Human Movement Science 29 (2010) 631–641

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Human Movement Science

journal homepage: www.elsevier .com/locate/humov

Corticospinal properties following short-term strengthtraining of an intrinsic hand muscle

Dawson J. Kidgell a,b,*, Alan J. Pearce b

a School of Exercise and Nutrition Sciences, Deakin University, Melbourne, Australiab Institute for Sport, Exercise and Active Living (ISEAL), Victoria University, Melbourne, Australia

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

Article history:Available online 18 April 2010

PsycINFO classification:25302540

Keywords:Transcranial magnetic stimulationCorticospinalCortical inhibitionStrength training

0167-9457/$ - see front matter � 2010 Elsevier B.doi:10.1016/j.humov.2010.01.004

* Corresponding author. Address: School of ExBurwood, 3125 Victoria, Australia. Tel.: +61 3 9251

E-mail address: dawson.kidgell@deakin.edu.au

Practicing skilled tasks that involve the use of the hand and fingershas been shown to lead to adaptations within the central nervoussystem (CNS) underpinning improvements in the performance ofthe acquired task. However, neural adaptations following a periodof strength training in the hand is not well understood. In order todetermine the neural adaptations to strength training, we com-pared the effect of isometric strength training of the right first dor-sal interosseous (FDI) muscle on the electromyographic (EMG)responses to transcranial magnetic stimulation (TMS) over leftM1. The specific aim of the study was to investigate the corticospi-nal responses, including latency, motor-evoked potential ampli-tude (MEP), and silent period duration (SP) following 4 week ofstrength training of the FDI muscle. Sixteen healthy adults (13male, three female; 24.12 ± 5.21 years), were randomly assignedinto a strength training (n = 8) or control group (n = 8). Corticospi-nal measures of active motor threshold (AMT), MEP amplitude, andSP duration were obtained using TMS during 5% and 20% of maxi-mal voluntary contraction force (MVC) pre and post 4 weekstrength training. Following training, MVC force increased by33.8% (p = .01) in the training group compared to a 13% increase(p = .2) in the untrained group. There were no significant differ-ences in AMT, latency, or MEP amplitude between groups follow-ing training. However, in the trained group, there was a 16 msreduction in SP duration at 5% of MVC (p = .01) and 25 ms reduc-tion in SP duration at 20% of MVC (p = .03). These results demon-strate a task dependent adaptation in corticospinal inhibition via

V. All rights reserved.

ercise and Nutrition Sciences, Deakin University, 221 Burwood Highway,7264; fax: +61 3 3 9244 6017.

(D.J. Kidgell).

632 D.J. Kidgell, A.J. Pearce / Human Movement Science 29 (2010) 631–641

a reduction in cortical SP duration that may in part underpin thestrength increases observed following strength training.

� 2010 Elsevier B.V. All rights reserved.

1. Introduction

The contributions of the central nervous system (CNS) to improvements in strength are well docu-mented (Duchateau & Enoka, 2002; Duchateau, Semmler, & Enoka, 2006; Folland & Williams, 2007).However, the mechanisms underlying these improvements are less well understood, particularly inthe primary motor cortex (M1). While evidence for the muscle morphological changes that occur withstrength training are clearly demonstrated through hypertrophy (Folland & Williams, 2007), the neuraladaptations induced by strength training may be comprised of more subtle changes (Datta & Stephens,1990) in many areas including supraspinal centers (Carroll, Riek, & Carson, 2002; Farmer, Swash, Ingram,& Stephens, 1993), descending neural tracts (Aagaard, Simonsen, Anderson, Magnusson, & Dyhre-Poulsen, 2002; Fimland, Helgerud, Gruber, Leivseth, & Hoff, 2009), spinal circuitry (Cannon & Cafarelli,1987; Del Balso & Cafarelli, 2007; Kamen, 2004), and the motor end plate connections betweenmotoneurons and muscle fibers (Staron, Karapondo, & Kraemer, 1994). Several investigations have re-ported maximal force increases of up to 15% within days following an exercise session (Berg, Larsson,& Tesch, 1997; Duchateau, 1995; Rogers & Evans, 1993; Schenck & Forward, 1965; Vandenborne, Elliot,& Walter, 1998; Yue, Bilodeau, Hardy, & Enoka, 1997), and up to 200% increase after 8 week, with nochanges in the cross-sectional area of muscle (Folland & Williams, 2007). These results imply that theearly stages of strength development may be due to some form of neural adaptation.

Although there is a general consensus that the CNS mediates this increase in strength following a per-iod of strength training, there is considerable debate concerning the extent and nature of involvement ofspecific sites within the CNS. Recently, a number of studies have used transcranial magnetic stimulation(TMS) to determine whether the M1 contributes to strength development, providing a potential site forneural adaptations to strength training (Carroll et al., 2002; Griffin & Cafarelli, 2007; Hortobágyi et al.,2009; Jensen, Marstrand, & Nielsen, 2005). Given that the M1 is heavily populated with corticospinalcells that descend onto motoneurons located within the spinal cord (Porter, 1985), the use of TMS en-ables the assessment of corticospinal excitability and inhibition following specific training interven-tions. For example, Carroll et al. (2002) examined the effect of heavy load (70–85% of MVC) isometricstrength training on corticospinal excitability following 4 week strength training of the first dorsal inter-osseous (FDI) muscle. Although strength training resulted in a 33% increase in strength, the strengthtraining program did not modify the size of the TMS produced motor-evoked potential (MEPs). Carrollet al. (2002) also used transcranial electrical stimulation (TES) to stimulate subcortical structures andconcluded that strength training does not affect the organization of the M1, suggesting that adaptationsare confined to the spinal cord. Similarly, Jensen et al. (2005) had participants perform heavy load (80% ofMVC) dynamic strength training (five sets of six to 10 repetitions) of the biceps brachii three times perweek for 4 week. MEP amplitude at 5% of MVC and stimulus–response curves were constructed prior toand after the 4 week training intervention. Following training, muscle strength increased by 31%, how-ever, maximal MEP amplitude produced by TMS at rest was reduced, suggesting a minimal role for theM1 and corticospinal pathway in strength development. In contrast to these findings, Beck et al. (2007)demonstrated increased MEP amplitude produced by TMS following 4 week of ballistic strength trainingin the soleus muscle, while Griffin and Cafarelli (2007) found a 32% increase in MEP amplitude with nochange in peripheral nerve excitability, suggesting that strength training leads to a task-specific adap-tation within the corticospinal tract. Therefore, strength training studies using TMS show either in-creased (Beck et al., 2007; Griffin & Cafarelli, 2007), reduced (Jensen et al., 2005), unchanged (Carrollet al., 2002), or task-specific modulation of corticospinal excitability (Beck et al., 2007).

Although the above mentioned TMS studies have tried to determine the effects of strength trainingon corticospinal excitability (by measuring MEP amplitude produced by TMS), changes in cortical inhi-bition may also be an important neural adaptation that contributes to strength development. Corticalinhibition refers to the neural mechanisms by which output from M1 is attenuated by inhibitory

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c-aminobutryic acid (GABA) receptor mediated interneuron transmission (McCormick, 1989). Inhibi-tory neurons located in the M1 use GABA as their neurotransmitter and the activity of these neuronscan be investigated with paired pulse or single-pulse TMS (Inghilleri, Berardelli, Cruccu, & Manfredi,1993; Jones, 1993; Kujirai et al., 1993). The paired pulse technique measures short interval intracor-tical inhibition (SICI) that is mediated by GABAA receptors (Kujirai et al., 1993), whereas the single-pulse technique measures inhibition mediated by GABAB (Siebner, Dressnandt, Auer, & Conrad,1998). Using the paired pulse technique, SICI can be measured and may be important for shapingthe output from the M1 (Chen, 2004). For example, SICI is reduced during voluntary muscle contrac-tions and has been proposed to improve corticospinal drive during intended movement by releasingcorticospinal cells from inhibition, therefore improving subsequent excitatory drive to produce the de-sired movement (Floeter & Rothwell, 1999). Using single-pulse TMS, it has been demonstrated thatthere is a reduction in the duration of the SP during both slow and fast finger movements, illustratinga task dependant change in corticospinal inhibition mediated by GABAB interneuronal transmission(Pearce & Kidgell, in press). Currently, no studies have examined the effect of strength training on cor-tical inhibition, although changes in inhibition may be important in force production. Studies havedemonstrated in M1 that prior to and during movement, there is not only an increase in corticospinalexcitability, but also a reduction in corticospinal inhibition (Chen, Yaseen, Cohen, & Hallett, 1998; Rey-nolds & Ashby, 1999; Ridding, Taylor, & Rothwell, 1995). Furthermore, the change in inhibition is spe-cific to the intended agonist muscle, as MEPs in antagonist muscle remain unchanged (Reynolds &Ashby, 1999; Ridding, Rothwell, & Inzelberg, 1995). Therefore, changes in inhibition seem to be selec-tive and act to focus the output from the MI by improving excitatory drive onto corticospinal cells thatproduce the intended movement (Ridding, Rothwell et al., 1995). In light of this, previous strengthtraining studies that have used TMS have not included the analysis of SP duration, despite severalinvestigations demonstrating changes in inhibition prior to and during movement (Reynolds & Ashby,1999; Ridding, Taylor et al., 1995). The novel aspect of the present study was that we investigatedwhether strength training of the FDI induces changes in corticospinal inhibition (SP duration) as pre-vious TMS strength training studies have not addressed this issue.

The purpose of the present investigation was to extend upon previous work (Carroll et al., 2002;Jensen et al., 2005) by investigating the corticospinal responses, with particular interest on the effectof isometric strength training on the duration of the cortical SP. The specific aim of the investigationwas to determine whether isometric strength training of the FDI altered corticospinal excitability andinhibition during moderate muscle activation. In order to investigate whether strength training causesadaptations along the corticospinal pathway, we determined the effect of isometric strength trainingon the magnitude of MEPs and the duration of the cortical SP produced by TMS at 5% and 20% MVC. Itwas hypothesized that strength training would increase the amplitude of the MEP, reflecting increasedcorticospinal excitability, reduce the duration of the cortical SP, reflecting a decrease in corticospinalinhibition and this would result in an increase in MVC force following training.

2. Methods

2.1. Participants

Sixteen healthy (24.12 ± 5.21 years, 13 males, and three females), right-handed university studentswere randomly allocated to either a strength training (seven males, one female) or a control group(six males, two females). All participants were right-handed, as assessed by the Edinburgh handednessinventory (Oldfield, 1971) and had not participated in any kind of strength training in the past 2 years. Allparticipants gave written, informed consent to the experimental procedures, which conformed to theDeclaration of Helsinki and were approved by the Human Research Ethics Committee of the University.

2.2. Experimental procedures

Participants assigned to the strength training group were required to undertake 12 supervisedstrength training sessions over a 4 week training period. Participants assigned to the control group

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completed no training, but participated in all testing procedures and were instructed to continue theircurrent activities for the 4 week period. TMS was applied prior to and following the 4 week strengthtraining intervention at 10% above active motor threshold (AMT) during a constant isometric contrac-tion of 5% and 20% MVC of the right FDI.

2.3. Electromyography and transcranial magnetic stimulation

Surface electromyography (EMG) activity was recorded from the FDI muscle of the right hand usingbipolar Ag–AgCl electrodes. Two electrodes were placed 1–2 cm apart over the FDI muscle, with thereference electrode (ground electrode) placed over the bony prominence of the III, IV, or V metacarpal.EMG signals were amplified (1–10 kHz), bandpass filtered (13–1000 Hz), digitized (2 kHz), recorded,and analyzed off-line using LabVIEW (National Instruments V4.0) software. TMS was applied usinga Magstim 2002 stimulator, with a standard 90 mm circular coil. The coil was placed over the vertexof the head and held tangential to the skull in an antero-posterior orientation, so that the current flo-wed in a counterclockwise direction for activating the left M1 (right-side muscles). For reliability ofcoil placement, participants wore a snugly fitting cap, positioned with reference to the nasion–inionand interaural lines. The cap was marked with sites at 1 cm spacing in a latitude–longitude matrixto ensure reliable coil position throughout the testing protocol and for repeated testing sessions overthe period of the study. The cap and coil position were checked consistently to ensure that no changesin position occurred. Sites near the estimated center of the FDI area were explored to determine thesite at which the largest MEP amplitude was evoked during a low level contraction at 5% of MVC. Thissite was defined as the ‘‘optimal” site. Given that establishing MT at rest requires the rigorous controlof background EMG activity (Curra et al., 2002) AMT, defined as the stimulus intensity at which a MEPcould be obtained with at least five of the 10 stimuli with peak–peak amplitude being greater than200 lV during 5% of MVC (Rothwell et al., 1999), was determined during a low level contraction at5% of MVC (Wilson, Lockwood, Thickbroom, & Mastaglia, 1993) in order to reduce variability(McDonnell, Ridding, & Miles, 2004). Five TMS stimuli were delivered at intensities 10% above partic-ipants AMT during controlled static abduction of the FDI at 5% and 20% MVC of the participant’spre-determined MVC force.

2.4. Strength testing

Participants were seated in a comfortable chair with a headrest to support the head and neck. Theright arm was abducted at the shoulder to allow the elbow, forearm, and right hand to be supported bya specially designed board that acted to isolate the right FDI (Fig. 1) (Pearce & Kidgell, in press). A low-sensitivity force transducer (Sensotec Model 13, Columbus OH, range 0-220 N, 16-bit resolution) wasfitted to the board and was used to act as the resistance during the static abduction task of the firstindex finger. The transducer was fixed but adjustable to suit the individual variations of hand/fingersize. The participant’s hand was restrained by Velcro straps at the wrist and on the remaining threefingers to isolate the FDI muscle. Participants were required to push against (abduction) the forcetransducer and produce a gradual rise in force to its maximum over a 3 s interval. Once the maximumforce was obtained it was held for a subsequent 3 s. Verbal encouragement and visual feedback of theforce exerted was provided via an oscilloscope which was located at eye level approximately 1.5 maway from the participant. The average of the three trials was used as the participant’s MVC.

2.5. M-waves

Direct muscle responses (Mmax) were obtained from the right FDI by supramaximal electrical stim-ulation of the ulnar nerve at the wrist under resting conditions. A Digitimer (Hertfordshire, UK) DS7Aconstant-current electrical stimulator (pulse duration 100 ls) was used to deliver each electricalpulse. An increase in current strength was applied to the ulnar nerve until there was no further in-crease in the amplitude of the EMG response. To ensure maximal responses, the current was increasedan additional 20% and the average M wave was obtained from five stimuli delivered at <0.5 Hz.

Fig. 1. An example of the force transducer used to measure finger force during movement studies. The force transducer wasfitted to a specially designed board to isolate the right FDI muscle. The participant’s hand was fastened by Velcro straps allowingthe first index finger to abduct and statically hold against the transducer.

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2.6. Strength training procedures

The training program involved maximum isometric abduction of the right index finger that wasperformed three times/week (Monday – Wednesday – Friday) in the laboratory. The task consistedof index finger abduction contractions that were held for 3 s, with a 3 s rest between contractions. Thiswas performed 10 times (1 set), and each participant performed 6 sets (separated by approximately3 min) for a total of 60 contractions.

2.7. Data and statistical analyses

All MEPs (500 ms epochs) were displayed and averaged online for visual inspection as well asstored off-line for further analysis. All MEPs in a trial (n = 5) were full-wave rectified. All corticospinalparameters (latency, amplitude, and SP, duration) were analyzed off-line. MEP amplitude was normal-ized as a percentage of the M wave. Latency was calculated from stimulus artifact to MEP onset and tomeasure SP duration (via visual inspection and cursored) its onset was defined as the commencementof the MEP and the endpoint coincided with the reoccurrence of EMG activity in individual trials(Byrnes, Thickbroom, Phillips, Wilson, & Mastaglia, 1999; Mills, 1999; Pearce & Kidgell, 2009; Wilson,Lockwood et al., 1993; Wilson, Thickbroom, & Mastaglia, 1993). Force signals were sampled at 200 Hzand analyzed off-line using custom designed software (National Instruments V4.0).

All data were first screened to ensure they were normally distributed. In order to have sufficientdata to test for questions of normality, all MEP, SP and MVC data were used to establish the distribu-tional properties. No variable’s z-score of skew or kurtosis were excessive. Further, Shapiro–Wilk testssuggested MEP amplitude, SP duration, and MVC variables were normally distributed (MEP, p = .42; SPduration, p = .17; MVC, p = .09). In order to determine the corticospinal responses to strength training,a two-way ANOVA was used to compare group (trained vs. control) by session (pre vs. post). For allcomparisons effect sizes (ES) of 0.2, 0.5, and 0.8 were established to indicate small, moderate and largecomparative effects, respectively (Cohen, 1988) and Pearson product-moment correlation coefficientswere used to determine correlations between significant criterion measures. Alpha was set at p 6 .05and results are presented as means ± SD.

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3. Results

All participants in the training group completed all training sessions, and all participants in bothgroups completed the pre and post testing sessions.

3.1. Voluntary muscle strength

Fig. 2 presents absolute strength changes following the training intervention for the strength train-ing and control groups. No significant differences were observed in strength between the groups priorto the training period (p = .23). Isometric strength training increased MVC force during index fingerabduction by 33.8% (p = .01; ES = .61) in the strength trained group, compared to a 13% increase forthe control group. The average MVC forces exerted during index finger abduction were44.48 ± 5.9 N (before training) and 59.54 ± 15.7 N (after training) for the strength trained group, and49.31 ± 24.58 N (before training) and 55.43 ± 22.72 N (after training) for the control group.

3.2. Cortical excitability – motor-evoked potentials

There were no significant differences in latency (all participants, mean 21.3 ± .1 ms) and normal-ized MEP amplitude/Mmax at 5% (p = .32) and 20% (p = .3) of MVC between groups at pre-training(Fig. 3).

Following the strength training intervention there were no significant differences in MEP/Mmax be-tween groups at 5% of MVC (trained; pre 40.3 ± 10.4% to post 48.9 ± 7.2%, vs. control; pre 46.1 ± 28.6%to post 43.4 ± 18.1%, p = .47; ES = .04). Similarly, there were no significant differences in MEP/Mmax at20% of MVC between groups (trained; pre 49.2 ± 15.6% to post 58.9 ± 12.6% vs. control; pre49.4 ± 20.2% to post 49.1 ± 16.7%, p = .21; ES = .13) following the strength training intervention.

3.3. Cortical inhibition – SP duration

No significant differences in SP duration were seen between groups at 5% (p = .14) and 20% (p = .88)of MVC pre-training. Following the training intervention, there was a significant reduction in SP dura-tion between groups at 5% of MVC (trained; pre 145 ± 18 ms to post 129 ± 38 ms vs. control; pre

Pre Post Pre PostTrained Untrained

Fig. 2. Absolute change in strength between the strength training and control groups. Mean (±SD). Four week of isometricstrength training resulted in a 33.8% increase in MVC strength. Asterisk denotes significant differences between groups (p = .01).

0.0

10.0

20.0

30.0

40.0

50.0

60.0

70.0

80.0

ME

P s

ize

(% o

f M-m

ax)

Pre Post Pre Post Pre Post Pre Post Trained (5%) Untrained (5%) Trained (20%) Untrained (20%)

Fig. 3. Group mean (±SD) data (strength trained, n = 8, control, n = 8) showing right FDI MEPs at 5% and 20% of MVC pre vs. poststrength training. MEP amplitudes are displayed as a percentage of the right FDI Mmax. There were no significant differences inMEPs pre and post strength training for both groups.

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SP D

urat

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Pre Post Pre Post Pre Post Pre Post Trained (5%) Untrained (5%) Trained (20%) Untrained (20%)

*

*

Fig. 4. Group mean (±SD) data (strength trained, n = 8, control, n = 8) showing right FDI SP duration at 5% and 20% of MVC prevs. post strength training. There was a significant reduction (as indicated by asterisk) in SP at 5% MVC (p = .04) and at 20% ofMVC (p = .01) following the strength training intervention for the trained group. There were no differences in SP duration for thecontrol group at any contraction level.

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133 ± 51 ms to post 124 ± 27 ms, p = .01; ES = .43: Figs. 4 and 5) and 20% MVC (trained; pre129 ± 34 ms to post 104 ± 29 ms vs. control; pre 126 ± 10.5 ms to post 129 ± 11 ms; p = .03; ES = .33;Fig. 4). Post training analysis demonstrated a mean reduction in SP duration of 16 ms and 25 ms for5% and 20% MVC for the trained group, respectively. Following the strength training intervention,there was a significant, but moderate correlation between the change in strength and the pooledchange in SP duration (r = �.51, p = .05) for the strength training group.

a

b

1 mV

50 ms

Fig. 5. Overlay of raw MEP sweeps in one participant (at 20% MVC) illustrating the reduction in SP duration pre (a) and post (b)training.

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4. Discussion

In the present study, we aimed to investigate the neural mechanisms contributing to strengthdevelopment following short-term strength training of the FDI using TMS, observing a significant in-crease in MVC force in the training group and a reduction in cortical inhibition.

There was a 33.8% increase in MVC force in the trained participants and this increase was compa-rable to other short-term strength training studies that have exercised intrinsic muscles of the hand(Carroll et al., 2002; Kidgell, Sale, & Semmler, 2006; Olafsdottir, Zatsiorsky, & Latash, 2008). Increasesin the expression of muscular force following short-term strength training are thought to be a result ofadaptive changes within neural control circuits projecting to the trained musculature (Carroll et al.,2002; Folland & Williams, 2007).

Although it has long been reported that adaptations in the CNS may account for increases instrength following short-term strength training (Sale, 1988; Sale, MacDougall, Upton, & McComas,1983), we found no differences in the size of the descending corticospinal volley during isometric con-tractions of 5% and 20% of MVC. These findings concur with other studies, who following strengthtraining of the hand and arm, found either no difference or small decreases in corticospinal excitability(Carroll et al., 2002; Jensen et al., 2005; Lee, Gandevia, & Carroll, 2009). These authors reported thatthe number of motoneurons activated, the size of the descending corticospinal volley, and the excit-ability of corticospinal cells for a particular level of muscle activity remained unaffected by short-termstrength training. However, this result is in contrast to the recent findings of Griffen and Cafarelli(2007) and Beck et al. (2007) who reported increases in corticospinal excitability in lower leg musclesfollowing short-term strength training. It was put forward that the increase in MEP amplitude was aresult of an increase in the size of the descending corticospinal volley and this consequently lead to anincrease in motor unit recruitment (Beck et al., 2007; Griffen and Cafarelli, 2007). The differences be-tween the results of the present study and that of other studies (Griffen and Cafarelli, 2007; Taubeet al., 2007) may partly reside in the divergent distribution of corticospinal cell projections onto spinalmotoneurons being different between upper and lower limb muscles (Devanne, Lavoie, & Capaday,1997) and as a result of the different strength training paradigm employed. Individual muscles re-spond differently to TMS and display differences in the input–output properties of the corticospinalpathway (Schieppati, Trompetto, & Abbruzzese, 1996).

A novel finding to the present study was the significant reduction in SP duration followingthe strength training program. Although changes in SP duration have been reported during different

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functional skilled tasks of the hands (Pearce & Kidgell, 2009; Pearce & Kidgell, in press; Sale &Semmler, 2005; Tinazzi et al., 2003) this is the first study to report associated changes in corticospinalinhibition (using single-pulse TMS) following a period of strength training. From our data and due tolimitations in the technique of single-pulse TMS, we can only speculate about the underlyingmechanism responsible for this reduction. Several studies have established that the initial portion(50–75 ms) of the TMS evoked SP is primarily due to spinal inhibitory mechanism such as after-hyper-polarization and recurrent inhibition of a-motoneurons (Chen, Lozano, & Ashby,1999; Fuhr, Agostino,& Hallett, 1991; Schnitzler & Benecke, 1994). The later component (>75 ms) represents an intracorticalinhibitory mechanism that is mediated by GABAB receptors generated within the M1 that leads to afailure in corticospinal drive (Chen, 2004; Fuhr et al., 1991; Kimiskidis et al., 2005; Schnitzler &Benecke, 1994). While the single-pulse technique can be used to assess changes in SP duration (Sale& Semmler, 2005; Tinazzi et al., 2003), the technique of paired-pulse TMS is a more appropriate meth-od to measure changes in cortical inhibition. Therefore, we are unable to determine whether thechanges in SP were predominantly of a cortical origin as we used the single-pulse technique andwe were not in a position to measure the duration of the peripheral SP. Despite these limitations,the associated reduction in SP duration observed following the strength training program providesindirect support for a reduction in corticospinal inhibition probably confined to the M1 and spinal cordcircuitry, based upon the negative correlation that we have reported.

There is a general consensus in the literature that strength training is a form of motor skill acqui-sition as it requires the participants to produce muscle recruitment patterns that are associated withoptimal performance of the task (Carroll et al., 2002; Farthing, 2009; Zhou, 2000). Given that previousstudies have demonstrated task dependant changes in corticospinal inhibition of the FDI during skilledtasks (Pearce & Kidgell, 2009; Sale & Semmler, 2005; Tinazzi et al., 2003), the changes in SP durationobserved in the present study may also be a result of task dependant changes that are similar to thoseobserved with motor skill acquisition (Tinazzi et al., 2003). Therefore, it appears that the strengthtraining program has altered the balance between excitation and inhibition, therefore improving vol-untary motor drive due to the reduction in SP duration. Several studies have reported a reduction involuntary motor drive when there is an increase in SP duration (Kimiskidis et al., 2005; Ridding, Tayloret al., 1995; Werhahn, Behrang-Nia, Bott, & Klimpe, 2007).

Despite the limitations of the present study, alterations in corticospinal inhibition have beenassociated with mechanisms that induce cortical plasticity and given that inhibition is reduced dur-ing voluntary contractions (Ridding, Taylor et al., 1995), it is possible that the repeated contractionof the FDI throughout the strength training intervention lead to some form of long-term inhibition(LTI) (Butefisch et al., 2000) and this would support the finding of task dependant adaptations incorticospinal output that occur with repetitive skill training (Pascual-Leone et al., 1995; Perez &Cohen, 2008). Changes in cortical inhibition have been suggested to ‘‘release” corticospinal neuronsfrom inhibition, thus enhancing the net excitatory drive during movement (Floeter & Rothwell,1999; Reynolds & Ashby, 1999). Although there was a reduction in SP duration, this was not as aresult of a reduction in the size of the descending corticospinal volley; therefore it appears thatthe strength training intervention may have resulted in a shift in the balance between inhibitoryand excitatory inputs onto corticospinal cells demonstrating that inhibition is physiologically sepa-rate from excitation.

In conclusion, in accordance with previous studies, we have demonstrated that following 4 week ofstrength training an intrinsic hand muscle, there was a rapid increase in strength; however, we ob-served no differences in corticospinal excitability as determined by MEP amplitude. The novel findingof a reduced SP duration suggests that strength training has resulted in a task specific neural adapta-tion, which is most likely due to both reduced inhibition within spinal cord circuitry and in GABAB

mediated cortical inhibition confined to the M1. Based upon this novel finding, future strength train-ing studies should assess changes in both corticospinal excitability and inhibition. The interpretationof a reduced SP duration being a possible mechanism for improved strength seems unjustified at pres-ent, and should be taken with caution, as it is still unclear what the functional properties of inhibitorycircuits are during voluntary force production. Although contributions from segmental sources cannotbe excluded, we suggest that isometric strength training has resulted in some form of neural adapta-tion within the M1 that maybe important in mediating strength development.

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References

Aagaard, P., Simonsen, E. B., Anderson, J. L., Magnusson, P., & Dyhre-Poulsen, P. (2002). Neural adaptation to resistance training:Changes in evoked V-wave and H-reflex responses. Journal of Applied Physiology, 92, 2309–2318.

Beck, S., Taube, W., Gruber, M., Amtage, F., Gollhofer, A., & Schubert, M. (2007). Task-specific changes in motor evoked potentialsof lower limb muscles after different training interventions. Brain Research, 1179, 51–56.

Berg, H. E., Larsson, L., & Tesch, P. A. (1997). Lower limbs skeletal muscle function after 6 wk of bed rest. Journal of AppliedPhysiology, 82, 182–188.

Butefisch, C. M., Davis, B. C., Wise, S. P., Sawaki, L., Kopylev, L., Classen, J., et al. (2000). Mechanisms of use-dependent plasticityin the human motor cortex. Proceedings of the National Academy of Sciences USA, 97, 3661–3665.

Byrnes, M. L., Thickbroom, G. W., Phillips, B. A., Wilson, S. A., & Mastaglia, F. L. (1999). Physiological studies of the corticomotorprojection to the hand after subcortical stroke. Clinical Neurophysiology, 110, 487–498.

Cannon, R. J., & Cafarelli, E. (1987). Neuromuscular adaptations to training. Journal of Applied Physiology, 63, 2396–2402.Carroll, T. J., Riek, S., & Carson, R. G. (2002). The sites of neural adaptation induced by resistance training in humans. Journal of

Physiology, 544, 641–652.Chen, R. (2004). Interactions between inhibitory and excitatory circuits in the human motor cortex. Experimental Brain Research,

154, 1–10.Chen, R., Lozano, A. M., & Ashby, P. (1999). Mechanism of the silent period following transcranial magnetic stimulation evidence

from epidural recordings. Experimental Brain Research, 128, 539–542.Chen, R., Yaseen, Z., Cohen, L. G., & Hallett, M. (1998). Time course of corticospinal excitability in reaction time and self-paced

movements. Annals of Neurology, 44, 317–325.Cohen, J. (1988). Statistical power analysis for the behavioral sciences. Hillsdale, NJ: Erlbaum.Curra, A., Modugno, N., Inghilleri, M., Manfredi, M., Hallett, M., & Berardelli, A. (2002). Transcranial magnetic stimulation

techniques in clinical investigation. Neurology, 59, 1851–1859.Datta, A. K., & Stephens, J. A. (1990). Synchronization of motor unit activity during voluntary contraction in man. Journal of

Physiology, 422, 397–419.Del Balso, C., & Cafarelli, E. (2007). Adaptations in the activation of human skeletal muscle induced by short-term isometric

resistance training. Journal of Applied Physiology, 103, 402–411.Devanne, H., Lavoie, B. A., & Capaday, C. (1997). Input-output properties and gain changes in the human corticospinal pathway.

Experimental Brain Research, 114, 329–338.Duchateau, J. (1995). Bed rest induces neural and contractile adaptations in triceps surae. Medicine and Science in Sports and

Exercise, 27, 1581–1589.Duchateau, J., & Enoka, R. M. (2002). Neural adaptations with chronic activity patterns in able-bodied humans. American Journal

of Physical Medicine and Rehabilitation, 81, S17–27.Duchateau, J., Semmler, J. G., & Enoka, R. M. (2006). Training adaptations in the behavior of human motor units. Journal of Applied

Physiology, 101, 1766–1775.Farmer, S. F., Swash, M., Ingram, D. A., & Stephens, J. A. (1993). Changes in motor unit synchronization following central nervous

lesions in man. Journal of Physiology, 463, 83–105.Farthing, J. P. (2009). Cross-education of strength depends on limb dominance. Implications for theory and application. Exercise

and Sport Sciences Reviews, 37, 179–187.Fimland, M., Helgerud, J., Gruber, M., Leivseth, G., & Hoff, J. (2009). Functional maximal strength training induces neural transfer

to single-joint tasks. European Journal of Applied Physiology, 107, 21–29.Floeter, M. K., & Rothwell, J. C. (1999). Releasing the brakes before pressing the gas pedal. Neurology, 53, 664–665.Folland, J. P., & Williams, A. G. (2007). The adaptations to strength training: Morphological and neurological contributions to

increased strength. Sports Medicine, 37, 145–168.Fuhr, P., Agostino, R., & Hallett, M. (1991). Spinal motor neuron excitability during the silent period after cortical stimulation.

Electroencephalography and Clinical Neurophysiology, 81, 257–262.Griffin, L., & Cafarelli, E. (2007). Transcranial magnetic stimulation during resistance training of the tibialis anterior muscle.

Journal of Electromyography and Kinesiology, 17, 446–452.Hortobágyi, T., Richardson, S. P., Lomarev, M., Shamim, E., Meunier, S., Russman, H., et al. (2009). Chronic low-frequency rTMS of

primary motor cortex diminishes exercise training-induced gains in maximal voluntary force in humans. Journal of AppliedPhysiology, 106, 403–411.

Inghilleri, M., Berardelli, A., Cruccu, G., & Manfredi, M. (1993). Silent period evoked by transcranial stimulation of the humancortex and cervicomedullary junction. Journal of Physiology, 466, 521–534.

Jensen, J. L., Marstrand, P. C., & Nielsen, J. B. (2005). Motor skill training and strength training are associated with differentplastic changes in the central nervous system. Journal of Applied Physiology, 99, 1558–1568.

Jones, E. G. (1993). GABAergic neurons and their role in cortical plasticity in primates. Cerebral Cortex, 3, 361–372.Kamen, G. (2004). Reliability of motor-evoked potentials during resting and active contraction conditions. Medicine and Science

in Sports and Exercise, 36, 1574–1579.Kidgell, D. J., Sale, M. V., & Semmler, J. G. (2006). Motor unit synchronization measured by cross-correlation is not influenced by

short-term strength training of a hand muscle. Experimental Brain Research, 175, 745–753.Kimiskidis, V. K., Papagiannopoulos, S., Sotirakoglou, K., Kazis, D. A., Kazis, A., & Mills, K. R. (2005). Silent period to transcranial

magnetic stimulation: Construction and properties of stimulus–response curves in healthy volunteers. Experimental BrainResearch, 163, 21–31.

Kujirai, T., Caramia, M. D., Rothwell, J. C., Day, B. L., Thompson, P. D., Ferbert, A., et al. (1993). Corticocortical inhibition in humanmotor cortex. Journal Physiology, 471, 501–519.

Lee, M., Gandevia, S. C., & Carroll, T. (2009). Short-term strength training does not change cortical voluntary activation. Medicineand Science in Sports and Exercise, 41, 1452–1460.

McCormick, D. A. (1989). GABA as an inhibitory neurotransmitter in human cerebral cortex. Journal of Neurophysiology, 62,1018–1027.

D.J. Kidgell, A.J. Pearce / Human Movement Science 29 (2010) 631–641 641

McDonnell, M. N., Ridding, M. C., & Miles, T. S. (2004). Do alternate methods of analysing motor evoked potentials givecomparable results? Journal of Neuroscience Methods, 136, 63–67.

Mills, K. R. (1999). Measurement of the silent period. In K. R. Mills (Ed.), Magnetic stimulation of the human nervous system(pp. 177). Oxford: Oxford University Press.

Olafsdottir, H. B., Zatsiorsky, V. M., & Latash, M. L. (2008). The effects of strength training on finger strength and hand dexterityin healthy elderly individuals. Journal of Applied Physiology, 105, 1166–1178.

Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113.Pascual-Leone, A., Nguyet, D., Cohen, L. G., Brasil-Neto, J. P., Cammarota, A., & Hallett, M. (1995). Modulation of muscle responses

evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. Journal of Neurophysiology, 74,1037–1045.

Pearce, A. J., & Kidgell, D. J. (in press). Comparison of corticomotor excitability during visuomotor dynamic and static tasks.Journal of Science and Medicine in Sport, 13, 167–171.

Pearce, A. J., & Kidgell, D. J. (2009). Corticomotor excitability during precision motor tasks. Journal of Science and Medicine inSport, 12, 280–283.

Perez, M. A., & Cohen, L. G. (2008). Mechanisms underlying functional changes in the primary motor cortex ipsilateral to anactive hand. Journal of Neuroscience, 28, 5631–5640.

Porter, R. (1985). The corticomotoneuronal component of the pyramidal tract: Corticomotoneuronal connections and functionsin primates. Brain Research, 357, 1–26.

Reynolds, C., & Ashby, P. (1999). Inhibition in the human motor cortex is reduced just before a voluntary contraction. Neurology,53, 730–735.

Ridding, M. C., Rothwell, J. C., & Inzelberg, R. (1995). Changes in excitability of motor cortical circuitry in patients withParkinson’s disease. Annals of Neurology, 37, 181–188.

Ridding, M. C., Taylor, J. L., & Rothwell, J. C. (1995). The effect of voluntary contraction on cortico-cortical inhibition in humanmotor cortex. Journal of Physiology, 487, 541–548.

Rogers, M. A., & Evans, W. J. (1993). Changes in skeletal muscle with aging: Effects of exercise training. In J. O. Holloszy (Ed.),Exercise and sport science reviews (pp. 65–102). Baltimore: Williams and Wilkins.

Rothwell, J., Hallett, M., Berardelli, A., Eisen, A., Rossini, P., & Paulus, W. (1999). Magnetic stimulation: motor evoked potentials.The international federation of clinical neurophysiology. Electroencephalography and Clinical Neurophysiology, Suppl. 52,97–103.

Sale, D. G. (1988). Neural adaptation to resistance training. Medicine and Science in Sports and Exercise, 20, S135–S145.Sale, D. G., MacDougall, J. D., Upton, A. R., & McComas, A. J. (1983). Effect of strength training upon motoneuron excitability in

man. Medicine and Science in Sports and Exercise, 15, 57–62.Sale, M. V., & Semmler, J. G. (2005). Age-related differences in corticospinal control during functional isometric contractions in

left and right hands. Journal of Applied Physiology, 99, 1483–1493.Schenck, J. M., & Forward, E. M. (1965). Quantitative strength changes with test repetitions. Physical Therapy, 45, 562–569.Schieppati, M., Trompetto, C., & Abbruzzese, G. (1996). Selective facilitation of responses to cortical stimulation of proximal and

distal arm muscles by precision tasks in man. Journal of Physiology-London, 491(Pt. 2), 551–562.Schnitzler, A., & Benecke, R. (1994). The silent period after transcranial magnetic stimulation is of exclusive cortical origin:

Evidence from isolated cortical ischemic lesions in man. Neuroscience Letters, 180, 41–45.Siebner, H. R., Dressnandt, J., Auer, C., & Conrad, B. (1998). Continuous intrathecal baclofen infusions induced a marked increase

of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve, 21, 1209–1212.Staron, R. S., Karapondo, D. L., & Kraemer, W. J. (1994). Skeletal muscle adaptations during early phase of heavy-resistance

training in men and women. Journal of Applied Physiology, 76, 1247–1255.Taube, W., Gruber, M., Beck, S., Faist, M., Gollhofer, A., & Schubert, M. (2007). Cortical and spinal adaptations induced by balance

training: Correlation between stance stability and corticospinal activation. Acta Physiologica (Oxf.), 189, 347–358.Tinazzi, M., Farina, S., Tamburin, S., Facchini, S., Fiaschi, A., Restivo, D., et al. (2003). Task-dependent modulation of excitatory

and inhibitory functions within the human primary motor cortex. Experimental Brain Research, 150, 222–229.Vandenborne, K., Elliot, M. A., & Walter, G. A. (1998). Longitudinal study of skeletal muscle adaptations during immobilisation

and rehabilitation. Muscle and Nerve, 21, 1006–1012.Werhahn, K. J., Behrang-Nia, M., Bott, M. C., & Klimpe, S. (2007). Does the recruitment of excitation and inhibition in the motor

cortex differ? Journal of Clinical Neurophysiology, 24, 419–423.Wilson, S. A., Lockwood, R. J., Thickbroom, G. W., & Mastaglia, F. L. (1993). The muscle silent period following transcranial

magnetic cortical stimulation. Journal of the Neurological Sciences, 114, 216–222.Wilson, S. A., Thickbroom, G. W., & Mastaglia, F. L. (1993). Transcranial magnetic stimulation mapping of the motor cortex in

normal subjects. The representation of two intrinsic hand muscles. Journal of the Neurological Sciences, 118, 134–144.Yue, G. H., Bilodeau, M., Hardy, P. A., & Enoka, R. M. (1997). Task dependant effect of limb immobilisation on fatigability of the

elbow flexor muscles in humans. Experimental Physiology, 82, 567–592.Zhou, S. (2000). Chronic neural adaptations to unilateral exercise: Mechanisms of cross education. Exercise and Sport Sciences

Review, 28, 177–184.