specific modulation of motor unit discharge for a similar change in

J Physiol 577.2 (2006) pp 753–765 753

Specific modulation of motor unit discharge for a similarchange in fascicle length during shortening andlengthening contractions in humans

Benjamin Pasquet, Alain Carpentier and Jacques Duchateau

Laboratory of Applied Biology, Universite Libre de Bruxelles, 28 avenue P. Heger, CP 168, 1000 Brussels, Belgium

This study examines the effect of a change in fascicle length on motor unit recruitment

and discharge rate in the human tibialis anterior during shortening and lengthening

contractions that involved a similar change in torque. The dorsiflexor torque and the surface

and intramuscular electromyograms (EMGs) from the tibialis anterior were recorded in eight

subjects. The behaviour of the same motor unit (n = 63) was compared during submaximal

shortening and lengthening contractions performed at a constant velocity (10 deg s−1) with the

dorsiflexor muscles over a 20 deg range of motion around the ankle neutral position. Muscle

fascicle length was measured non-invasively using ultrasonography. Motor units that were

active during a shortening contraction were always active during the subsequent lengthening

contraction. Furthermore, additional motor units (n = 18) of higher force threshold that were

recruited during the shortening contraction to maintain the required torque were derecruited

first during the following lengthening contraction. Although the change in fascicle length was

linear (r2 > 0.99), and similar for both shortening and lengthening contractions, modulation

of discharge rate differed during the two contractions. Compared with an initial isometric

contraction at short (11.9 ± 2.4 Hz) or long (11.7 ± 2.2 Hz) muscle length, discharge rate

increased only slightly and stayed nearly constant throughout the lengthening contraction

(12.6 ± 2.0 Hz; P < 0.05) whereas it augmented progressively and more substantially during

the shortening contraction, reaching 14.5 ± 2.5 Hz (P < 0.001) at the end of the movement. In

conclusion, these observations indicate a clear difference in motor unit discharge rate modulation

with no change in their recruitment order between shortening and lengthening contractions

when performed with a similar change in muscle fascicle length and torque.

(Resubmitted 26 July 2006; accepted after revision 6 September 2006; first published online 6 September 2006)

Corresponding author J. Duchateau: Laboratory of Applied Biology, Universite Libre de Bruxelles, 28 avenue P. Heger,

CP 168, 1000 Brussels, Belgium. Email: [email protected]

The force produced by a muscle is influenced by its length(Gordon et al. 1966), and the modality and velocity of thecontraction (Katz, 1939; Edman et al. 1978). A commonobservation in whole-muscle or single-fibre studies inexperimental animals is that the force achieved during amaximal contraction is greater in lengthening (eccentric)than in isometric and shortening (concentric) conditionswhen measured on the plateau and on the descendinglimb of the length–tension curve (Katz, 1939; Edmanet al. 1978; Morgan et al. 2000). In the performance ofvoluntary actions, the contraction-type difference in theforce capacity of muscle may be related to the controlstrategy used by the central nervous system (CNS) toactivate the motor unit pool of the muscle (Westinget al. 1991; Pinniger et al. 2000). This hypothesis issupported by the observation that EMG activity recordedat the same movement velocity is usually lower during

maximal voluntary lengthening compared with shorteningcontractions (Komi & Burskirk, 1972; Westing et al. 1991;Aagaard et al. 2000). Furthermore, the maximal torquethat can be achieved during a lengthening contractionis increased by the addition of electrical stimulationsuperimposed over the voluntary effort (Westing et al.1991; Pinniger et al. 2000). The incomplete activationduring lengthening contractions is accompanied by lowerexcitability of the corticospinal tract to transcranialmagnetic or electrical stimulation (Abbruzzese et al.1994; Sekiguchi et al. 2003) and depressed monosynaptic(Romano & Schieppati, 1987; Abbruzzese et al. 1994;Nordlund et al. 2002) and polysynaptic reflex excitability(Nakazawa et al. 1997). Furthermore, EEG recordingsindicate greater and earlier cortical activity duringsubmaximal and maximal lengthening elbow flexoractions (Fang et al. 2001, 2004), suggesting that the CNS

C© 2006 The Authors. Journal compilation C© 2006 The Physiological Society DOI: 10.1113/jphysiol.2006.117986

754 Benjamin Pasquet, Alain Carpentier and Jacques Duchateau J Physiol 577.2

may plan and program lengthening movements differentlyfrom shortening contractions.

The mechanisms that give rise to specific muscleactivation during shortening and lengthening contractions(see Enoka, 1996) involve modulation in motor unitrecruitment and rate coding. While some studies reportedthat lengthening contractions are associated with aselective activation of high-threshold fast-twitch motorunits and a derecruitment of low-threshold slow-twitchunits (Nardone et al. 1989; Howell et al. 1995; Linnamoet al. 2003), others reported a recruitment order that isconsistent with the size principle (Henneman, 1957) forboth shortening and lengthening contractions (Garlandet al. 1994; Søgaard et al. 1996; Bawa & Jones, 1999; Stotz &Bawa, 2001). Although, Stotz & Bawa (2001) reported therecruitment of additional higher threshold units duringsome lengthening contractions, this occurred only whenthe force or movement profile was erratic. In contrast tothe similarity in recruitment order, motor unit dischargerate does vary with contraction type. Average dischargerate is usually lower during submaximal lengtheningcontractions compared with shortening contractions (Taxet al. 1989; Howell et al. 1995; Søgaard et al. 1996; Kossev &Christova, 1998; Semmler et al. 2002; Del Valle & Thomas,2005), even when the number and properties of identifiedactive motor units were similar (Søgaard et al. 1996).

To obtain a more complete understanding of thefunctional organization of the motor unit pool duringshortening and lengthening contractions, it would beinstructive to determine if a similar change in torque isreached mainly by selective recruitment of high-thresholdmotor units, the modulation of discharge rate, or byboth mechanisms. Some of the discrepancy in the existingliterature could be explained because populations of unitswere often compared, instead of analysing the behaviour ofthe same unit during both contraction types. Furthermore,movement velocity was not always carefully controlled,and the change in muscle length during movement wasonly estimated from the recording of joint position andnot from direct measurement of fascicle length. This is acritical issue because it has been shown that fascicle lengthduring maximal shortening and lengthening contractionsis not linearly related with joint angle in the tibialis anterior(Reeves & Narici, 2003). Another major advantage ofmeasuring fascicle length during movement is that it canprovide length information from the portion of musclewhere the motor units are recorded, in contrast with theestimate of the whole muscle length from changes in jointangle. Nonetheless, the association between changes infascicle length with joint angle may vary across muscles,which could explain the divergent results on motorunit recruitment and discharge rate in shortening andlengthening contractions.

Therefore, the purpose of this work was to examinethe effect of a change in fascicle length of the tibialis

anterior muscle on the recruitment and discharge rateof the same motor unit during submaximal shorteningand lengthening contractions for a similar change intorque. Angular velocity about the ankle joint was constantduring both types of contractions. It was hypothesizedthat differences in the rate of change in fascicle lengthcould explain some of the previously reported differencesin motor unit discharge rate observed during shorteningand lengthening contractions.

Methods

Subjects

Eight subjects (6 men and 2 women) age 22–48 years,participated in this investigation and were tested on severaloccasions for a total of 24 experimental sessions. Twosuccessive sessions were separated by at least 1 week. Priorto the experimental sessions, all subjects were familiarizedwith the procedure and contraction modalities during oneor two sessions. None of the subjects had any knownneurological or motor disorder prior to testing. Theywere all volunteers and gave their informed consentbefore participating in the study. This investigation wasapproved by the University Ethics Committee and all theexperimental procedures were performed in accordancewith the Declaration of Helsinki.

Ergometric device

A motor-driven computer-controlled ergometer (TypeHDX 115C6; Hauser Compax 0260M-E2; Offenburg,Germany) was used (Pasquet et al. 2000). This device,equipped with a footplate that was fixed to the rotationalaxis of the motor, recorded the torque generated by thedorsiflexor muscles under static and dynamic (isokinetic)conditions. The subject was secured on an adjustable chairin a slightly reclined position. The right foot was strappedto the plate so that the axis of rotation of the ankle jointwas aligned with the shaft of the torque motor. The platewas inclined at an angle of 45 deg relative to the floorand the position of the subject was adjusted to obtain a90 deg angle for the ankle (neutral position or 0 deg) anda 120–130 deg knee angle. This position was duplicatedacross sessions. The foot was held in place by a heel blockand was tightly attached to the plate by means of two straps.One strap was placed around the foot, 1–2 cm proximal tothe metatarsophalangeal joint of the toe, and the secondstrap was placed around the foot, just below the anklejoint.

Mechanical and EMG recordings

The torque produced by the dorsiflexor muscles duringcontractions was measured by a strain-gauge transducer

C© 2006 The Authors. Journal compilation C© 2006 The Physiological Society

J Physiol 577.2 Motor unit behaviour during fascicle length change 755

(sensitivity, 0.018 V (N m)−1; linear range, 0–200 N m)mounted on the rotational axis of the motor. The forcesignal was amplified and filtered (AM 502; Tektronix,Beaverton, OR, USA; bandwidth DC–300 Hz).

Motor unit potentials were recorded by a selectiveelectrode that comprised two 50 μm diamel-coatednichrome wires glued into the lumen of a 30 gaugehypodermic needle (Duchateau & Hainaut, 1990). Theelectrode was inserted in the middle part of the tibialisanterior muscle and during each experimental session theneedle was inserted at different locations. At each location,the needle was manipulated to various depths and anglesto obtain a recording site from which the same motor unitwas monitored at the two ankle joint positions (10 degplantarflexion and 10 deg dorsiflexion) and during theshortening and lengthening phases of the contraction. TheEMG signal was amplified by a custom-made differentialamplifier (×2000) and filtered (100 Hz to 10 kHz) beforebeing displayed on a Tektronix TAS 455 oscilloscope. Thesurface EMG of the tibialis anterior, soleus and lateralgastrocnemius were recorded by means of two silver diskelectrodes (8 mm diameter) placed 2–3 cm apart on thebelly of the muscle. The electrodes over tibialis anteriorwere located on either side of the needle electrode. Theground electrodes (silver plates of 2 cm × 3 cm) wereplaced over the tibia. The EMG signals were amplified(×1000) and filtered between (10 Hz and 1 kHz) by acustom-made differential amplifier.

Experimental procedure

Prior to the recording of single motor units, the isometrictorque exerted by the dorsiflexor muscles during a maximalvoluntary contraction (MVC) was determined. First, thesubject performed three MVCs of 4–5 s duration, separatedby 2–3 min rest in a random order at ankle angles of 10 degplantarflexion (long) and 10 deg dorsiflexion (short). Thiswas followed by the recording of the dorsiflexion torquerecorded during maximal shortening and lengtheningcontractions (2–3 MVCs in each condition) at a constantangular velocity of 10 deg s−1. Once a motor unit actionpotential was clearly identified at each recording site, sub-jects were asked to produce a ramp contraction at thetwo ankle positions at a rate of ∼5% MVC s−1 up to therecruitment of the selected unit and then to hold the torqueconstant to sustain a minimal, repetitive discharge of theunit for at least 5 s. Target torques were thus determinedat short and long muscle lengths (Pasquet et al. 2005).Thereafter, subjects were asked to perform the followingtask: (1) sustain an isometric dorsiflexion torque at thetarget torque for the long muscle length for 5 s; (2) as thetorque motor dorsiflexed the foot about the ankle, to assistthe motion with the dorsiflexors and to reach smoothly thetarget torque for the short muscle length at the end of the

movement; (3) to sustain an isometric dorsiflexion torqueat the target torque for the short muscle lengths during5 s; (4) as the torque motor plantarflexed the foot aboutthe ankle, to resist the motion with the dorsiflexors and toreach smoothly the target torque for the long muscle lengthat the end of the movement (Fig. 1). This cycle was repeatedat least 10 times depending on the ability of the subjectto perform the task accurately (see below for the criteriaused). To accomplish the task, subjects were providedwith visual feedback on a digital oscilloscope of the actualtorque and the torque targets for the two muscle lengths(Model 120; Nicolet, Madison, WI, USA). The subjectsalso received audio feedback of motor unit discharge rateto help them to recognize the selected unit. The shorteningand lengthening contractions lasted 2 s at a constantangular velocity (10 deg s−1) over a 20 deg range ofmotion (from 10 deg plantarflexion to 10 deg dorsiflexion,and from 10 deg dorsiflexion to 10 deg plantarflexionaround the ankle neutral position for shortening andlengthening contractions, respectively). The contractionswere performed at a relatively slow velocity to diminishthe interference of the unloading (shortening contraction)or stretch (lengthening contraction) reflexes with thecentral command to the muscle and to minimize torquefluctuations at the onset of movement. Two successivetrials from different electrode locations were separated byat least 5–10 min of rest.

The protocol was intended to compare the behaviourof the same unit during the isometric and dynamic(shortening and lengthening) contractions when themuscle produced a similar change in torque. The strategyto control the change in muscle torque was pre-ferred to using the EMG as an index of contractionintensity. Indeed, EMG activity is usually less duringlengthening contractions (Westing et al. 1991; Aagaardet al. 2000; Klass et al. 2005) and differences in the levelof motor unit synchronization during shortening andlengthening contractions (Semmler et al. 2002) wouldprobably contribute to differences in the amount of EMGcancellation in the two conditions (Keenan et al. 2005) thatwould confound the comparison of the EMGs.

Data analysis

Data processing was performed off-line from taped records(Sony PCM-DAT, DTR 8000; Biologic, Claix, France). Allsignals were acquired on a personal computer at a samplingrate of 3 kHz (force), 6 kHz (surface EMG) or 12 kHz(intramuscular EMG) by a MP150 data acquisition system(Biopac Systems, Santa Barbara, CA, USA).

MVC torque (isometric or dynamic contractions) wasdetermined from the trial that yielded the largest value.The MVC torque and associated average full-wave rectifiedEMG amplitude (aEMG) were measured during a 2 s



epoch during the MVC plateau (isometric contractions)or throughout the entire range of motion (shorteningand lengthening contractions). Motor unit discriminationwas accomplished either with a window discriminator(Duchateau & Hainaut, 1990) or, when necessary,by a computer-based, template-matching algorithm(Signal Processing Systems, SPS 8701, Malvern Victoria,Australia). Trials that contained abnormally short andlong interspike intervals due to discrimination error werere-analysed on a spike-by-spike basis. Single motor unitaction potentials were identified on the basis of amplitude,duration, and waveform shape. Only the motor units that:(1) were clearly identified, (2) showed waveforms andamplitudes that changed gradually and systematically overtime throughout the different parts of the task, and (3)that differed by less than 20% in amplitude at the two

Figure 1. Behaviour of a single motor unit during isometric and dynamic contractionsA typical discharge pattern of the same motor unit recorded in the tibialis anterior is illustrated during a sustainedisometric contraction and during shortening (A) and lengthening (B) contractions of the dorsiflexor muscles. Forboth conditions, angular ankle displacement (a), the torque produced during dorsiflexion (b), rectified surface(c) and intramuscular (d) EMG of the tibialis anterior, and instantaneous discharge rate (e) of the motor unitare illustrated. F, the action potentials of the identified unit are superimposed with an expanded display. Therecruitment threshold of the unit was 3.9 N m (10.9% maximal voluntary contraction (MVC)) and 6.6 N m (18.0%MVC) in short and long positions, respectively. The discharge rate was first decreased from 9.3 to 5.3 Hz at thetransition between the isometric and shortening contractions before increasing progressively up to 12.1 Hz at theend of the movement. Conversely, for the lengthening contraction, the discharge rate was first increased from10.0 to 15.0 Hz before slowly returning to its initial value (9.4 Hz) after the end of the movement. The verticaldashed lines indicate the beginning and the end of the movement in each condition.

ankle angles and movement modalities were included inthe analysis. Furthermore, only trials during which torqueincreased linearly within a 90% confidence interval anddid not deviate for more than 5% MVC at the two targetlevels were included in the analysis. These criteria andthe technical difficulty of recording the same motor unitduring movements explain the relative low yield in eachsession (∼3). Motor unit recruitment threshold, definedas the torque at which the motor unit began to discharge,was determined during the isometric ramp contractionsat the two different ankle angles (10 deg dorsiflexionand 10 deg plantarflexion). Recruitment threshold wasthen expressed as a percentage of the MVC torqueobtained at the same ankle angle. Motor unit dischargerate was measured during the different phases of thetask.



Ultrasonography

The architectural changes of the tibialis anteriorduring shortening and lengthening contractions wereinvestigated in each subject during a separate session byultrasonography (Fukunaga et al. 2001; Reeves & Narici,2003). Fascicle length was assessed by images obtainedusing real-time B-mode ultrasonographic apparatus (AU5;Esaote, Firenze, Italy; 13 MHz linear-array probe with a38 mm scanning length) positioned on the skin along themid-sagittal plane of the tibialis anterior muscle over thesite corresponding to the location of the needle insertions.Once muscle fascicles had been clearly identified, theposition of the probe was firmly held in place usinga self-made resin sheath to provide a standardizedmeasurement site and ensure that measurements weretaken from the same position. The probe was coatedwith a water-soluble transmission gel to provide acousticcontact. A metallic marker was placed between the skinand the ultrasound probe to verify that the probe did notmove during the recording. Images acquired during themovements were recorded at a frequency of 20 Hz. Thesignal from the footplate rotation was used to synchronizethe ultrasound images with the ankle movement.

Images were obtained for each subject from anklemovements at torques corresponding to those recordedduring motor unit recordings. With the help of visualfeedback, subjects had to match target torques determinedfrom previous experimental sessions. Measurements offascicle length were obtained with digitizing software(Scion Image, National Institutes of Health, USA). Becausethe tibialis anterior is a bipennate muscle with a centralaponeurosis (Reeves & Narici, 2003), fascicle length wasdetermined as the distance from the central to thesuperficial aponeuroses. When the superficial end of

Figure 2. Change in average discharge rate inmotor units during isometric and dynamiccontractionsThe average discharge rate is reported duringshortening (•) and lengthening ( �) contractions (from 0to 2 s), and during isometric contractions (from 2 to 4 s)at short (�) and long (�) muscle lengths. Each value,expressed as percentage of the discharge rate recordedduring the initial isometric contractions, represents theaverage (±S.E.M.) over 0.2 s bins for all motor unit(n = 63) computed across all contraction intensities. Theinset illustrates the average (±S.E.M.) changes indischarge rate for the first 10 discharges at thetransition between the sustained isometric contractionand the onset of movement. The horizontal dashed linerepresents the average discharge rate during theprevious isometric contraction. Significant differencefrom initial value in each conditions: ∗P < 0.05,∗∗P < 0.01, ∗∗∗P < 0.001. Significant differencebetween the two conditions: +P < 0.05, ‡P < 0.01,†P < 0.001.

the fascicle extended off the acquired ultrasound image,fascicle length was determined by trigonometry byassuming a linear continuation of the fascicles (Reeves &Narici, 2003).

Statistics

Data are reported as means ± s.d. within the text, anddisplayed as means ± s.e.m. in the figures. Torque andsurface EMG during MVCs, recruitment threshold, andaverage discharge rate of motor units at the two ankle jointangles (10 deg plantarflexion and 10 deg dorsiflexion) wereanalysed using Student’s paired t test. Changes in aEMG,motor unit discharge rate and muscle fascicle length duringshortening and lengthening contractions were analysed bya two-way ANOVA with repeated measures. A Tukey posthoc test was conducted when significant main effects wereobserved. Significance was set at P ≤ 0.05.

Results

The average isometric MVC torque produced bythe dorsiflexor muscles at long muscle length(10 deg plantarflexion) was greater (44.3 ± 4.2 versus35 ± 3.3 N m; P < 0.001) than at short muscle length(10 deg dorsiflexion). In contrast, the correspondingaEMG of the tibialis anterior decreased (P < 0.05)with increased muscle length (0.43 ± 0.06 versus0.47 ± 0.08 mV). The average MVC torque during theshortening and lengthening contractions was 28.7 ± 4.2and 45.3 ± 3.8 N m, respectively. As expected, the torquewas significantly higher (P < 0.001) during maximallengthening contractions. In contrast, the aEMG of the



tibialis anterior was lower during the lengthening thanshortening MVC (0.40 ± 0.06 versus 0.43 ± 0.08 mV;P < 0.01).

Behaviour of single motor unit during shorteningand lengthening contractions

The behaviour of the same motor unit was trackedduring shortening and lengthening contractions of thedorsiflexors performed at a constant angular velocity. Atypical example of the discharge of a single motor unit isillustrated in Fig. 1. The unit was recruited at an isometricdorsiflexion torque of 3.9 N m (10.9% MVC) and 6.6 N m(18.0% MVC) in the short and long positions, respectively.In this example, the unit was activated continuouslyduring the isometric contraction at the two ankle positionsand the shortening and lengthening contractions. Thedischarge rate first decreased from 9.3 to 5.3 Hz at thetransition between the isometric and shortening contra-ctions (unloading reflex) before increasing progressivelyup to 12.1 Hz at the end of the movement. Conversely,the discharge rate during the lengthening contractionfirst increased to 15.0 Hz (stretch reflex) before slowlyreturning to its initial value (9.4 Hz) at the end of themovement.

The same behaviour was observed for all 63 motorunits. The range of recruitment thresholds, expressed aspercentage of their respective isometric MVC, extendedfrom 0.2 to 21.1% (mean ± s.d.; 5.7 ± 5.9% MVC) andfrom 0.5 to 32.8% (9.8 ± 8.6% MVC) at short and longmuscle lengths, respectively. The difference between themean values corresponded to a significant reduction ofthe recruitment threshold of 45.1 ± 24.1% (P < 0.001)when the ankle joint was moved from 10 deg plantarflexion(long) to 10 deg dorsiflexion (short).

Before the onset of the dynamic contractions, theaverage discharge rate computed over a 2 s epochand across all isometric contraction intensities was11.9 ± 2.4 and 11.7 ± 2.2 Hz for short and long musclelengths, respectively, and did not differ statistically. InFig. 2, motor-unit discharge rate computed across allcontraction intensities during shortening and lengtheningcontractions (from 0 to 2 s) and the isometric contractions(from 2 to 4 s) has been expressed as a percentage of changefrom the values recorded during the initial isometriccontractions. The typical pattern observed at the onset ofshortening contraction (first 10 discharges; Fig. 2, inset),was a rapid reduction in discharge rate to 72 ± 14.3% of theinitial values (from 11.7 ± 2.2 to 8.2 ± 2.5 Hz; P < 0.001)for the first interspike interval. This first depression wasfollowed by a rapid return to initial values and a progressiveincrease during the remaining part of the contraction(from 0.4 to 2 s; Fig. 2, main graph). The average dischargerate was 29.1 ± 16.9% greater (14.5 ± 2.6 Hz; P < 0.001)

at the end of the movement when compared with initialvalues. In contrast, discharge rate during lengtheningcontractions was first enhanced to 115.2 ± 14.0% of theinitial values (from 11.9 ± 2.4 to 13.7 ± 2.7 Hz; P < 0.001;Fig. 2, inset) and roughly maintained at this level to theend of the movement (Fig. 2, main graph). However, atthis stage, no significant difference was observed comparedwith control discharge rate (106.7 ± 12.8%; 12.4 ± 2.0 Hz;P > 0.05). The following sustained isometric contractionat both muscle lengths was associated with a progressivereturn to control values, and 1.4 s after the end ofthe shortening contraction no significant difference indischarge rate was observed.

Recruitment of additional motor units

Eighteen additional motor units were recruited duringthe shortening contraction. These units, recorded insix of the eight subjects, were recruited at an averageisometric threshold of 7.8 ± 4.6% MVC (3.4 ± 2.1 N m)and 13.2 ± 6.1% MVC (5.4 ± 2.6 N m) at short and longmuscle lengths, respectively. These additional units wererecruited at an average ankle angle of 2.4 ± 4.3 degdorsiflexion (range: from 4.8 deg plantarflexion to8.6 deg dorsiflexion) during the shortening contractions,and derecruited during the lengthening phase of thecontraction at an average ankle angle of 7.2 ± 2.9◦

plantarflexion (range: from 2.5 to 10 deg plantarflexion;Fig. 3A). In some inaccurate trials, when the subjectovershot the target torque and a greater dorsiflexiontorque during the lengthening contraction was produced,these units continued to discharge up to the endof the movement and during the following isometriccontraction. When averaged throughout their activation,the discharge rate of these units was 13.1 ± 2.1, 11.4 ± 2.1and 12.6 ± 2.9 Hz for the shortening, lengtheningand isometric contractions, respectively. The averagedischarge rate was significantly greater (P < 0.001)during shortening compared with lengthening contraction(Fig. 3B) and differed significantly for both shorteningand lengthening contractions from isometric contraction(P < 0.01).

Figure 4 displays an example of additional recruitmentand derecruitment during dynamic contractions. In thisexample, the second unit (MU2) was recruited duringthe shortening contraction at an ankle angle of 1 degdorsiflexion and derecruited during the lengtheningcontraction at a more extended ankle joint angle (8.0 degplantarflexion). The second unit was recruited (shorteningcontraction) or derecruited (lengthening contraction)although a nearly constant and similar discharge rate ofthe first unit (15.2 ± 3.2 and 15.5 ± 2.0 Hz for shorteningand lengthening contractions, respectively) and showscomparable changes of the general discharge pattern tothe first recruited unit (MU1).



Surface EMG activity

The modulation in motor unit activity during movementparalleled the change in the surface EMG activityof the tibialis anterior, as illustrated by Fig. 5. Whencomputed across all contraction intensities, the aEMG(percentage change) decreased to 76.4 ± 13.7% of theinitial values (from 0.075 ± 0.031 to 0.058 ± 0.028 mV;P < 0.001) from the beginning of the movement to thefirst 0.1 s sequence of shortening contraction. Thereafter,the aEMG increased progressively up to the end ofthe shortening contraction and reached 134.8 ± 21.0%(0.098 ± 0.037 mV; P < 0.001) of the initial values. TheaEMG declined progressively during the subsequentisometric contraction at the short muscle length, but stayedabove (118.7 ± 16.4%; 0.087 ± 0.035 mV; P < 0.001) thevalues recorded at the long muscle length. In contrast,the aEMG reached slightly higher values (108.1 ± 6.3%;from 0.084 ± 0.035 to 0.09 ± 0.036 mV; P = 0.06) assoon as the lengthening contraction was initiated, andit remained constant up to the end of the movement.The aEMG regained its control value (96.9 ± 19.1%;0.078 ± 0.029 mV; P > 0.05) during the subsequentisometric contraction at the long muscle length.

Coactivation of antagonist muscles (soleus and lateralgastrocnemius) paralleled the changes observed forthe agonist muscles and augmented progressively withincreased dorsiflexion torque during both shorteningand lengthening contractions. When computed acrosssubjects and over all contraction intensities, excluding thetransition phases (first 0.4 s) at the beginning of each

Figure 3. Characteristics of the additional motor units recruited during shortening contractionsA, each line shows the recruitment threshold of 1 of 18 motor units recruited during a shortening contraction (•)and its derecruitment threshold during the subsequent lengthening contraction ( �). Each threshold is expressed as afunction of ankle angle (◦) around the neutral position (horizontal dashed line), and the negative and positive valuescorrespond to dorsi- and plantarflexion, respectively. B, comparison of the average discharge rate of these unitsduring shortening (•) and lengthening ( �) contractions. For each unit, the average discharge rate was computedfrom its recruitment to the end of the shortening contraction (shortening) and from the beginning of lengtheningcontraction to its derecruitment (lengthening)

movement, the ratio between antagonist and agonistaEMG activity differed slightly but significantly betweencontraction types (Table 1). The coactivation ratio wassignificantly greater (P < 0.001) during lengtheningcompared with shortening contractions for both thesoleus and lateral gastrocnemius, and during isometriccontractions at long compared with short muscle lengthfor the soleus.

Fascicle length change

The effect of a change in ankle position on fasciclelength during shortening and lengthening contractions atdifferent torque levels (from 5 to 30% MVC) is illustratedfor one subject in Fig. 6A. This graph shows that regardlessof ankle angles, fascicle length shortened progressivelywith an increase in dorsiflexion torque. Furthermore,there was no difference in the change in fascicle lengthduring the shortening and lengthening contractions.When averaged across subjects and over the torque levelsat which the 63 units were recorded (Fig. 6B), fasciclelength decreased by 18.3 ± 1.4% (from 75.9 ± 2.7 to62.0 ± 2.7 mm; P < 0.001) and increased by 22.1 ± 2.9%(from 62.2 ± 3.6 to 75.8 ± 4.0 mm; P < 0.001) duringshortening and lengthening contractions, respectively.When comparing both shortening and lengtheningvalues across all contraction intensities, no significantdifference was observed throughout the 20 deg anklerange of motion (Fig. 6B). Within the range of the ankledorsiflexion torques during the motor unit recordings,a linear change of muscle fascicle length was observed



during shortening (y = 0.644x + 69.2; r2 = 0.997) andlengthening (y = 0.650x + 69.4; r2 = 0.998) contractions.When computed across both contraction modalitiesand contraction intensities, fascicle length changedby 13.7 ± 1.4 mm (20.1 ± 3.1%) when the ankle jointmoved over a 20 deg range of motion around the neutralposition. The average fascicle velocity did not differsignificantly between shortening and lengtheningcontractions (7.0 ± 0.8 and 6.8 ± 1.2 mm s−1,respectively).

Discussion

The main finding of the current study was a differencein the modulation of motor unit discharge rate inthe tibialis anterior, with no change in recruitmentorder between shortening and lengthening submaximalcontractions performed at a constant ankle angularvelocity and for a similar change in torque. Furthermore, a

Figure 4. Behaviour of an additional motor unit recruited during shortening contractionA typical discharge and recruitment pattern of two motor units (MU1 and MU2) recorded in the tibialis anteriorduring a sustained isometric contraction and during shortening (A) and lengthening (B) contractions. In bothconditions, angular ankle displacement (a), rectified surface (b) and intramuscular (c) EMG of the tibialis anterior,and instantaneous discharge rate (d and e) of MU1 (d) and MU2 (e) are illustrated. Action potentials of MU1 (f )and MU2 (g) are superimposed with an expanded display. MU2 was recruited during the shortening phase at anankle angle of 1 deg dorsiflexion and derecruited during the lengthening contraction at a more extended anklejoint angle (8.0 deg plantarflexion). Note that the discharge rate of the first motor unit remained relatively constantwhen the second unit was recruited (shortening) and derecruited (lengthening contraction). The vertical dashedlines indicate the beginning and the end of the movement in each condition.

similar change in fascicle length at the same speed involveda greater recruitment and modulation of discharge rate ofthe same motor units during slow shortening contractionscompared with lengthening contractions.

A major strength of our study was the measurement ofaverage fascicle length during shortening and lengtheningcontractions; this provided length information on theportion of the muscle from where the motor units wererecorded. The results indicated that fascicle length of thetibialis anterior varied linearly with ankle joint rotation,despite a slight variation in the moment arm of thedorsiflexors during ankle rotation (Maganaris et al. 1999).The average fascicle length changed by ∼20% when theankle joint moved over the 20 deg range of motion andthere was no statistical difference in the change in fasciclelength and its average velocity between shortening andlengthening contractions. Although the range of motionexamined in the current study might represent a differentportion of the active torque–angle curves for the different



Table 1. Coactivation ratio for the soleus and the lateral gastrocnemius during differentcontraction types with the tibialis anterior

Isometric

Short Long Shortening Lengthening

Soleus 4.9 ± 1.5% 6.1 ± 1.4% 5.3 ± 1.1% 7.0 ± 2.3%Lateral gastrocnemius 2.1 ± 1.4% 2.3 ± 1.2% 1.8 ± 1.1% 2.4 ± 1.3%

Antagonist coactivation is expressed as the ratio of average full-wave rectified EMG (aEMG)activities between the soleus or the lateral gastrocnemius and the tibialis anterior. Datarepresent mean values (±S.D.) computed across subjects and over all contraction intensities,and averaged over 2 s for the isometric contractions and during the movement (excludingthe first 0.4 s) for the shortening and lengthening contractions. For the soleus, all contractionmodalities differ statistically from each other at P < 0.001, except for the comparisonbetween shortening and isometric contraction at short length for which the statistical levelis P < 0.05. For the lateral gastrocnemius, all contraction modalities differ statistically fromeach other at P < 0.001, except for the comparisons between isometric contractions at thetwo lengths, and between lengthening and isometric contraction at long muscle length forwhich significant difference was observed.

subjects, it should have minor effect on our results becausethis part of the torque–angle curve is relatively flat duringsubmaximal activations (Marsh et al. 1981) and oursubjects showed a similar increase in maximal isometrictorque (range 17–32%) when tested at long compared withshort muscle lengths.

It is well known from animal studies on wholemuscles and single fibres that force during lengtheningcontractions increases above isometric force whenmeasured on the plateau and on the descending limbof the length–tension curve (Katz, 1939; Edman et al.1978; Morgan et al. 2000). The usual explanation forthis extra force is the development of sarcomere lengthnon-uniformity in the fibres (Julian & Morgan, 1979),although the contribution of other mechanisms cannotbe excluded (see Pinniger et al. 2006). Force enhancementis not observed for all muscle groups in humans duringvoluntary lengthening contractions, possibly due to atension-limiting mechanism (Westing et al. 1991; Aagaardet al. 2000; Pinniger et al. 2000). However, the absolutetorque produced by the dorsiflexor muscles aroundthe neutral (90 deg) ankle angle during lengtheningcontraction is usually much greater than during isometricand shortening contractions (Pasquet et al. 2000; Klasset al. 2005). Due to the greater force capacity ofmuscle during lengthening contractions, neural activationmust be augmented during a submaximal shorteningcontractions performed against a given load or for a similarchange in torque.

Although the utility of EMG to infer changes in thevoluntary drive to muscle can be misleading (Keenanet al. 2005), our results for a similar change in torqueare consistent with this interpretation as a greateraEMG was reached during shortening compared withlengthening contractions. The results included transientchanges in surface aEMG at the transition between

the sustained isometric contraction and the movement.There was a small increase in aEMG at the onset ofthe lengthening contraction that was probably due toincreased motor unit discharge rate (see Figs 1 and 4)

Figure 5. Change in aEMG during isometric and dynamiccontractionsThe surface average full-wave rectified EMG (aEMG) of the tibialisanterior is reported during shortening (•) and lengthening ( �)contractions (from 0 to 2 s), and during isometric contractions (from 2to 4 s) at short (�) and long (�) muscle lengths. Each value representsthe average (±S.E.M.) over 0.2 s bins for all subjects and trialscomputed across all contraction intensities. The horizontal dashed linerepresents the average aEMG during the previous isometriccontraction. Significant difference from initial value in each conditions:∗∗P < 0.01, ∗∗∗P < 0.001. Significant difference between the twoconditions: +P < 0.05; †P < 0.001.



caused by the sudden muscle stretch (Struppler, 1975; Roll& Vedel, 1982; Wise et al. 1999). Thereafter, the aEMGremained nearly constant during muscle lengtheningand at a slightly greater level compared with isometriccontractions at both lengths. In contrast, aEMG decreasedinitially during the shortening contraction due to theunloading reflex (Struppler, 1975; Roll & Vedel, 1982;Wilson et al. 1997); this matches the transient reductionin motor unit discharge rate (see Figs 1 and 4).Subsequently, the aEMG increased progressively until theend of the shortening contraction by the recruitment ofadditional motor units and increased discharge rate (seebelow). The greater aEMG during the sustained isometriccontraction at the short muscle length compared with thelong length was mainly due to the recruitment of motorunits.

Due to technical difficulties, few studies have analysedthe behaviour of the same motor units during shorteningand lengthening contractions (Nardone et al. 1989;Howell et al. 1995; Søgaard et al. 1996; Stotz & Bawa,2001; Semmler et al. 2002). Such recordings are moreproblematic during dynamic than isometric conditionsbecause of electrode movement and the difficulty inperforming shortening and lengthening contractions

Figure 6. Change in muscle fascicle length during dynamic contractionsThe average fascicle length of the tibialis anterior when the ankle joint moved over a 20 deg range of motion aroundthe neutral position (0 deg) is reported during shortening (•; from 10 deg plantarflexion to 10 deg dorsiflexion)and lengthening contractions ( �; from 10 deg dorsiflexion to 10 deg plantarflexion). A, the effect of a change inankle position on fascicle length during shortening and lengthening contractions at different torque levels (from5 to 30% MVC by steps of 5% MVC) is illustrated for one subject. B, average (±S.E.M.; n = 63) fascicle lengthcomputed across subjects and over contraction intensities corresponding to the torque recorded during motorunit recordings. A linear change between muscle fascicle length and ankle joint ankle is obtained for shortening(y = 0.644x + 69.2; r2 = 0.997) and lengthening (y = 0.650x + 69.4; r2 = 0.998) contractions. Note the similarchange in fascicle length between shortening and lengthening contractions for different torque levels in a singlesubject and when averaged across subjects and over contraction intensities.

against an inertial load at a constant velocity. Tominimize these technical difficulties and becausedifferences in the kinematics of dynamic contractionsmay change the discharge pattern of motor units, weimposed an identical movement velocity during muscleshortening and lengthening. The protocol required thesubject to sustain the discharge of an identified motorunit during isometric contractions at two muscle lengthsand during shortening and lengthening contractionsof the dorsiflexors. All motor units (n = 63) activatedduring the initial isometric contraction at long musclelength discharged continuously throughout the task,including the lengthening contraction. Furthermore, therecruitment of an additional motor unit was observedat 18 recording sites during the shortening contraction.These additional motor units had a greater force thresholdthan the units that were active from the beginning ofthe task and were recruited to maintain the requiredtorque during muscle shortening. They continued todischarge during the subsequent isometric contractionat the short muscle length and were derecruited duringthe lengthening or isometric contraction at the longmuscle length. The derecruitment during the lengtheningcontraction was always observed at a more extended ankle



joint angle (fascicle length) than during the shorteningcontraction (Fig. 3A). In all the trials when the recruitmentof another motor unit was observed during the shorteningcontraction, the unit recruited initially remained activebeyond the derecruitment of the later-recruited unit. Inagreement with previous studies (Garland et al. 1994;Søgaard et al. 1996; Bawa & Jones, 1999; Stotz &Bawa, 2001; Semmler et al. 2002), these observationsindicate that recruitment order was preserved during slowshortening and lengthening contractions at a constantvelocity.

As for studies that have compared populations of motorunits (Søgaard et al. 1996; Linnamo et al. 2003; Del Valle& Thomas, 2005), the average discharge rate of the samemotor unit was lower during lengthening compared withshortening contractions in our study. After the transientincrease or decrease in discharge rate due to the stretchor unloading reflex, respectively (Fig. 2), the modulationof motor unit discharge differed for the two contractiontypes when compared for a similar change in fasciclelength and torque. The rate of motor unit discharge wasnearly constant during the entire lengthening contractionand slightly greater than that recorded during theisometric contractions at short and long muscle lengths. Incontrast, motor unit discharge rate increased progressivelyup to the end of the movement during shortening contra-ctions and reached greater values than during isometricconditions. The greatest difference between shorteningand lengthening contractions was observed when themuscle was at a short length due to an increased neuralactivation that was required to compensate for the reducedmuscle force capacity at that length. A similar behaviourwas observed for motor units recruited during the courseof the task. These findings indicate that rate codingis more important during shortening than lengtheningcontractions (Del Valle & Thomas, 2005). The greatermotor unit recruitment in isometric contractions at shortmuscle length, although similar discharge frequencies wererecorded at the two muscle lengths (Pasquet et al. 2005),further suggests that recruitment is more related to musclelength and that rate coding is critical during shorteningcontractions. It could be argued that the torque producedduring shortening and lengthening contractions relativeto their respective MVCs can be slightly less in the lattercondition and might have reduced the absolute dischargerate. Although this possibility cannot be excluded, it isunlikely that the contrasting modulation of motor unitsdischarge rate during the two contraction types would beinfluenced when there was a smooth change in torquebetween the two targets. Furthermore, in the inaccuratetrials recorded during lengthening contractions, duringwhich the subject overshot the target torque and a greaterrelative dorsiflexion torque was produced, motor unitsdischarge rate did not increase when compared with theaccurate trials.

The contribution of the other synergistic muscles(extensor hallucis longus, extensor digitorum longusand peroneus tertius) to the torque developed bythe dorsiflexors during ankle movement could haveinfluenced the recruitment–derecruitment and dischargeof motor units in the current study. Although the relativecontributions of these muscles to the net dorsiflexor torquecould change during shortening and lengthening contra-ctions, these muscles are all monoarticular with extensiveretinaculum systems surrounding the distal tendons andare likely to experience only a minor relative variation inthe moment arms during the small (20 deg) ankle rotation.Also, the similar excursion for these muscles suggests thatthe length–tension curves probably did not differ greatly(Rassier et al. 1999). Furthermore, when an additionalmotor unit was derecruited during muscle lengthening,the constant discharge rate of the unit that remained active(see Fig. 4) indicates that the synaptic excitatory drive tothe motor neurone pool was not greatly reduced at a timethe second unit ceased to discharge.

The similar recruitment order during shortening andlengthening contractions in our study implies that thenervous system employs a single size-related strategy toactivate the involved motor neurones in the different typesof contractions. The contrasting modulation of motorunit discharge rate in the two contraction types, however,indicates a difference in the distribution of the sensoryinputs to the motor neurone pool together with a possiblechange in the supraspinal command (Nielsen, 2004).Spinal networks do appear capable of controlling afferentinput for specific tasks (Rudomin, 1999). Accordingly, thegreater amplitude of the motor evoked potential inducedby transcranial magnetic and electrical stimulationduring shortening contractions suggests that excitationof the motoneurone pool is reduced during lengtheningcontractions (Abbruzzese et al. 1994; Sekiguchi et al. 2003).Furthermore, the amplitude of the Hoffmann (H) reflexappears to be modulated in a similar manner as fortranscranial stimulations (Romano & Schieppati, 1987;Abbruzzese et al. 1994; Nordlund et al. 2002). Despite aslightly greater level of coactivation during lengtheningcontractions in the present study, the similar modulationof the H reflex at rest and during contraction (Abbruzzeseet al. 1994) discounts a key role for reciprocal Ia inhibitionand autogenic Ib inhibition in the excitation of themotoneurone pool. Rather, the comparable variationin both magnetically and electrically evoked motorresponses and in the H reflex suggests that the effectwas mediated by mechanisms located in the spinal cord,presumably presynaptic in origin (Abbruzzese et al. 1994).Because muscle spindle activity is increased to a greaterextent during lengthening than shortening contractions(Burke et al. 1978), centrally and peripherally regulatedpresynaptic mechanisms (Hultborn et al. 1987; Moritaet al. 1998) might explain the different modulation of



motor unit discharge rate during the two contractiontypes. This possibility is consistent with the observationthat, regardless the level of voluntary drive, the meandischarge rate of motor neurones is lower when deprived ofmuscle afferent feedback (Macefield et al. 1993). Becauselengthening contractions are more difficult to controlthan shortening contractions (Nordlund et al. 2002;Semmler et al. 2002), depression of Ia excitation frommuscle spindles may facilitate an accurate performance ofthe task.

In conclusion, the current study demonstrated thatsubmaximal lengthening contractions at constant velocityinvolved a specific modulation of motor unit dischargerate with no change in motor unit recruitment order.This behaviour contrasted with that observed duringshortening contractions, despite a similar linear changein fascicle length and torque during the two tasks.These observations indicate that recruitment order ispreserved during submaximal lengthening contractionsat a slow constant velocity, but that motor unitdischarge is modulated less compared with shorteningcontractions.

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Acknowledgements

The authors are particularly grateful to Professor R. Enoka and

Dr K. Keenan for useful comments on this paper. We would

also like to thank Professor M. Narici for his helpful advice

regarding ultrasonography, and Ms A. Deisser for assistance in

the preparation of the manuscript. This study was supported by

the Universite Libre de Bruxelles and the Fonds National de la

Recherche Scientifique of Belgium.


specific modulation of motor unit discharge for a similar change in

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