at 0 087 rad s-' to a predeterminedangle followed by a 90 s holding phase. Subjects were brought to the same angle before andafter the training period. Protocol 2 was a similar stretch, but continued to the point of pain.
3. During protocol 1 the torque rose during the stretch and then declined during the holdingphase. EMG activity was small and did not change significantly during the protocol. Nosignificant differences in stiffness, energy and peak torque about the knee joint were seen as
a result of the training. During protocol 2 the angle to which the knee could be extended wassignificantly increased as a result of the training. This was accompanied by a comparableincrease in peak torque and energy. EMG activity was small and not affected by training.
4. It is concluded that reflex EMG activity does not limit the range of movement during slowstretches and that the increased range of motion achieved from training is a consequence ofincreased stretch tolerance on the part of the subject rather than a change in the mechanicalor viscoelastic properties of the muscle.
The stretching of human skeletal muscle to augment therange of motion of joints is commonly applied in diverseareas of medicine and recreational activities. However, themechanism for the acute and chronic changes in joint rangeof motion remains ambiguous. The acute response tostretching has been attributed to both neurophysiologicaland mechanical factors (Taylor, Dalton, Seaber & Garrett,1990; Hutton, 1993). The neurophysiological explanationsuggests the limiting factor during stretching to bemuscular resistance secondary to reflex activity (Hutton,1993). Accordingly, the aim of stretching is to inhibit thereflex activity, which reduces resistance and therebyimproves joint range of motion (Hutton, 1993), butparadoxically, the techniques most effective in acutelyincreasing joint range of motion have been associated withan elevated EMG response (Moore & Hutton, 1980;Osternig, Robertson, Troxel & Hansen, 1987). Alternativelyit has recently been proposed that acute adaptation may beattributed to an amplified stretch tolerance rather than achange in EMG activity (Magnusson, Simonssen, Aagaard,Dhyre-Poulson, MIcHugh & Kjaer, 1996a).
A third explanation for the acute effects of stretching is achange in the mechanical properties of the muscle (Tayloret al. 1990). Biological materials under tension exhibitviscoelastic behaviour and animal data have providedevidence that the muscle-tendon unit displays viscoelasticbehaviour both during the loading and holding phases of astretch (Abbott & Lowy, 1956; Taylor et al. 1990). Humanmodels have shown that a chronic regimen of stretchingmay increase joint range of motion (Sady, Wortman &Blanke, 1982; Gajdosik, 1991; Bandy & Irion, 1994). Thesuggested mechanism for this augmented joint range ofmotion is a change in the tissue properties of the muscle(Gajdosik, 1991; Hutton, 1993). The development of a newtechnique allows for the continuous and synchronousmonitoring of joint angle, velocity, muscle EMG responseand passive resistance to stretch of the human hamstringmuscle during the stretch and holding phase of a stretch(Magnusson, Simonsen, Aagaard, Gleim, McHugh & Kjaer,1995). The purpose of the present study was to investigateif tissue properties and stretch tolerance changed as a resultof a long-term stretching regimen in a human model usingthis measurement technique.
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METHODSSubjectsSe-en femnale subjects v-olunteered to participate. The mean + s.i.
for the age, body mnass and heiglht was 26-0 + 6-0 years,59-1 + 5-1 kg and t*70 + 0-10 m, respectively. The subjects were
free of any lower extremnity or lower back pathology. The subjectsdid not participate in any organized sporting activities and onlyoccasionally participated in recreational sports. None of the subjectshad performed any slpecific stretching regimen of the hamstringmuscle group prior to enitering the study. The study was approvedlbv the local Ethics Coimmittee and informed consent was obtainedfrom the subjects.
Measurement techniqueResistance to stretch was definedl as the passive torque (N m)offered by the hamiistr ing muscle group during passive kneeextension using a KinCoom dynamomneter (Kinetic Communicator,Chattecx Corp., Chattanooga, TN, USA) writh a modified thiglh pad(Fig. 1). All measurements of passive torque were gravity coriected(AIagnusson et al. 1995). Subjects were seated with the trunkperpendicular to the seat for the stIretch procedure. The thighrested on a specially constructed thigh pad elevating it to between0 524 and 0-785 i-ad (range) from horizontal. The trunk and thighposition disallow-ed subjects to reachi complete knee extension.Consequently, the position of the subject during the stretchmanoeuvre placed tension primarily on the mnuscle-tendon unitwithout invol-ement of posterior capsular constraints about theknee. Passive force (N) was detected by the load cell of thedynamometer, hich was calibrated prior to the experiment(10-750 N). The dynamometer and knee joint axis were alignedand the torque about the knee joint was calculated by multiplyingthe measured force by the lever arm distance. The lever arInattachment w,as placecl 2 cm proximal to the lateral malleolus. Thedistal thigh and pelxis xx-ere firmly secured with straps in an
attempt to minimize joint movement during the stretch manoeuvre.
The load cell was calibrated -ith 98 N load to ensure that stressrelaxation of the load cell did not occur. No stress relaxationoccurred over 90 s ancl w\hen manuallY unloaded the load cellreturned from 98 N to baseline (0 N) in < 0-2 s. Reliability of themethod has been deinonstrated; it y-ields a correlation coefficient ofr = 099 with a coefficient of variation of 6-5% -with respect topassive torque (Mlagnusson et al. 1995).
GIross electrical activity of the human hamstring muscle group wrasimleasured withi Ag-AgCl surface electrodes (MIedicotest, TypeN-10-A, Denmark) placed midw-ay between the gluteal fold andthe knee joint (AIcHugh et al. 1992), with a 3 cm inter-electrodeclistance. Custom-macle amplifiers with a frequencyT response ofbetween 20 and 10 kHz and 1 : 1 preamplifiers were used for EMGsignal sampling. The mean EMG signal was full-wave rectified andintegrated (time constant, 200 ms) (Basmajian & DeLuca, 1985).
Protocol 1Protocol 1 was adiministered to determine if tissue changes resultedfrom the stretching regimen. It consisted of a stretch phase to apredetermined final angle followed by a 90 s holding phase. Thefinal angle during the stretch manoeuv,re was determined bypassively extending the knee to an angle which provoked asensation of tightness in the posterior thiglh similar to a hold stretchmanoeuvre. Care was taken to avoid a painful response duringdetermination of the final angle. The leg was then immediatelyreturned to the starting position. The final angle was determinedfor the left and right side separately on the first test day. The samefinal angle was used for the pre- and post-training stretchmanoeuvre. During protocol 1, the dynamometer was programmedto extend the knee passively at 0-087 rad s-' from the startingpoint of 1-222 rad below horizontal to the final angle (stretch phase)where it remained for 90 s (holding phase) (Fig. 2). Throughout thestretch manoeuvre, subjects were requested to relax completely andnot offer any voluntary resistance. After 90 s in the holding phase,subjects were requested to produce a maximal voluntary contraction(MAVNC) effort with the hamstring muscle to produce a flexion torque.This yielded an EAMG and torque response which could be comparedwith that during the holding phase of the stretch manoeuvre.
Protocol 2Protocol 2 was administered to determine the stretch tolerance. Forthis part of the data collection, subjects wsere requested to closetlheir eyes. The dynamometer extended the knee passively at0 087 rad s-' from the starting point of 1-222 rad below horizontalto the onset of pain, at which point the subjects were instructed topress a switch which instantaneously stopped the lever arm; theleg was immediately returned the starting position. Subjects werethoroughly instructed in this manoeuvre and were allow-ed to trythe procedure to a point below the pain threshold prior to datacollection. In addition, one test trial was performed prior to datacollection. Throughout the stretch manoeuvre subjects wererequested to relax completely and not offer any voluntary resistance.
gure 1. Test position for stretch manoeuvreplatforim for distal thigh; 2, thigh strap; 3, pel-ic strap;KinCom ankle attachment with load cell.
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Humani muscX
Training regimenThe subjects were ranclomily assigned to stretchl the hamstr ingmuscle group on one leg while the opposite side served as a control.Two sessions, one in the morning and one in the afternoon, were
performed on a daily basis for 20 consecutixe days. Each session
consisted of fix-e stretches for 45 s with a 15-30 s rest in between.
The total stretch stimulus was 9000 s, which to our knowledgeexceedecl any previously published study. The stretch manoeuvre
was performed in the seated position with the stretch leg in a
straight position in fiont of the subject and the hip in neutralrotation. The control leg was flexed at the knee andchip ancl slightly
abducted to ensure that the hamstring muscle group wsas not undeltension. Subjects w-ere requested to lean forwarcl with a straightback to a point where the} experienced a 'stietch' sensation wthiclhwas subsequently maintained for 45 s. Previous research has shownthat a 45 s stretch in this position acutely vields a 29% stressrelaxation (Magnusson et at. 1995). The subjects filled out a form on
a daily basis to register compliance. They were instructed not toinitiate any new formns of training.
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Protocols 1 and 2 were aclministered to the left and right side of thesubjects prioi to (test 1) and after (test 2) the 3 week stretchingperiod. The tests were performed at the same time on both testdays. The subjects did not perform any stretel training on the dayof test 2.
Data reduction and analysisPassive torque, joint range of motion, angular velocity andhamstring EMIG were continuously recorded over the entire rangeof stretch manoeuvres. Signals were sampled at 50 Hz, A/Dconverted (DT 2801A, Data Translation), and stored on a PC forsubsequent analysis. In the stretch phase in protocol 1 the totalenergy (Alagnusson, Simonsen, Aagaard & Kjaer, 1996b) and themnean EMG amplitude wXere calculated. Further, the torque-anglecurve was considered to contain three approximately even portions;
an initial toe region, a transition periodl and a linear portion(Fig. 3). The slope, i.e. the stiffness, of the linear portion of thetorque-angle curve was calculated (Alagnusson et al. 1996b). In theholding phase, peak torque was obtainecd the instant the lever arm
Final
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Figure 2. Data for one subject from protocol 1A slhows the passive torque (gravity corrected) recording with the peak torque, final torque ancl maximalvoluntary contraction (AIVC). B, the corresponding EMG amplitude. Note the absence of activity despite a
decline in torque from peak to final. C, velocity, which during the stretch phase is 0-0875 rad s-'. D showsthe angle (negative -alue indicates angles above horizontal) with its stretch phase (1, continuous line) and
90 s hlolding phase (2, dashed line) prior to MV C.
J Physiol.497.1
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reached the final angle, and final torque was obtained after 90 s inthe holding phase. ATorque was the decline in torque expressed asa percentage of peak torque. The mean EMIG amplitude wascalculated for the initial and final 5 s of the 90 s in the holdlinigphase. Additionally, peak torque and EMG amplitude werecalculated for the MIVC. FoI protocol 2, maximal joint angle andcorresponding peak torque were obtained at the point of pain. Thearea under the torque-angle curve (energy) and the mean EMGIamplitude of the last 1 s prior to the onset of pain were calculated.
W'ilcoxon matchledl pairs signied rank tests were used to determinewhether differences existed between test 1 and test 2 for the
J. Physiol. 497.1
Figure 3. Data for one subject from thestretch phase of protocol 1Data have been gravity corrected and a 4th orderpolynomial fit was employed. The area under thecurve represents the potential energy returnfrom the tissue. The stiffness, or elastic modulus,was calculated in the linear portion of the curve(labelled Slope on the curve).
-0 50
measured variables. An a level of 0-05 was considered significant.Results are reported as the means + S.E.M.
RESULTSProtocol 1The results of variables examined in the stretch phase ofprotocol 1 are shown in Fig. 4. There were no significantdifferences in stiffness between the control (P = 0 86) andstretch side (P = 0-86). Similarly, no differences existed inenergy (control side, P= 0- 24; stretch side, P= 0-61) or in
- 30-X T6-
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Figure 4. Results from the stretch phase of protocol 1
.No significant differences existed for stiffness (A), energy (B) or EMG(C) before and after the training period on the control (0) and thestretchl side (0). Note that the EMG variation as negligible. Here,and in the follow ing figures, vertical lines and bars indicatethe S.E.AI.
S. P Magnusson and others
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Table 1. Initial and final 5 s EMG amplitudes (usV) in the holding phase of protocol 1
The knee joint torques in the holding phase are shown inFig. 5. All stretches yielded a significant decline in torque(Atorque, P = 0 018). However, peak and final torques andAtorque remained unchanged before and after the trainingperiod. The EMG results from the holding phase are shown inTable 1. There were no significant changes in EMG amplitudewithin a stretch (initial vs. final EMG) or between tests (test 1vs. test 2). The MVC resulted in a knee joint torque of64-7 + 5-8 N m with a corresponding EMG amplitude of273 2 + 43-2 ,V. The peak torque in the holding phase of thestretch represented 23 +4% of the MVC torque. Initial andfinal EMG amplitude in the holding phase corresponded to0 9 + 0-2 % of the EMG amplitude during MVC.
Protocol 2Figure 6 shows the results from protocol 2. There were nosignificant changes on the control side. On the other hand,
B
Figure 5. Results from the holding phase of protocol 1No significant differences existed for peak torque (A), final torque (B)or Atorque (the decline in torque as a percentage of peak torque; %;C) before and after the training period on the control (0) and thestretch side (0).
C
there were significant increases on the stretch side inmaximal angle (P = 0-018), peak torque (P = 0-018) andenergy (P = 0-018) (Fig. 7). The EMG amplitude prior topain was unchanged on the control side between test 1 andtest 2 (2-8 + 0 7 vs. 3-1 + 0-66V). Similarly, the EMGamplitude prior to pain did not differ on the stretch sidebetween test 1 and test 2 (3-8 + 0-6 vs. 5-6 + 2-0 #,V).The subjects completed 94 + 1% of the stretch sessions,i.e. the hamstring muscle group on the stretch side wassubjected to a total of 8460 s of stretch stimulus duringthe training period. None of the subjects undertook anynew forms of training.
DISCUSSIONThe purpose of the present study was to determine whethertissue properties and stretch tolerance changed as a result ofa 3 week regimen. No permanent change was observed in thetissue properties after the stretching period. On the other
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hand, maximum joint range of motion and correspondingpassive torque increased, which suggests that the mechanismfor improved joint range of motion is an increased stretchtolerance rather than a viscoelastic accommodation.
Protocol 1In the stretch phase, reduced stiffness and energy would beexpected after the training period if the stretching regimenproduced an enduring effect on the tissue properties of thehamstring muscle group. In animal models muscle stiffnessand energy during stretch can change acutely withtemperature increases (Strickler, Malone & Garrett, 1990;Noonan, Best, Seaber & Garrett, 1993) and stimulation(Garrett, Safran, Seaber, Glisson & Ribbeck, 1987) andchronically as a result of age and endurance training(Kovanen et al. 1984; Kovanen & Suominen, 1988).However, it has never been confirmed that tissue propertiesare affected by stretch training. In the present study, bothstiffness in the final portion of the torque-angle curve andenergy, which accounts for the entire torque-angle curve,were unaffected by the stretch training. In addition, in theholding phase peak, final and Atorque remained constantover the training period on both the control and trainingsides. Again, the low-level EMG response did not influencethe results since it was constant over the training period onboth sides.
The holding phase of protocol 1 confirms earlierobservations of the acute effects of a single stretch in animal(Abbott & Lowy, 1956; Taylor et al. 1990) and human in
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vivo models (McHugh et al. 1992; Magnusson et al. 1995). Inthe present study the low-level EMG response remainedunchanged in the holding phase, which suggests that the33-35% decline in torque about the knee joint was a tissueresponse. Further, since during the holding phase the EMGamplitude was below 1 % and peak torque was 23% of thatduring MVC, it is unlikely that muscle activity contributedsignificantly to passive peak torque and its subsequent stressrelaxation response. In contrast to the neurophysiologicalexplanation (Hutton, 1993), the present data demonstratethat the acute effects of stretching in the holding phase is aviscoelastic accommodation rather than a decline in EMGactivity.
Human models have shown that habitual stretchingproduces chronic increases in joint range of motion (Sady etal. 1982; Gajdosik, 1991; Bandy & Irion, 1994). Althoughunconfirmed, such increases are frequently attributed to achange in the tissue properties of the muscle (Gajdosik,1991; Hutton, 1993). Tissue properties may be affected byrepeated stretches (Magnusson et al. 1995; Magnusson et al.1996b), but the change is transient in nature and theviscoelastic properties return to baseline values within 1 h(Magnusson et al. 1996b). In the present study the totalstretching stimulus far exceeded that provided by previousstudies but produced no lasting change in the viscoelasticproperties of the muscle-tendon unit. It cannot be excludedthat rigorous forms of stretching regimens, such as in balletor gymnastics, over several years is a sufficient stimulus toyield a lasting change in the tissue properties.
**
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Figure 6. Results from protocol 2The stretching regimen resulted in significant increases on thestretch side (O) in maximal angle (A), peak torque (B) and energy (C),P = 0 018, while the control side (0) remained unchanged.
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296 J. Physiol.497.1
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Protocol 2After the training period the subjects reached a greatermaximal joint angle on the stretch side while the control sidewAas unchanged. Accompanying this increased angle was anincreased peak torque, while the low-level EMG remainedunchanged (Figs 6 and 7). Consequently, the present datasuggest that the mechanism for increased joint range ofmotion as a result of lhabitual stretching is an altered stretchtolerance, while the tissue properties remain unaffected. Ithas been demonstrated that stretch tolerance may be alteredacutely as a result of an isometric contraction, as evident bya 5 deg increase in joint angle and an accompanying increasein passive torque (Magnusson et at. 1996a). However, therehave been no reports of such chronic changes in flexibility. Inthe present study the magnitude of the joint angle increaseappears to have been greater (approximately 10 deg) thanthe acute increase (5 deg) previously reported. However,since the subjects did not perform any stretching on the testday after the training period it appears that the change wasenduring in nature.
An increased joint range ofincrease in torque about thewhen the knee was brought> 50 1NV before and after
motion with a concomitantknee joint has been shownto an angle which yieldeda 3 week training period
(Gajdosik, 1991). The results were attributed to an increasein muscle length. However, a change in the tissue propertymay only be concluded if a decrease in force was observed atthe same joint angle, or if a greater joint angle was achievedwrith the same load. Therefore, the reported change in jointangle cannot be a change in length, but may be explained byan altered stretch tolerance. The present study demonstratesthat increases in joint range of motion (protocol 2) canclearly be achieved without an accompanying change in thepassive length-tension relationship (protocol 1, stretchphase) or viscoelastic stress relaxation (protocol 1, holdingphase). Therefore, muscular flexibility is best defined asjoint range of motion rather than stiffness, or compliance.The mechanism for an altered stretch tolerance is unknown.However, it is possible that nociceptive nerve endings in thejoint and muscle play a role (Netter, 1983; Marchettini,1993).
Although the total stretch stimulus in the present study farexceeded that of previous studies (Gajdosik, 1991; Bandy &Irion, 1994), the magnitude of the increased joint range ofmotion appears to have been similar. It has been shown thatstretch durations of 30 and 60 s yield similar results over a6 week training period (Bandy & Irion, 1994). Others(Hardy, 1985) have shown comparable increases in joint
A50 -
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Figure 7. Torque-angle data for 1 subject fromprotocol 2A, the training side: note that after training thesubject reached a greater knee joint angle prior tothe onset of pain with an accompanying increase intorque. Further, it should be noted that the pre-tr-aining and post-trainiing are similar wvithl respectto the slope. B, the control side: the slope and theend point do not differ ov-er the training period. Thearrows indicate the end points for pre- and post-training.
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<- Post<- Pre
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J. Phy8iol.497.1 297
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range of motion over a 1 week period with a total stretchstimulus of merely 360 s. Consequently, it is possible that astretch stimulus of considerably smaller duration could haveproduced a similar clhange in stretch tolerance, or that theobserved changes occurred early in the training period.
ConclusionProtocols 1 and 2 were used to examine whether tissueproperties and stretch tolerance, respectively, changed as aresult of a 3 week stretching regimen in a human model.The result showed that the tissue properties wereunchanged. On the other hand, stretch tolerance wasaugmented, as evidenced by the increased maximal jointangle and the accompanying increased knee joint torque.Therefore improved joint range of motion appears to be dueto an increased stretch tolerance.
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AcknowledgementsThis project was funded in part by The Danish Sports ResearchCouncil J.nr. 1995-1-15.
S P Magnusson, E B Simonsen, P Aagaard, H Sørensen and M Kjaer A mechanism for altered flexibility in human skeletal muscle.
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Figure 10. Time course of effects of ryanodine (A) and Ruthenium Red (B) on glutamate-evoked sustained [Ca2+]nA, control, 0; ryanodine, 0. B, control, 0; Ruthenium Red, 0). Same scales as in Fig. 9. Both the effects ofryanodine and Ruthenium Red could not be washed out and no recovery was seen.
S. Peter Magnusson, Erik B. Simonsen, Per Aagaard, Henrik S0rensen and Michael Kjer
Journal of Physiology 497, 291-298 (1996)
On page 297, left-hand column, line 16, (approximately 10 deg) should appear as:
