The effects of isometric resistance training on stretch reflex induced tremor in the knee extensor...

The effects of isometric resistance training on stretch reflex induced tremorin the knee extensor muscles

Rade Durbaba,1 Angela Cassidy,2 Francesco Budini,3,4 and Andrea Macaluso3

1Department of Applied Sciences, Faculty of Health and Life Sciences, Northumbria University, Newcastle, United Kingdom;2Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, Glasgow, United Kingdom;3Department of Human Movement and Sport Sciences, University of Rome Foro Italico, Rome, Italy; 4Institute for Sportand Health, University College Dublin, Dublin, Ireland

Submitted 21 July 2011; accepted in final form 4 April 2013

Durbaba R, Cassidy A, Budini F, Macaluso A. The effects ofisometric resistance training on stretch reflex induced tremor in theknee extensor muscles. J Appl Physiol 114: 1647–1656, 2013. Firstpublished April 11, 2013; doi:10.1152/japplphysiol.00917.2011.—This study examines the effect of 4 wk of high-intensity isometricresistance training on induced tremor in knee extensor muscles.Fourteen healthy volunteers were assigned to either the training group(n � 7) or the nontraining control group (n � 7). Induced tremor wasassessed by measuring force fluctuations during anisometric contrac-tions against spring loading, whose compliance was varied to allowfor preferential activation of the short or long latency stretch reflexcomponents. Effects of high-intensity isometric resistance training oninduced tremor was assessed under two contraction conditions: rela-tive force matching, where the relative level of activity was equal forboth pre- and post-training sessions, set at 30% maximum voluntarycontraction (MVC), and absolute force matching, where the level ofactivity was set to 30% pretrained MVC. The training group experi-enced a 26.5% increase in MVC in contrast to the 0.8% for the controlgroup. For relative force-matching contractions, induced tremor am-plitude and frequency did not change in either the training or controlgroup. During absolute force-matching contractions, induced tremoramplitude was decreased by 37.5% and 31.6% for the short and longcomponents, respectively, with no accompanying change in fre-quency, for the training group. No change in either measure wasobserved in the control group for absolute force-matching contrac-tions. The results are consistent with high-intensity isometric resis-tance training induced neural changes leading to increased strength,coupled with realignment of stretch reflex automatic gain compensa-tion to the new maximal force output. Also, previous reported reduc-tions in anisometric tremor following strength training may partly bedue to changed stretch reflex behavior.

gain realignment; tremor; steadiness; force fluctuations; motor control

THE ABILITY TO MAINTAIN STEADY force during contractions of thelower limb is important for mobility and steadiness and isknown to be impaired in older adults (2, 7, 23, 36, 41, 53, 60,70, 84, 85, 86). As this impairment is seen for both isometricand anisometric contractions, it is suggested that neural mech-anisms such as decreased number of motor units (56, 57) andincreased variability of discharge (46) could be responsible.High-intensity resistance training, either isometric or anisomet-ric, is known to restore some of this loss in function (41, 53, 67,77, 84, 86), as well as leading to an increase in maximal forceproduction. An interesting feature of note was that improve-ments in steadiness were specific to submaximal anisometric

contractions (41, 53, 84, 86). This implies that high-intensityresistance training may be influencing neural circuitry that isassociated more with steadiness in anisometric contractionsthan isometric and thus could implicate some change in be-havior to neural circuitry involved in monitoring length,namely the muscle spindle and the stretch reflex pathway.

Various studies have shown that self-maintaining force fluc-tuations, hereafter referred to as induced tremor, occur whencontracting anisometrically under appropriate compliant load-ing, that are not present during isometric contractions. Thisinduced tremor during anisometric contractions has been at-tributed to the stretch reflex pathway (21, 24, 43, 50, 55, 78, 79,88). Indeed, Durbaba et al. (21) showed that in the digastricmuscle, which is naturally devoid of muscle spindles and hencelacks a stretch reflex, it was not possible to induce tremor. Inaddition, other studies have indicated a role for the stretchreflex in contributing to “physiological tremor” (9, 24, 31, 34,40, 72, 80, 81).

The question then arises what the link is between the stretchreflex and reductions in force fluctuations following resistancetraining. As high-intensity resistance training leads to an in-crease in maximal force production, it is possible that thereductions are linked to the “relative” levels of activity pre- andposttraining and the behavior of the stretch reflex pathway tothese different levels of activity.

It is known from experimental and modeling studies that theresponse of the stretch reflex pathway, measured either asreflex torque, electromyogram (EMG) amplitude, or reflexgain, shows a bell-shaped relationship to the background levelof activity, with an increase in gain up to 30–40% maximumvoluntary contraction (MVC), a plateau region between 40 and50% MVC, followed by a decline for high contraction levels(5, 8, 11, 35, 54, 61, 83). This is known as automatic gaincompensation. A similar behavior has been observed for theamplitude of induced tremor during anisometric contractions atthe elbow against a compliant load (43, 55). Thus if, followinghigh-intensity training, automatic gain compensation is “re-aligned” to the new maximal force production, then the re-sponse of the stretch reflex pathway at any “relative” level ofactivity should be the same pre- or post-training. This wouldimply that reductions in force fluctuations during anisometriccontractions seen in the lower limb following training, could bedue to a lower response of the stretch reflex pathway associatedwith a lower “relative” level of activity post-training.

The purpose of this study was to examine the effects of 4 wkhigh-intensity isometric resistance training using a protocolthat is known to produce an increase in maximal force produc-tion (52) on induced tremor in knee extensors during aniso-

Address for reprint requests and other correspondence: R. Durbaba, Depart-ment of Applied Sciences, Faculty of Health and Life Sciences, EllisonBuilding, Northumbria University, Newcastle upon Tyne, UK, NE1 8ST(e-mail: [email protected]).

J Appl Physiol 114: 1647–1656, 2013.First published April 11, 2013; doi:10.1152/japplphysiol.00917.2011.

8750-7587/13 Copyright © 2013 the American Physiological Societyhttp://www.jappl.org 1647

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metric contractions against a compliant load. We hypothesized,for submaximal (�30% MVC) anisometric contractions, that1) during a relative force-matching contraction task, where therelative level of activity pre- and post-training are the same(30% MVC), following training there will be no change ininduced tremor; and 2) during an absolute force-matchingcontraction task, where the relative level of activity post-training will be less than pretraining, training would result in adecrease in the amplitude of induced tremor. We would attri-bute the lack of change and the reduction in induced tremor forrelative and absolute force-matching contraction tasks, respec-tively, to be due to a realignment of automatic gain compen-sation for the stretch reflex pathway to the new maximal forceproduction post-training. Preliminary results have been pub-lished in abstract form (20).

METHODS

Participants. With approval of the Ethics Committee of the Uni-versity of Strathclyde, 14 individuals [aged 28.5 � 6.8 yr (mean �SD); body mass 74.6 � 19.1 kg; stature 1.76 � 0.11 m], 9 males and5 females, were matched for maximal isometric force of their quad-riceps muscle and randomly assigned to either training or controlgroup. Volunteers provided written informed consent and were in-structed to maintain their usual levels of physical activity throughoutthe duration of the study. After completing a familiarization sessionon a separate day, all participants were tested before the onset oftraining (week 0) and then the assessment was repeated after training(week 4).

Recording apparatus. Knee extension torque of the dominant legwas recorded using a dynamometer (Biodex System 3, Biodex Med-ical System, Shirley, NY). The participants were seated comfortablyin the dynamometer chair, with their trunk erect and fastened by twocrossing belts, with the angle at the hip and knee being set to 90°. Thetorque motor of the Biodex was placed behind the seated subject. Thelever arm of the torque motor was locked in a vertical position,pointing toward the ground and was linked to the subject to allow foreither isometric or anisometric contractions. The linkage was attachedto the subject via a noncompliant cuff placed around the lower leg,with the cuff’s bottom edge about 1 cm above the malleolus. With thisarrangement the only rotation that could occur was at the knee of thesubject. The sensitivity of the torque transducer was 139 N·m·V�1,and since the length of the lever arm was set to 0.5 m for all subjects,the force sensitivity was 278 N/V. The force output from the Biodexwas accessed and two signals extracted. The first was the DC forceoutput, which provided a feedback to the subjects on a computerscreen to assist them in maintaining the requested levels of contrac-tion. The second signal was an AC coupled version of the output, toallow for the amplification of irregularities in force during the steadystate period of the contraction. Both signals were low-pass filtered at100 Hz, while the AC-coupled version of the force was also high-passfiltered at 0.5 Hz. The two force signals were A/D converted, using theCambridge Electronic Design (CED) Power1401 system, and cap-tured at a sampling rate of 2000 Hz using the CED Spike2 package.Data files were stored on computer for off-line analysis.

Force output from an individual was assessed isometrically andanisometrically. Isometric recordings were achieved by contractingagainst the dynamometer lever arm through an inextensible rod. Toachieve anisometric recordings, a spring of appropriate stiffness wasinserted between the cuff and the dynamometer lever arm, with theinextensible rod being shortened to maintain a 90° knee angle. Underanisometric conditions, the frequency at which oscillation might beexpected to occur is very much dependent upon the spring stiffnessand the total inertia of the moving parts. The resonant frequency (fr)of a spring-mass system rotating about a pivot point can be deter-mined by the equation

f r � �1 ⁄ 2�� k � d2 ⁄ IT�0.5 (1)

where k and IT are the spring stiffness and total inertia of the system,respectively, and d is the distance from the pivot to the point ofattachment of the spring (� 38 cm; knee joint to middle of cuff). Twosprings of different stiffness were used, 5.35 N/mm and 11.06 N/mm.The total inertia can be expressed as

IT � IL � ISp (2)

where IL and ISp are the inertial components for the lower limb belowthe knee and spring, respectively. The simplest model for the leg is toassume that it is made up of two cylinders representing the shank andthe foot. Thus

IL � IShank � IFoot (3)

where IShank is the inertia of the shank about the knee joint, and IFoot

the inertia of the foot about the ankle joint but also taking into accountthat the foot rotates about the knee joint. The equations for IShank andIFoot are

IShank � �MS ⁄ 12� � �3SR2 � 4SL

2� (4)

IFoot � ��MF ⁄ 12� � �FL2 � 3FR

2 �� MF � ��FL ⁄ 2� � SR�2

� MF � �SL � FR�2 (5)

where MS, MF, SL, FL, SR, and FR are the masses, lengths, and radiiof the shank and the foot, respectively. With the exception of SR,estimates of mean values for these measures could be computed basedon simple scaling factors related to whole body mass or length (49,87). For whole body mass or length, we used the mean values for theindividuals recruited for this study. An estimate of the mean shankradius was made from measures taken from cadavers. Using thesemean values, we computed mean inertial values for the shank and footof 0.22 and 0.28 kg·m2, respectively, giving the total mean inertialcomponent due to the leg below the knee of 0.50 kg·m2.

The inertia due to the spring was modeled as a thick-walled hollowcylinder and took into account how its point of attachment relates tothe rotation about the knee joint. The equation for ISp is

ISp � �MSp ⁄ 12� � �3�Ro2 � Ri

2� � 4L2� � �MSp � d2� (6)

where MSp, Ro, Ri, and L are the mass, outer and inner radii, andlength of the spring, values for which were obtained by weighing andmeasuring the springs. The inertial components due to the 5.35 N/mmand 11.06 N/mm springs were calculated to be 0.08 and 0.04 kg·m2,respectively. Thus, by combining appropriate inertial components andspring stiffnesses together, it was computed that the resonant fre-quency of the spring-mass system associated with the 5.35 N/mm and11.06 N/mm springs would be 5.85 and 8.72 Hz, respectively.

In addition to the spring-mass element, it is necessary to considerthe contribution of the whole oscillating system in determining thefinal expected oscillation frequencies. To do this, the model developedby Durbaba et al. (21) was modified to represent the behavior aboutthe knee. The above-computed frequencies for the spring mass systemwere incorporated into the model, along with a second-order criticaldamped element relating EMG to force output from the muscle andmuscle spindle afferent feedback. Only Ia afferent feedback is mod-eled, as this is generally accepted as being the principal sensoryfeedback related to induced tremor (24, 31, 43, 50, 55). A feature ofthe model is the neural loop delay related to the stretch reflex. As weare only considering Ia afferent feedback, then only neural delaysrelated to the short and long latency components need be considered,as the medium latency component is thought to be predominantly dueto secondary (group II) muscle spindle afferent input (74, 75). Ideally,the model should include the short and long components together, interms of synaptic gain and their relative interaction at the level of thealpha motoneurone. However, these are not known. Therefore the twocomponents were modeled separately as though they “dominated” thereflex contribution to the induced tremor for each of the springs used.

1648 Resistance Training and Stretch Reflex Induced Tremor • Durbaba R et al.

J Appl Physiol • doi:10.1152/japplphysiol.00917.2011 • www.jappl.org

The mean latency for the short component was taken as 25 ms and thatfor the long component as 78 ms (62). Thus for the whole oscillatingsystem, the expected frequencies of oscillation were 5.6 and 5.0 Hzfor the short and long components when using the 5.35 N/mm springand 8.4 and 5.3 Hz for the 11.06 N/mm spring.

Experimental protocol. A recording session consisted of two parts.At the start of the session the strength of the knee extensors of thedominant leg of an individual was assessed by asking them tovoluntarily contract to their maximum effort (maximum voluntarycontraction; MVC) and hold there for 3 s, before returning to the restposition. During the MVC, participants followed their performance ona computer screen and were verbally encouraged to achieve a maxi-mum, in an attempt to exceed the previous force recording. MVC wascalculated as the largest 1 s average reached within any single forcerecording. Three attempts were performed, separated by 5 min, andthe greatest of the three attempts was chosen as MVC. After the lastMVC participants rested for 20 min prior to making the tremorrecordings. During this part of the recording session volunteers wereasked to contract anisometrically, against a compliant spring, to aparticular level of force and to hold at this level for 20 s beforereturning to rest. Both the target force and the actual force weredisplayed on a computer screen to provide feedback to the subjects.Individuals repeated the contractions four times with a 2 min restingperiod occurring between contractions to minimize the effects offatigue. Thus two sets of anisometric contraction were recorded, onefor each spring, in a random order, with a 5 min rest period betweensets. For the pretraining session (week 0) the level of force requiredduring anisometric contractions was 30% of their MVC. In thepost-trained recording session (week 4), in addition to contracting totheir new 30% MVC (referred to as “relative force matching”)subjects also performed contractions at a force level equivalent to30% of their “pretraining” MVC (old 30% MVC force, referred to as“absolute force matching”).

Strength training. The training protocol used in this study wasidentical to that used by Macaluso et al. (52). The protocol was chosenas it has been observed to be effective in increasing MVC force outputby 20% following 4 wk of training. Participants took part in a 4-wkperiod of isometric resistance training involving the knee extensormuscles of the dominant leg, three times a week, for about 45 min persession. Each training session consisted of a total of 15 sets, 10repetitions each (5 s contraction, 3 s rest). Each subject started with 2sets at 20% MVC, followed by 2 sets at 40% MVC, 4 sets at 60%MVC, 3 sets at 80% MVC (only 8 repetitions each), 2 sets at 40%MVC and finally 2 sets at 20% MVC. The interval time between eachset was 15 s at 20% MVC, 30 s at 40% MVC, 2 min at 60% MVC,and 3 min at 80% MVC. The resting period at the end of each set was15 s after 20% MVC, 1 min after 40% MVC and 3 min after 60%MVC and 80% MVC. In the subsequent training weeks, the load foreach set was increased by 5% each week, to maintain a high trainingintensity.

Data analysis. All force signals were converted off-line into New-tons by multiplying the voltage by the force sensitivity (see above).For anisometric contractions, the A/C coupled force trace was furtherdividing by the appropriate stiffness to obtain displacement in milli-meters. The steady state period of each of the four 20 s contractionsof a set were combined and the autospectra of the displacement signalwere constructed by fast Fourier transformation (FFT) using in-builtfunctions of the CED Spike2 analysis package. Each spectra rangedfrom DC to 15 Hz, with a resolution of 0.488 Hz, which for simplicityis considered to be 0.5 Hz. Frequencies above 15 Hz were not requiredas they had no relevance to this study. Also, the high-pass filteringrenders the DC to 1 Hz components meaningless so these were notplotted. Spectra were plotted on linear amplitude scales. The com-puted spectra were then inspected to determine the amplitude andfrequency of any principal rhythmic components that might have beenpresent, which reveal themselves as a peak about a frequency ofoscillation. If a peak was present, then its amplitude was expressed as

the root mean squared amplitude (ARMS), where ARMS is √(PT/2) andPT is the total power within the peak, with the peak being defined asthe bin where maximum power occurred �3 bins. This approach wasused to take into account that with the application of a windowingfunction, such as a Hanning window, to counteract the sharp start/endtapering effects of data sections used for the FFT analysis there is aloss in power of the signal at the expected frequency. Also, this isaccompanied by a spread of the signal into one or more adjacent binsaround the expected. Thus one would underestimate the amplitude bysimply taking the value at the maximum power of the peak. Frequencyof oscillation (fo) of the induced tremor was taken to be the frequencyof the bin that corresponded to the maximum power of the peak.

Statistical analysis. All data were normally distributed in terms ofkurtosis and skewness (all values �2). Statistical comparisons of theparameters (MVC, ARMS, fo) between the two groups (training andcontrol) across time (week 0 and week 4) were carried out usingtwo-way repeated-measures ANOVA, followed by post hoc Student’spaired and unpaired t-tests where appropriate. Comparisons of fo

between the predicted values from the model and the experimentaldata were carried out by single sample t-test. Statistical significancelevel was set at P � 0.05 and all statistical procedures performedusing SPSS software. Unless otherwise specified, data were presentedas mean � standard error.

RESULTS

There were no significant differences in any of the variablesmeasured between the two groups at week 0 (P � 0.05). Nosignificant changes were observed in any of the anthropometricmeasurements at any time point (P � 0.05). Compliance of theexercise group with the exercise protocol was 100% and noinjuries related to training occurred.

Effect of training on MVC force. The ANOVA for MVCforce showed a significant effect of time and a significant groupby time interaction (F � 21.2, P � 0.001). The post hocanalysis showed that at week 0 there were no differences inMVC force between the control and training groups. Followingthe intervention, there was a significant increase across time inthe training group by 26.5% (P � 0.01, 534 � 75 N at week 0,676 � 82 N at week 4), compared with the 0.8% increase in thecontrol group (P � 0.05, 589 � 42 N at week 0, 593 � 47 Nat week 4).

Stretch reflex induced tremor in a control subject. Fig. 1, Aand B, show 1 s segments of displacement recordings from acontrol participant during anisometric contraction at 30%MVC, with the 5.35 N/mm and 11.06 N/mm springs, respec-tively. Visual inspection shows no difference in the amplitudeor the frequency of oscillation between week 0 and week 4.Figure 1, C and D, show the amplitude autospectra of thedisplacement recordings from Fig. 1, A and B. A clear peak isseen centered at about 4.5 Hz and 8 Hz in Fig. 1, C and D,respectively, and which show no change between weeks 0 and4. For this individual, the observed frequencies of oscillationare lower than the expected values for the two springs. Quan-titative analysis of the ARMS of the peaks revealed no changebetween weeks 0 and 4 (370 and 362 �m for Fig. 1C and 210and 203 �m for Fig. 1D). A similar lack of change wasobserved in the other six control subjects.

Effect of strength training on stretch reflex induced tremor.Figure 2, A and B, shows 1-s segments of displacementrecordings from a training participant during anisometric con-tractions with the 11.06 N/mm spring for the absolute andrelative force-matching protocols, respectively. Prior to thetraining intervention, this individual showed oscillations in

1649Resistance Training and Stretch Reflex Induced Tremor • Durbaba R et al.


displacement with peak-to-peak amplitude of �0.6 mm and afrequency of about 8 Hz. Following the training intervention,when the subject was asked to do anisometric contractionsunder the absolute force-matching protocol, there is a reductionin the amplitude of the oscillation but no change in thefrequency of oscillation (Fig. 2A). This reduction in amplitudeis clearly seen in Fig. 2C, which shows the amplitude auto-spectra for the records in Fig. 2A. There is a 55% reduction inARMS with no change in frequency. In contrast, with therelative force-matching protocol there was no change in am-plitude of oscillation (Fig. 2, B and D). As in the case of

absolute force-matching, during relative force-matching thefrequency of oscillation did not change. When this subject wasasked to contract using the 5.35 N/mm spring, the samebehavior was observed, though the oscillations occurred at alower frequency. A similar pattern was observed in the othersix training subjects.

Tremor amplitude. Figure 3 shows a comparison of theARMS of the induced tremor for control and training groupsbetween week 0 and week 4. The top and bottom rows in Fig.3 relate to 5.35 N/mm and 11.06 N/mm springs, respectively.For the subjects in the control group, no consistent change in

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DCFig. 1. A and B: 1 s segments of week 0 (blackline) and week 4 (gray line) anisometric recordsfor 5.35 N/mm and 11.06 N/mm springs, re-spectively, of a control subject. C and D: auto-spectra relating to full records from A and B;week 0 is represented by a black line, and week4 is represented by a gray line.

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Fig. 2. A and B: 1 s segments of week 0 (blackline) and week 4 (gray line) anisometric re-cords for the 11.06 N/mm spring for absoluteand relative force-matching contraction tasks,respectively, of a training group subject.C and D: autospectra relating to full recordsfrom A and B. See Fig. 1 for symbol legend.



ARMS was observed from week 0 to week 4 (filled circles, Fig.3, A and D). Within the training group, for the absoluteforce-matching condition all subjects showed a clear decreasein ARMS at week 4 compared with week 0 for either spring(filled circles, Fig. 3, B and E), while for the relative force-matching condition no consistent change in ARMS was ob-served (filled circles, Fig. 3, C and F).

In the absolute force-matching condition, ANOVA showed asignificant effect of time and a significant group by timeinteraction in induced tremor ARMS for either spring used (F �5.34 for the 5.35 N/mm spring; F � 5.58 for the 11.06 N/mmspring; P � 0.05). Post hoc analysis revealed that at week 0there was no difference in ARMS between control and traininggroups (open circles on left-hand axes of Fig. 3). For thecontrol group, there was no significant difference betweenweek 0 and week 4 for either spring (open circles, Fig. 3, A andD). In the training group, the mean induced tremor ARMS

reduced from 181 � 26 �m at week 0 to 124 � 23 �m at week4 (a 31.6% reduction; open circles, Fig. 3B) and from 112 � 30�m at week 0 to 70 � 13 �m at week 4 (a 37.5% reduction;open circles, Fig. 3E) for the 5.35 N/mm and 11.06 N/mmsprings, respectively. In the case of the 5.35 N/mm spring thisreduction was significant (P � 0.01), while for the 11.06N/mm spring the reduction did not quite reach significance(P � 0.068) despite the greater relative reduction in meaninduced tremor ARMS. In the case of the relative force-match-ing task, there were no significant differences in ARMS in bothgroups for either spring.

Tremor frequency. Figure 4 shows a comparison of thefrequency of oscillation of the induced tremor for control andtraining groups between week 0 and week 4. As in Fig. 3, thetop and bottom rows in Fig. 4 relate to 5.35 N/mm and 11.06N/mm springs, respectively. No consistent change in frequencywas observed from week 0 to week 4 for the subjects in thecontrol group or for those in the training group in either theabsolute or relative force-matching conditions.

ANOVA showed no significant effect of time and no sig-nificant group by time interaction in induced tremor frequencyfor either spring used, and this is reflected in Fig. 4 whichshows the mean values for tremor frequency for each groupand contraction task (open circles). This lack of change ininduced tremor frequency is consistent with a lack of change inthe dynamics of the system being tested. Owing to the lack ofdifference between groups for each spring or contraction task,it was decided to combine the observed values between groups.Thus for the 5.35 N/mm spring the mean frequency of oscil-lation was 5.1 � 0.1 Hz, while for the 11.06 N/mm spring itwas 8.0 � 0.1 Hz.

When these values were compared with the predicted valuesfrom the model, it was observed that in the case of the 5.35N/mm spring, the computed mean value differs significantlyfrom that expected when the short latency pathway dominates(P � 0.01; predicted � 5.6 Hz) but not when the long latencypathway dominated the oscillations (P � 0.05; predicted � 5.0Hz). This suggests that for the 5.35 N/mm spring, the oscilla-tions were being generated with a strong influence from the

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Fig. 3. Root mean squared amplitude (ARMS)values at week 0 and week 4 for the (top) 5.35N/mm and (bottom) 11.06 N/mm springs. A andD: control group. B and E: training group abso-lute force-matching condition. C and F: traininggroup relative force-matching condition. Filledcircles with solid lines represent individual sub-jects in each group. Open circles with dashedline represent mean values. *Significantly dif-ferent between week 0 and week 4 at the P �0.01 level.



long latency stretch reflex pathway. For the 11.06 N/mmspring, the computed mean value was significantly differentfrom the expected values from the model for both the short andlong latency pathway, P � 0.05 (predicted � 8.4 Hz) andP �� 0.001 (predicted � 5.3 Hz), respectively.

DISCUSSION

The main finding of this study was that 4 wk of high-intensity isometric resistance training lead to a contraction taskspecific reduction in induced tremor amplitude during aniso-metric recordings in healthy young individuals, which accom-panied the increased level of maximal voluntary contraction.

The 26.5% increase in maximal voluntary strength observedin the training group is similar to that found by others over anequivalent period of training (12, 44, 52, 58, 68). It has to benoted that direct comparison between studies is difficult, sincemany variables, such as the intensity, the number of sets andrepetitions of a given exercise, the muscle groups exercised,and the subjects’ group (e.g., age, sex), must be considered. Wechose an isometric resistance training program that has previ-ously shown to be effective in increasing maximal isometricvoluntary strength by 20% after 4 wk of training (52). Giventhe period of training, 4 wk, it seems likely that this increasecan be attributed mostly to neural adaptations of the trainedmuscle, rather than structural changes to the trained muscleitself (33, 51, 59, 71), although the evidence is far fromconclusive (28). Neural adaptations include, among other fac-

tors, improvements in agonist surface EMG amplitude, whichmight be related to either increased motor unit recruitment orfiring rate of single motor units (51), with concurrent reduc-tions in the activity of antagonist muscles (32), an increasedcorticospinal excitability (10), although some studies reportedan unexpected decrease in corticospinal excitability (6, 42, 47),or reduced presynaptic inhibition of spinal reflexes (39, 45).

The possibility that tremor could arise due to the stretchreflex has been studied previously (21, 43, 50, 55, 71, 78, 79,88). These studies have tended to emphasize the contributionplayed by the spinal, or short latency, stretch reflex, with littleconsideration to the long latency pathway. The modelingdescribed in the Methods section indicates that the long latencypathway does have the potential to induce instability, with atendency toward oscillations having a lower frequency than forthe short latency component. As both components of thestretch reflex can be seen in muscles that activate knee exten-sors (62), it seems likely that these frequencies are derived asa result of the individual responsiveness of the two pathwaysand their relative interaction. As we do not know what theseinteractions and their values are, our modeling was based onpredicting expected frequency values with each componentdominating the reflex behavior of the system. Compared withthe expected values from the modeling study, there is a sug-gestion that one pathway may dominate the other for eachparticular spring. Thus, for the 11.06 N/mm spring, the ob-served mean frequency of induced tremor (8.0 Hz) though not

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matching the expected value for the short latency pathway, isnevertheless at the lower limit of the generally accepted rangeof frequency values (8–12 Hz) for tremor linked to shortlatency stretch reflex activity (21, 43, 50, 55, 71, 78, 79, 88).Therefore it seems likely that in our setup the short latencypathway may be the dominant pathway for inducing tremorwhen using the 11.06 N/mm spring, though a contribution fromthe long latency pathway cannot be excluded. For the 5.35N/mm spring, the long latency pathway appears to dominatewith there being no significant difference between the meanobserved frequency and the expected value from the modelingfor a dominant effect via the long latency pathway. This agreeswith previous experimental and modeling studies relating topossible role for long loop reflex being able to generate tremorat 4–6 Hz (29, 66, 78, 79, 80, 88). There is some evidence tosuggest that the long latency reflex might be involved in thegeneration of tremor in Parkinson’s disease or drug-inducedParkinsonism, through increased loop gain (25, 82). Also,Deuschl et al. (14) found that Essential Tremor patients couldbe subdivided according to long loop reflex behavior, with onegroup having increased long loop reflex amplitudes. This groupof patients exhibited a lower tremor frequency than the groupwhose long loop reflex was normal. Therefore using springs ofappropriate stiffness to mimic tremor frequencies associatedwith pathological tremors could be a useful tool for assessmentof associated neural pathways.

It is important to recognize that there are limitations withany modeling relating to the choice of values used for theparameters. In our model the critical calculation relates to thatof lower leg inertia. With the exception of the shank radius, todetermine appropriate mass, length, and radii of the shank andfoot we used a mean value for scaling factors from publisheddata (49, 87). If we consider the upper and lower limits of thepublished scaling factors and taking the �5% variation forshank radius, then it is possible to calculate that the potentialrange of values of total inertia for the lower limb is between0.48 and 0.51 kg·m2. This translates itself to a �1.5% variationin either the resonant frequency of the spring-mass systemalone or expected frequency of the whole oscillating system.This degree of variation does not affect our conclusions relat-ing the oscillation frequency to a dominant reflex component.

Previous studies have examined the effect of strength train-ing on steadiness of knee extensor contractions (3, 41, 53, 84,86). All these studies reported that strength training resulted ina reduction in force fluctuations when subjects contractedanisometrically but not during isometric contractions. As in-duced tremor has been reported to occur during anisometriccontractions and not during isometric contractions (21, 50, 55),this reported difference of the effect of strength training on theanisometric and isometric contracted states would be consistentwith the idea that the reductions might be mediated via thestretch reflex pathway. Hortobagyi et al. (41) found a reductionin force fluctuations of 31% and 30% for eccentric and con-centric absolute force-matching anisometric submaximal con-tractions. Subsequent studies were all carried out using relativeforce-matching eccentric and concentric anisometric submaxi-mal contractions (53, 84, 86), and they also found a reductionin force fluctuations. This is in contrast to the present studywhere no change was observed during relative force-matchingcontractions. Though the previous studies examined trainingon elderly adults, while in our study the subjects were young,

it seems unlikely that age could account for the differenceobserved during a relative force-matching task, as similarneural and muscular changes have been reported for young andolder individuals following resistance training (2, 28, 51).Instead, differences may be related to some methodologicalaspects. First, different forms of anisometric contractions wereused, namely isokinetic concentric and eccentric contractionsin the previous studies (53, 84, 86) as opposed to the “steady-state” contraction against a compliant spring in this study.During a lengthening contraction, stretch reflex activity forboth the short and long latency component is decreased com-pared with a constant load contraction, while for a shorteningcontraction, the short latency component shows no changecompared with constant load contraction and the long latencypathway is increased (17, 19, 63, 65, 69). It is possible thatthese sensory feedback differences coupled to the differentmotor commands that occur for the different forms of aniso-metric contraction (15, 64) may be influenced by training indifferent ways and could in part explain the difference betweenthe current study and previous studies (53, 84, 86) duringrelative force-matching tasks. Further work is needed to deter-mine if this is the case. Second, length of training; 4 wk usedin our study while previous studies used either 10 wk (53) or16 wk (84, 86). Periods of training � 8 wk have been shownto lead to significant muscular changes, particularly hypertro-phy (2, 28, 30, 51). It is possible that these muscular changes,interacting with reported neural changes, might in part alsoexplain the difference between the current study and previousstudies (53, 84, 86) during relative force-matching tasks.

It is well known that the response of the stretch reflex variesas the level of muscle activity increases. Initially there is anincrease, followed by a plateau region between 40 and 50%MVC with a reduction at higher contraction levels (5, 8, 11, 35,54, 61, 83). This is the concept known as automatic gaincompensation. Our observations, that following 4 wk of high-intensity isometric resistance training, induced tremor ampli-tude did not change during the relative force-matching task butwas reduced during the absolute force-matching task could beexplained in terms of “realignment” of the automatic gaincompensation of the stretch reflex to the new maximal forceoutput that typically accompanies high-intensity isometric re-sistance training. With such a realignment, the response of thestretch reflex pathway at a particular “relative” level of activityshould be the same pre- or posttraining. Thus for a relativeforce-matching task, where the relative levels of activity arethe same pre- or post-training, the lack of reduction we ob-served would be consistent with no change in stretch reflexresponse. For the absolute force-matching task, where thepost-training activity is at a lower relative level to that pre-training, then the reduction in induced tremor amplitude can beexplained by the stretch reflex response being reduced to thatrequired for the lower level of relative activity.

Previous studies have examined the effect of resistancetraining on the behavior of the stretch reflex pathway, asassessed by the H-reflex response. Most of these studies havebeen done by assessing the H-reflex response at rest (i.e., zerocontraction) and, despite post-training increases in MVC rang-ing from 18 to 46% for training ranging from 3 to 16 wk,observed no change in H-reflex behavior (1, 13, 18, 22, 26, 27,39, 73, 76). This is perhaps not surprising given that comparingthe rest state pre- and post-training is an extreme example of



relative force matching. In addition, it is difficult to directlyrelate H-reflex behavior at rest with that which occurs during asubmaximal contraction, due to the different states of depolar-ization and cortical drive to �-motoneurones, as well as auto-matic gain compensation of the stretch reflex behavior. Indeed,Aagaard et al. (1) questioned the usefulness of relating trainingeffects on H-reflex behavior assessed at rest to muscle activa-tion. Only three studies have looked at H-reflex characteristicsduring submaximal contractions pre- and post-training andoffer some evidence of an adaptation in stretch reflex behaviorduring submaximal contractions following resistance training(13, 39, 45). Lagerquist et al. (45) found that 5 wk of MVCisometric training of plantar flexors of the ankle lead to a15.3% increase in MVC of the trained leg, which was accom-panied by a 35% increase in H-reflex amplitude post-trainingduring a 10% maximal EMG relative force-matching task. Thiswas considered to be consistent with an increase in spinalexcitability of the stretch reflex pathway following training andpotentially mediated via a reduction in presynaptic inhibitionof Ia synapses on to �-motoneurones. However, though theH-reflex amplitude was increased, the input/output character-istic of the system, reflex gain, was not changed as the slope ofthe ascending limb of the M-H recruitment curve was unalteredpost-training. Del Balso and Cafarelli (13) similarly reportedthat 4 wk isometric resistance training of ankle plantar flexorsinduced a 20% increase in MVC, but during a 20% MVCrelative force-matching task they did not observe a change inreflex, which in their study was computed as the ratio of Hslope

and Mslope, obtained from standard H-reflex and M-waveresponse/stimulus intensity curves. The lack of a change inreflex gain seen in both studies would indicate that the reflexinput is increased in proportion to changes in behavior of motoroutput following resistance training. Thus the overall behaviorof the reflex pathway pre- and post-training could be the sameat a particular relative level of background activity. Reflex gainhas been shown to be an important factor in determining tremoramplitude, with an increase or decrease leading to increased ordecreased tremor output, respectively (78, 79, 88). Our obser-vation of a lack of change in induced tremor amplitude duringrelative force-matching tasks following resistance trainingwould be consistent with the idea that there has been no changein reflex gain. The observations by Langerquist et al. (45) andDel Balso and Cafarelli (13) that reflex gain does not changefor relative force-matching tasks following training relates onlyto low-level contractions, and therefore further studies relatingreflex gain to training effects covering a wider range ofsubmaximal contraction levels are needed to confirm theirobservations and whether it can be applied to all levels ofactivity.

The only study to have examined H-reflex behavior duringsubmaximal absolute and relative force-matching contractionsfollowing resistance training is that by Holtermann et al. (39).Following training, they found for a low-level submaximalrelative force-matching contraction (20% MVC) that the H-re-flex amplitude was increased by 17.4%. When the responsewas measured for the corresponding absolute force-matchingcontraction (17% of post-training MVC) the increase was only14.8%. Also, they examined the H-reflex response at a higherlevel of submaximal contraction. For a 60% MVC relativeforce-matching task the H-reflex amplitude increased by14.7%, while a larger increase (18.5%) was observed with the

corresponding absolute force-matching task (51% of post-training MVC). The increases, irrespective of the level or thetype of contraction task, were consistent with those seen byLangerquist et al. (45), and were in part attributed to decreasedpresynaptic inhibition following resistance training. The dif-ference in the increase in H-reflex amplitude between relativeand absolute force-matching tasks at either level of contractionobserved by Holtermann et al. (39) may be explained byautomatic gain compensation. If the reported profile of auto-matic gain compensation for the stretch reflex is realigned tothe new MVC output following training, then for contractions�40% MVC a smaller overall reflex output would be observedduring an absolute force-matching contraction when the rela-tive level of activity is less than for an relative force-matchingtask. For contractions �50% MVC a larger reflex output wouldbe observed for absolute force-matching contractions despitethe decreased level of activity. Thus it is suggestive that thereduction in the amplitude of induced tremor we observeduring low-level absolute force-matching contractions follow-ing resistance training could be explained by automatic gaincompensation leading to a lower stretch reflex output. The ideathat automatic gain compensation may be realigned to the newMVC output following resistance training is a novel conceptthough might not be unexpected. Capaday and Stein (5)showed that the reported profile for stretch reflex automaticgain compensation is dependent upon the recruitment of pro-gressively larger motor units. As motor unit recruitment orderis not changed by resistance training (16), then it might be thatthe profile of stretch reflex automatic gain compensation islikewise unaltered. Investigation of stretch reflex automaticgain compensation pre- and post-training is required over thefull range of submaximal contraction levels to determine if thisis the case.

Resistance training has been shown to restore some of theloss in function in stability in the lower limb of elderlyindividuals, with improvements in steadiness specific to sub-maximal anisometric contractions (41, 53, 84, 86). On the basisof our present observations it is a reasonable assumption thatthese observed improvements may in part be due to reducedstretch reflex activity that accompanies a lower level of muscleactivity during an absolute force-matching contraction post-training.

Resistance training has also been shown to be effective inindividuals who have neuropathological tremor. Bilodeau et al.(4) found in individuals with Essential Tremor that 4 wk ofhigh-intensity strength training lead to a 13% increase inmaximal index finger abduction force, which was accompaniedby a reduction of isometric force fluctuations during absoluteforce-matching tasks only, where the relative force level wassmaller post-training compared with pretraining. This decreaseappears unlikely to be associated to the stretch reflex due to theminimal role it plays in generating instability during an iso-metric contraction (21, 50, 55). However, there is evidence toindicate that the stretch reflex may be a contributing factor tothe isometric tremor of individuals with Essential Tremor (37,38, 48). Thus it is possible that some of the loss in tremorreported by Bilodeau et al. (4) could be due to a reduction instretch reflex response, though further studies will need to becarried out on individuals with Essential Tremor to determineif this is the case.



In conclusion, the present study has shown that high-inten-sity isometric resistance training leads to a reduction in inducedtremor that is contraction task dependent. This reduction can berelated to a realignment of the stretch reflex automatic gaincompensation in relation to the new maximal force output. Thiscould in part explain the reported usefulness of resistancetraining as a rehabilitation tool for individuals with instabilityproblems associated to aging.

ACKNOWLEDGMENTS

The authors thank Chris Mercer for his help in carrying out some of theexperimental measures.

DISCLOSURES

No conflicts of interest, financial or otherwise, are declared by the author(s).

AUTHOR CONTRIBUTIONS

Author contributions: R.D. and A.M. conception and design of research;R.D., A.C., F.B., and A.M. analyzed data; R.D., A.C., F.B., and A.M.interpreted results of experiments; R.D., A.C., and F.B. prepared figures; R.D.and A.M. drafted manuscript; R.D., A.C., F.B., and A.M. edited and revisedmanuscript; R.D., A.C., F.B., and A.M. approved final version of manuscript;A.C. and F.B. performed experiments.

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The effects of isometric resistance training on stretch reflex induced tremor in the knee extensor...

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