Strength training induces physiological adaptations in both the muscular and the nervous systems that contribute to the development of strength (1,12,13,34). Although neural adaptation is thought to be primarily responsible for the rapid increase in muscle force observed in the early phase of strength training (i.e., 2-6 wk) (9,14,37), there remains the possibility that peripheral factors (such as enzyme and fiber type changes, excitation-contraction coupling changes, muscle protein synthesis, etc.) might also contribute to strength increases in the early phase of training (23,28). At present, the nature of neural adaptation is unknown, and there is limited information on the sites of adaptation (e.g., cortical or subcortical). Small adaptive changes may occur at multiple sites in the nervous system, which together alter muscle output (18). Strength training may increase voluntary drive via increased activation of agonist and synergist motor units or via inhibition of antagonists (6,19).
At present, twitch interpolation (2,26) is probably the best technique to assess voluntary neural drive, which is also known as "voluntary activation" (16). Traditional twitch interpolation assesses the completeness of muscle activation via the application of a supramaximal, electrical stimulus to the motor nerve during a maximal voluntary contraction (MVC). Any motor units not recruited by volition, or firing at a submaximal rate, will yield "extra" force. This "superimposed twitch" indicates that voluntary activation is submaximal (22). Single-pulse transcranial magnetic stimulation (TMS) can be used to assess the completeness of motor cortical output (42). If a superimposed twitch can be evoked during maximal efforts withTMS, cortical drive is considered submaximal, and impairment in voluntary activation must occur at or above the level of motor cortical output (42,43). Voluntary activation is quantified by normalizing the amplitude of a superimposed twitch during MVC to the twitch force produced by the same stimulus at rest. Measurement of resting twitch using TMS requires special consideration because both motor cortical and motoneuronal excitability vary with activity (36). Therefore, it is not possible to generate a maximal muscle twitch at rest with TMS. To overcome this, Todd et al. (42,43) estimated the resting motor twitch that would be produced if background excitability were the same as during a strong contraction. This "estimated" resting twitch is measured by linear extrapolation between the size of the superimposed twitch produced by cortical stimulation and voluntary torque. This measure is reliable for the elbow flexors (42,43) and wrist extensors (25).
A few studies have used twitch interpolation to examine the effects of strength training on voluntary activation, but no studies have used TMS. Most studies were conducted in lower limb muscles. Some reported an increase (31,33,39,40), and others reported no change in voluntary activation (5,20,38). Data for the upper limb muscles are scarce, with only one report for the elbow flexors. Herbertet al. (21) found no change in voluntary activation after 8 wk of strength training despite increases in elbow flexion force.
The primary objective of the present study was to investigate the effects of a 4-wk unilateral strength training program for the wrist on voluntary activation using twitch interpolation with motor nerve and motor cortical stimulation. A second aim was to examine training specificity (27,34). Subjects trained to improve the strength of the wrist abductors, while we investigated maximal voluntary force and voluntary activation changes for both wrist abductors and extensors. According to the training specificity principle (27,34), we expected strength gains and changes in voluntary activation to be more pronounced in the wrist abductors. As some strength increases may occur for the opposite untrained limb (8,29), voluntary activation (with motor nerve stimulation) and MVC were also assessed in the untrained wrist.
Twenty-three healthy volunteers aged between 18 and 51 yr (16 males, 7 females; 4 left-handed, 19 right-handed) participated in this study. All subjects trained with their right hand. The participants gave written, informed consent to the procedures, which conformed to the Declaration of Helsinki and were approved by the Human Research Ethics Committee at the University of New South Wales.
Strength and voluntary activation were assessed in testing sessions conducted before and after a 4-wk training program. The final testing session was conducted 2-4 d after the last training session. During testing sessions, the participants sat in a chair with the hand comfortably maintained in a neutral position and secured in a custom-made manipulandum. The elbow was kept at an angle of 110° with the forearm parallel to the table and was supported by a device similar to that described previously (24). The left arm was always tested before the right arm.
The exercise performed during training was dynamic wrist abduction (range of motion was from 5° abduction to 30° adduction). Subjects wererandomly allocated to either a strength training group (n = 12) or a control group (n = 11). A custom-built training device involving a pulley system and weighted rig was used to apply resistance to wrist abduction movements for subjects in the training group. The pulley's center of rotation was aligned approximately with the center of wrist joint rotation, and the hand was coupled with the pulley system in a neutral pronation-supination position. Coupling was achieved via an adjustable, padded device that contacted the hand with four horizontal and vertical surfaces just proximal to the metacarpophalangeal joints. All strength training sessions were supervised and consisted of four sets of eight dynamic contractions, three times per week, for 4 wk. Each subject's maximum dynamic strength or one repetition maximum (1RM) was determined at the first training session. Training loads were then set at 70% of pretraining 1RM for the first week, 75% of pretraining 1RM for the second week, 80% of pretraining 1RM for the third week, and 85% of pretraining 1RM for the fourth week. This type of progressive strength training is an effective way to increase voluntary strength (4) and has been used successfully to increase isometric force in the index fingerduring a 4-wk period (10). The control subjects performed an identical number of training sessions involving four setsof wrist abductions without an external load. The control subjects completed a logbook to document theirtraining.
We recorded surface EMG from the wrist flexors (flexor carpi radialis, FCR) and extensors (extensor carpi radialis brevis and longus, ECRB and ECRL) via bipolar Ag/AgCl surface electrodes (1-cm diameter), with an interelectrode distance of 2 cm. The FCR was located by manual muscle testing, and the recording electrodes were placed over the muscle belly, 8 cm from the medial epicondyle. The location of ECRB and ECRL recording sites was determined according to theanatomical measurement described by Riek et al. (35) and manual muscle testing. Briefly, the ECRB electrodes were positioned at 45% of the length of the radius as measured from the styloid process, at which position, the ECRL is tendinous and passes under the ECRB muscle belly. The signals were bandpass-filtered (30-1000 Hz) and amplified (gain 500; Grass P511, Astro-Med Inc., West Warwick, RI).
Participants were familiarized with the procedures and practiced submaximal voluntary wrist contractions. They then performed two MVC in extension and two MVC in abduction. Voluntary and evoked forces in both abduction and extension directions were simultaneously recorded via a 6-df force transducer (JR3 45E15A-I63-A 400N60S, Woodland, CA), coupled with a custom-made wrist manipulandum that was adjustable and was padded to ensure a snug fit of the hand just proximal to the metacarpophalangeal joint. The largest force obtained in the nominated direction was taken as the MVC. The participants were asked to increase their force steadily to a maximum for 2 s and to maintain a maximum force for a further 2 s. A 2-min rest separated each MVC. All subjects were given standard verbal encouragement during each MVC attempt, and visual feedback of performance was provided. The subjects were allowed to repeat an MVC measurement in the event of any perceived submaximal effort. They were instructed to keep the opposite forearm relaxed throughout.
Radial nerve stimulation.
Single electrical stimuli (duration = 200 μs) were delivered to the radial nerve lateral to the humerus (DS7AH; Digitimer, Hertfordshire, United Kingdom). The anode was below the deltoid tuberosity approximately halfway between the olecranon and acromion, and the cathode was 2-3 cm distal to the anode over the radial nerve. At the start of the experiment, the size of the maximal compound muscle action potential (Mmax) was measured in the ECRB and ECRL at rest and during abduction and extension MVC. The stimulus intensity was set at 120% of the current required to produce a maximal response. The amplitude of evoked EMG responses was normalized to Mmax amplitude.
A Magstim 2002 magnetic stimulator with a figure-of-8 coil (outside diameter of each loop of 70 mm) was used to elicit motor evoked potentials (MEP) in the right wrist extensor muscles. The coil was held over the left motor cortex at 45° to the sagittal plane at an optimal position to elicit MEP in the ECRB muscle (with posterior to anterior current flow). In each session, resting motor threshold was determined as the lowest stimulator intensity to elicit MEP (>50 μV) in at least three of five trials. During threshold determination, we monitored EMG at high gain and excluded trials if voluntary activity was detected. Once threshold was established, the position of the coil was marked on the scalp with a whiteboard marker, and its distance relative to anatomical landmarks was recorded. The stimulator output (70%-85% maximum) was set to produce a large MEP in the ECRB of at least 50% Mmax during extension MVC and a small MEP (<10% Mmax) in the wrist flexors (FCR). The stimulus intensity remained constant throughout each experimental session. See Todd et al. (42) for a detailed description of the rationale underlying the protocol.
Voluntary activation testing protocols.
In each session, the left wrist was always tested before the right. For the left (untrained) wrist, voluntary activation was measured via 10 brief (2 s) MVC (5 in extension and 5 in abduction). Single, supramaximal radial nerve stimuli were delivered during each MVC and at rest 2 s after the maximal effort (Fig. 1A). Each MVC was separated by at least 2 min to minimize fatigue. Extension and abduction contractions were performed in alternate order (but thecontraction direction executed in the first trial was selectedrandomly).
For the right (trained) wrist, subjects performed 10 trials, each consisting of four voluntary contractions (two 100% MVC and two submaximal contractions at 50% and 75% of MVC; Fig. 1B). Each contraction lasted for 2 s with 5 s separating contractions within a single trial. A 2 min rest was provided between each trial to prevent fatigue. Five trials were performed for extension contractions and five forabduction contractions. TMS was delivered to evoke superimposed twitches during 75% and 50% MVC contractions (25). Supramaximal radial nerve stimulation and TMS were delivered during alternate 100% MVC. The type of stimulus applied during the first contraction in each trial alternated between motor nerve and motor cortical stimulation (but the first stimulus type to be used in the first trial was selected randomly). Visual feedback of the required torques was provided at the appropriate times to guide subjects throughout the experiment.
Analysis of MEP and Mmax.
MEP and Mmax data were sampled at 10 kHz with a 12-bit National Instruments A/D board interfaced with a computer running a custom-written Labview program (National Instruments, Austin, TX). The peak-to-peak amplitude of the MEP and Mmax were analyzed offline using a Labview program, which allowed the experimenter to set cursors at the beginning and at the end of each waveform. Because the results were similar for amplitude and area under the Mmax and MEP waveforms, the area data are not reported.
Analysis of evoked twitch forces.
The same force transducer for MVC measurement was used to simultaneously record force twitches evoked in both extension and abduction directions. Custom software was used to inspect short windows (∼150 ms) of the force traces around the stimulus times, and cursors were placed to capture the beginning and the peak of the evoked twitches in both abduction and extension directions. Figure 2 shows examples of twitches in extension and abduction produced by TMS (A and B, respectively) recorded from a representative subject during 50% MVC abduction contractions. The amplitude and direction of the resultant twitch forces were resolved via trigonometry. Figure 2C shows examples of the resultant twitch force.
Calculation of voluntary activation.
Force increments evoked by radial nerve stimulation during abduction or extension MVC (i.e., the superimposed twitch force) were expressed as a fraction of the peak amplitude of twitches evoked in the same direction by the same stimulus at rest, obtained 1-2 s after MVC (resting twitch). Each force trace was inspected offline, and data were discarded if the superimposed twitch was not evoked at, or close to, the peak force. We then expressed voluntary activation as a percentage using the conventional formula: voluntary activation (%) = (1 − superimposed twitch force / resting twitch force) × 100. This formula was also used to quantify cortical voluntary activation, except that the resting twitch was estimated rather than measured directly ("estimated resting twitch"). A linear regression was calculated on the relationship between the amplitudes of superimposed twitch and the voluntary force obtained before stimulation at approximately 100%, 75%, and 50% MVC (25,42). The y-intercept was taken as the estimated resting twitch (25,42).
Two-way (group × time) repeated-measures ANOVA was used to determine the effects of training on MVC force in extension and abduction, voluntary activation during extension and abduction MVC, superimposed twitch amplitude during wrist extension and abduction contractions, and resting twitch amplitude. MVC and peak twitch amplitudes were taken as the highest forces attained in any trial throughout the experiment (i.e., peak twitch force occurred when the muscle was potentiated). Planned contrast analyses were used to compare differences between pretraining and posttraining measurements. Results are presented as mean ± SD. For all analyses, a probability of <5% was considered statistically significant.
Voluntary muscle strength.
Strength training increased MVC during wrist abduction by 11.0 ± 8.7% (P < 0.01), whereas MVC did not change during wrist extension during the 4-wk period. Group data are presented in Figure 3. The control group showed no significant change in MVC in either contraction direction. The strength of the left, untrained wrist was also unchanged for both groups. The average MVC forces exerted during wrist abduction were 167.1 ± 52.8 N (before training) and 174.0 ± 54.2 N (after training) for the strength training group, and 155.0 ± 71.8 N (before training) and 159.0 ± 65.8 N (after training) for the control group.
Radial nerve stimulation.
The amplitude of Mmax produced by supramaximal radial nerve stimulation at rest and during MVC did not change in the trained or untrained wrist for either group during the 4-wk period. There was no significant change in the average size of the superimposed twitch recorded during MVC or resting twitch evoked by radial nerve stimulation in either group. There was also no change in the direction of the (potentiated) resultant twitch evoked at rest by supramaximal radial nerve stimulation in either group (right hand data, training group: before = 57.9°, after = 57.5°; control group: before = 54.8°, after = 55.3°; left hand data, training group: before = 57.7°, after = 57.5°; control group: before = 57.5°, after = 57.0°; P > 0.1). Voluntary activation measured via radial nerve twitch interpolation did not change significantly during wrist extension or wrist abduction in the trained or untrained wrist for either group (Fig. 4).
The resting motor threshold for both the strength training and control group did not change significantly across time (strength training: before training = 45 ± 10%, after training = 44 ± 9%; control: before training = 42 ± 7%, after training = 42 ± 5%). Raw MEP and Mmax traces from a representative subject exerting wrist abduction forces are shown in Figure 1C. Within a session, the sizes of the MEP evoked during wrist abduction and extension were similar across all contraction intensities (∼50% Mmax). The amplitude of the MEP recorded from the wrist extensors during voluntary contractions was not significantly different during the 4-wk period (Table 1).
Raw traces of the TMS-evoked superimposed twitches recorded from a representative subject during wrist abduction contractions are shown in Figure 1C. In the trained wrist, the average amplitude of superimposed twitches was significantly larger during wrist abduction at 75% MVC (before training = 6.1 ± 3.7 N, after training = 9.4 ± 6.2 N, P< 0.01) and 50% MVC (before training = 15.3 ± 6.2 N, after training = 19.3 ± 8.2 N, P < 0.01) but was unchanged for 100% MVC (before training = 1.5 ± 2.1 N, after training = 2.0 ± 1.7 N; Fig. 5A). Note that all force levels are expressed relative to the MVC measured in the same session. The changes that occurred during submaximal wrist abduction increased the slope of the linear regression between voluntary force and the superimposed twitches and contributed to a larger estimated resting twitch (27 ± 20% increase, P = 0.03). Data from a representative subject are shown in Figure 6. There were no significant changes in the size of superimposed twitches or estimated resting twitches for the control group. By contrast with the training-induced effects observed during wrist abduction, the sizes of the superimposed twitches evoked during wrist extension were not affected (Fig. 5B). During the 4-wk period, there were no significant changes in the amplitudes of the estimated resting twitch for either group.
Four weeks of strength training did not significantly alter cortical voluntary activation during wrist abduction or extension (pretraining abduction = 93.8 ± 8.8%, posttraining abduction = 94.7 ± 4.3%; pretraining extension = 92.3 ± 5.1%, posttraining extension = 92.4 ± 4.5%). Voluntary activation measured via TMS was also unchanged for the control group (pretraining abduction = 97.2 ± 2.6%, posttraining abduction = 96.3 ± 4.4%; pretraining extension = 95.0 ± 4.1%, posttraining extension = 92.5 ± 6.6%).
Resultant twitch angle.
In the trained wrist, the angle of the resultant twitches evoked by TMS during wrist abduction contractions shifted toward the abduction direction (16.5° change at 100% MVC, P = 0.03; 13.6° change at 75% MVC, P < 0.01; 5.2° change at 50% MVC, P = 0.04). The resultant angle of twitches evoked during extension contractions at 100% MVC also shifted toward abduction (9.5° change, P = 0.04; Fig. 7). The resultant twitch produced by TMS represents the net contribution of all muscles activated by TMS that have a wrist joint moment. In the control group, the resultant twitch angle was unchanged for both extension and abduction contractions across all intensities.
In the present study, we quantified voluntary activation during wrist abduction and extension via motor nerve and motor cortical stimulation before and after a 4-wk unilateral wrist abduction strength training program. This is the first study to use TMS to examine cortical voluntary drive in the early phase of strength training. Wrist abduction strength training specifically improved abductor but not extensor MVC of the trained wrist. However, strength training did not alter voluntary activation of the wrist abductors during MVC, which suggests that a simple increase in cortical voluntary drive (to the wrist abductors) was not the primary mechanism responsible for the increase in maximal strength.
Only one other study has examined the effects of strength training on voluntary activation of upper limb muscles. Herbert et al. (21) found that 8 wk of strength training did not change voluntary activation of the elbow flexors despite a significant gain in voluntary strength. They noted that their results do not necessarily mean that the neural drive hypothesis should be abandoned, as training may have increased voluntary activation to other elbow flexor synergists in which voluntary activation was not measured (such as the brachioradialis) (21). In support of this, Allen et al.(3) reported that the brachioradialis muscle is generally less well activated than the biceps brachii and, therefore, has greater potential for improvement with strength training. This consideration is relevant to our results. Before strength training, voluntary activation of the wrist abductors, measured via both motor cortical and motor nerve stimulation, was already high for all subjects (via TMS = 95.4 ± 6.8%; via nerve stimulation = 98.4 ± 2.2%). Therefore, as reported for biceps brachii, the wrist abductors are well activated and may therefore have little scope for improvement. There are muscles that have an abduction moment at the wrist joint but are not activated by the radial nerve (e.g., flexor pollicis longus and flexor carpi radialis) (17) Therefore, the motor-nerve measure of voluntary activation obtained during wrist abduction contractions may overestimate the overall level of voluntary drive. This is less likely with the assessment of voluntary activation with motor cortical stimulation because TMS should activate all of the synergists involved during wrist abduction contractions. However, the TMS intensity and the stimulating coil were set to preferentially activate the primary wrist abductor and extensor muscle (extensor carpi radialis, ECR). We could not be certain that this "ECR-focused" TMS activated all of the synergists maximally because we did not record EMG selectively from many muscles that have an abduction moment. Furthermore, given the variability between subjects, it is possible that a small increase in voluntary activation was missed.
If an increase in voluntary activation of the main agonists was not responsible for the increase in strength after training, the question remains: what is the underlying mechanism? As there were no significant changes in the amplitudes of MEP and Mmax recorded from the wrist abductors (ECRB and ECRL) during voluntary contractions during the 4-wk period, this might support the conclusion that intramuscular changes occurred in the wrist abductors. This is relevant for muscles not innervated by the radial nerve because the average size and angle of the resting (potentiated) muscle twitch produced by supramaximal radial nerve stimulation was unaffected by training. Furthermore, in separate experiments conducted on a subsample of subjects involved in the current study, the same strength training intervention did not change the amplitude of twitches elicited by supramaximal radial nerve stimulation when elicited during wrist abduction or extension contractions at 50% MVC (i.e., under identical contractile conditions to the TMS-evoked force increments; ). However, muscles such as the flexor pollicis longus and flexor carpi radialis have an abduction moment at the wrist joint (17) but are innervated by nerves other than the radial nerve and could have adapted positively to strength training. The possibility of rapid peripheral change is supported by data that myofibrillar and collagen protein synthesis occur rapidly after acute bouts of strength training (23,28). A weakness of this interpretation is that it is difficult to explain why intrinsic muscle adaptations should be specific to nonradial innervated muscles.
The observations of increases in the amplitude of the superimposed twitches evoked by TMS during submaximal abduction, but not extension, contractions, and the shift in the direction of the superimposed twitches toward wrist abduction, are consistent with the training specificity principle. The results suggest a facilitation in corticospinal output, which is specific to the wrist abductors. A change in the direction of TMS-evoked twitches toward the training direction has been reported after practice of simple repetitive thumb movements (11). As the resting motor threshold and MEP amplitudes remained constant during the 4-wk period, an increase in cortical excitability in ECRcannot explain the increase in twitch amplitude.
One explanation for our results could be that after strength training, the subjects were able to activate (via volition and via TMS) more efficiently the cortical output cells with divergent connections to the wrist abductor motoneuron pools during voluntary contractions. This might contribute to an increase in the overall gain of the motoneuronal output to the group of wrist abduction synergists and lead to increased strength and TMS-evoked twitch amplitudes during submaximal efforts. This idea is supported by anatomical and neurophysiological evidence demonstrating that most corticospinal axons branch extensively within the spinal cord and terminate at multiple motoneuron pools at one or more spinal levels (15,41). The divergent projections to motoneuron pools of distal limb muscles are generally more extensive and stronger than those projections to proximal muscles (32), and some projections even suppress antagonist motoneurons during voluntary movements. An increase in activation of some corticomotoneuronal cells with divergent output to the wrist abductors after strength training could also explain the shift in the direction of the resultant twitches toward the abduction plane during abduction contractions. The observation that changes in twitch amplitude and the direction of the resultant twitch were more pronounced during submaximal contractions may be related to the fact that the twitch signal is much larger during submaximal thanmaximal efforts and is therefore easier to measure. The cortical output cells with divergent connections to the wrist abductor motoneuron pools are unlikely to have been fully activated by volition during submaximal contractions and would therefore have been accessible to cortical stimulation.
We also measured strength and voluntary activation changes in the opposite untrained wrist during the 4-wk period because it is well known that the benefit of unilateral strength training can generalize to the opposite limb (8,29). We found no significant change in MVC or voluntary activation of the untrained wrist. Although our results provide no evidence that cross-limb transfer of strength occurs at the wrist, a real effect may have been masked by the small sample size. For the elbow flexors, it is evident that a large sample size is required to detect the small cross-transfer of strength (30). In addition, there was a lack of training and testing specificity in the present study (i.e., dynamic training but isometric testing).
Four weeks of unilateral wrist abduction strength training significantly increased MVC force during abduction but not extension of the trained wrist. Our results suggest that an increase in neural drive to the main wrist extensors (ECR) was not the primary mechanism responsible for the strength improvements because voluntary activation (measured with motor nerve and motor cortical twitch interpolation) did not change. The data show that there was a specific facilitation of the corticospinal output to the wrist abductor muscles, which was large during submaximal abduction contractions. This may contribute to the small increase in maximal voluntary force produced by the wrist abductors after training.
The authors thank Justin Barton and Marlene Hsu for supervising training sessions and data collection and the Australian Research Council and the National Health and Medical Research Council for the financial support. The results of the present study do not constitute endorsement by ACSM.
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Keywords:©2009The American College of Sports Medicine
TWITCH INTERPOLATION; RESISTANCE TRAINING; CROSS-EDUCATION; NEURAL DRIVE