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Department of Exercise and Sport Sciences and Department of Neuroscience and Pharmacology, Panum Institute, University of Copenhagen, Copenhagen, Denmark
Submitted 29 October 2007 ; accepted in final form 19 June 2008
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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motor control; agonist-antagonist coordination; rate of torque development
This is especially important at the onset of fast and powerful contractions where inadvertent activation of the antagonist muscle, through descending activation or stretch reflex activity, would be an impediment for the initial acceleration of the muscle contraction (15). Therefore, effective reciprocal inhibition may play an important role in sports that require very fast and powerful activation of specific muscle groups, such as sprint and long and high jump. The ground contact time in these sports is in the order of 80–220 ms (18, 30, 31), which underlines the importance of fast force production. Improving the ability to develop a rapid rise in muscle force, i.e., increase the rate of force development (RFD), could reduce ground contact time for the sprinter and thus improve stride frequency and thereby acceleration (30).
Explosive strength training has been shown to result in an increased RFD within the early phase of muscle force production (0–200 ms) (1, 23, 41). Evidence that changes in the nervous system are responsible for these changes in RFD has been presented (1, 22, 23), but it is unclear to what an extent coordination of the activity in agonist and antagonist muscles are involved. Although the majority of studies measuring surface electromyograph (EMG) have found significant increases in agonist activation (1, 23, 41), only some have found a decrease in antagonist coactivation (6, 23), whereas others have not (3, 11, 26).
The role of agonist-antagonist coordination in fast movements can be further investigated by measuring the amount of DRI of the antagonist muscle at the onset of contraction after a period of training.
The purpose of the present study was therefore to test the hypothesis that DRI may be increased when subjects are trained to perform dorsiflexion movements as quickly as possible.
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METHODS |
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The experiments were performed on 14 healthy human subjects (6 men, 8 women) with an average age of 26 ± 7 yr. After the training experiment, a control group of six subjects (4 men and 2 women, 24 ± 3 yr) were tested on two occasions separated by 
4 wk of no training. None of the subjects had performed regular strength training in the last 6 mo before the experiments, and no subjects had any history of neurological disease. All subjects gave their written, informed consent to the experimental procedures, which were approved by the local ethics committee [j.nr. (KF) 100.1969/1991] and the study was performed in accordance with the Declaration of Helsinki.
General Organization of the Study
The participants in the training group performed 12 training sessions over a 4-wk training period (3/wk). In addition, each subject participated in an experimental session before the training period (pretest), the day after the last training session (posttest), and 2 wk after the training period (retest; Fig. 1). A retest after 2 wk was chosen because possible neural changes caused by the training sessions were expected to be short lived. Subjects were comfortably seated in an armchair, and the left leg was positioned with the hip semiflexed (120°), the knee flexed (110°), and the ankle at a slightly plantar-flexed position (140°). The left foot was firmly attached to a force pedal using adjustable straps. The experimental sessions involved 1) tests of the ability to contract the dorsiflexors as quickly and forcefully as possible and 2) evaluation of DRI at rest and at the onset of dorsiflexion.
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An auditory signal (a beep) told the subject to be ready, and on the following beep (3 s later) the subject was instructed to perform a brief maximal dorsiflexion with the aim of increasing the torque as rapidly as possible. The subject was given visual feedback of the torque applied to the pedal by a moving line on a monitor placed in front of the subject. This paradigm was repeated every 15 s for 4 min until 16 contractions had been performed. Each training session consisted of 3 of these sets of 16 dorsiflexions separated by 4-min rest periods and was performed 3 days a week for 4 wk.
Testing Procedures
Subjects were instructed to keep their head straight and not to talk while measurements were taking place.
Strength measurements. At the beginning of the testing procedure, the subjects warmed up for 5 min. The warm-up began with brief dorsiflexion movements (0.5–1 s) to about half of the maximal voluntary (dorsiflexion) contraction torque (MVC) and ended with three to five brief dorsiflexions to MVC (1–2 s). After the warm-up, the subjects were instructed to perform a dorsiflexion (1–2 s) to MVC with the aim of increasing the torque as fast as possible. Subjects were verbally encouraged to produce maximal torque and visual feedback of the torque was displayed by a moving line on the monitor. At least six trials were performed separated by 1-min rest periods.
EMG measurements. Surface electrodes were used for electrical nerve stimulation and recording of EMG activity. EMG activity was recorded from the anterior tibial (TA) and soleus (Sol) muscles by nonpolarizable bipolar electrodes (diameter 0.5 cm; Blue Sensor, Ambu, Ølstykke, Denmark) placed over the belly of the muscles with an interelectrode distance of 2 cm. The EMG signals were amplified (500–2,000x) filtered (band pass, 25 Hz to 1 kHz), sampled at 2 kHz, and stored on a PC for offline analysis (CED 1401+ with Spike 2.6 and Signal 3.07 software, Cambridge Electronic Design, Cambridge, UK).
All EMG and H-reflex measurements (see below) were normalized to the maximal M response (Mmax) evoked in either the TA or Sol muscle by supramaximal stimulation of the common peroneal nerve or the tibial nerve, respectively (for details of stimulation see below). In these measurements, the intensity of stimulation of the respective nerves was increased from a subliminal level until there was no further increase in the peak-to-peak amplitude of the M response with increasing stimulation intensity. The Sol Mmax was measured several times throughout the experiment to ensure that the H-reflex measurements were always standardized to the current size of Mmax, but changes were minimal and will not be mentioned further.
Maximal torque and half relaxation time were measured from the twitch evoked by supramaximal stimulation of the peroneal nerve and the tibial nerve.
H-reflex measurements. H reflexes were induced by stimulation (1-ms rectangular pulses; model DS7A, Digitimer, Hertfordshire, UK) of the posterior tibial nerve (PTN) using a ball-shaped monopolar electrode (Simon electrode) placed in the popliteal fossa. The anode was placed proximal to the patella.
The H reflex was used to evaluate DRI at rest and at the onset of contraction (13, 15, 17).
Evaluation of DRI at rest and during dorsiflexion. DRI of the Sol H reflex was evoked by conditioning stimulation of the common peroneal nerve (CPN) through bipolar surface electrodes (diameter 0.5 cm; Blue Sensor, Ambu) placed 1–3 cm distal to the neck of the fibula. Care was taken to ensure that the conditioning stimulus was applied at a position where the threshold for an M response [motor threshold (MT)] in TA was lower than the MT in the peroneal muscle. The specificity of this stimulation was checked several times during the experiments. In all subjects, a time course of the effect of CPN stimulation on the Sol H reflex was obtained at rest. A stimulation strength of 1.1 x MT was used in all trials to obtain a small M response in the TA muscle, which could be monitored throughout the experiments and used to ensure that the effect of the conditioning stimulus was comparable (40). Higher stimulation intensities were avoided to minimize an influence from other pathways than the disynaptic Ia reciprocal pathway to the measured inhibition (40). Also, a stimulation intensity of 1.1 x MT is submaximal for activation of all inhibitory interneurons and thus permits that both facilitatory and inhibitory effects may be demonstrated (40). An H reflex was elicited every 5 s and preceded by either nothing (control) or a conditioning stimulation of the CPN with conditioning-test (CT)intervals from 1 to 6 ms in 1-ms steps. At least 10 control and 10 conditioned reflexes (at each CT interval) were sampled at each testing session.
The CT interval that produced the largest inhibition (either 2 or 3 ms) was then used to evaluate DRI at onset of dorsiflexion. At these intervals, only DRI is likely to contribute to the measured inhibition (13). An auditory signal (a beep) warned the subject to be ready and on the following beep (3 s later) to perform a brief maximal dorsiflexion with the aim of increasing the torque as quickly as possible. A window discriminator made it possible to time the stimulation relative to the onset of TA EMG activity. The size of the control reflex at the onset of dorsiflexion was matched with the control reflex size at rest (13, 14). Trials were randomized so that subjects were presented with test stimulation only, test stimulation preceded by a conditioning stimulation, or no stimulations. This paradigm was repeated every 15 s until at least 10 trials of each condition had been obtained.
Each individual response was measured and the average H-reflex amplitudes were calculated in each situation and stored on a PC for offline analysis.
One subject got a leg cramp in the pretest, which made it impossible for the subject to perform more dorsiflexions. In another subject, it was not possible to elicit an H reflex of a reasonable size (<10% of Mmax) in the posttest of this experiment, and it was therefore not possible to compare the data to the pre- and retest data. These subjects were therefore excluded from the analysis of the experiments described in this section.
The size of the control H reflex was adjusted to 15–25% of Mmax in all conditions unless stated otherwise (14). In the post- and retest, an effort was made to keep the control reflex of each subject as close to the pretest value as possible.
A 5-s interstimulus interval was used for DRI measures at rest for practical reasons, but at this interval postactivation depression may potentially influence the inhibition. However, postactivation depression is relatively small at 5-s interstimulus interval and because the intervals used were the same before and after training postactivation depression should not influence the DRI findings. Occlusion is also very unlikely to play a role because submaximal stimulation intensities were used.
Offline analysis. The voluntary dorsiflexion torque was calculated at different time points (30, 50, 100 and 200 ms; Fig. 2A) following onset of contraction (0 ms, defined as the baseline plus 2 SDs). Values from all six trials were averaged. The term rate of torque development (RTD) was used to designate these measurements.
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Out of the six trials performed, the trial that produced the highest peak torque (independent of time) was used for the analysis of the MVC.
EMG activity from TA and Sol was analyzed to investigate the amount of cocontraction during dorsiflexion. The resolution of the raw amplified TA EMG was increased to allow for precise visual inspection of the onset of TA EMG. The root-mean-square amplitude in the raw Sol and TA EMG was then calculated for the first 30, 50, 100, and 200 ms relative to onset of TA EMG in each trial.
The TA and Sol EMG data were then related to the Mmax in TA and Sol, respectively, and finally expressed relative to each other to calculate the amount of coactivation.
Statistics
Statistical analysis was done using Sigmastat 2.03 (SPSS). Before statistical comparison, all data sets were tested for normal distribution by a Kolmogorov-Smirnov test. The mean and SE were calculated online for all measurements involving peripheral nerve stimulation.
Differences in the size of the conditioned and control reflexes within the same session were tested using paired t-test. Long-term adaptations to training were investigated by comparing post- and retraining data with pretraining data using repeated-measures ANOVA. For multiple-comparison analysis, post hoc Tukey's test was used for all pairwise comparisons between the group mean responses. DRI during dorsiflexion was compared with DRI at rest using paired t-test and a Spearman rank order analysis were used to test for any correlation between changes in DRI and RTD parameters.
Statistical significance is given for P values of 0.05, 0.01, and 0.001 in the figures. Data are presented as means ± SE unless reported otherwise.
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RESULTS |
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Following the 4 wk of explosive strength training RTD increased significantly for all measured time periods: 0–30 ms by 32% (P < 0.05), 0–50 ms by 33% (P < 0.05), 0–100 ms by 30% (P < 0.05), and 0–200 ms by 24% (P < 0.05). RTD measured in the retest was not significantly different from pre- (P = 0.07–0.22) or posttest values (P = 0.51–0.97), although RTD in the first 200 ms in the retest was 20–30% higher than in the pretest. The MVC increased by 20% (P < 0.01) after training and was still significantly increased, by 21% (P < 0.01), in the retest 2 wk after (Fig. 3).
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An increase in the absolute TA EMG was found for all time periods (Table 1), but this did not reach statistical significance (P = 0.3–0.5). This was also the case when the EMG was expressed relative to Mmax (Table 1).
The maximal torque and half relaxation time of the twitch evoked by supramaximal stimulation of either the peroneal nerve (2.78 ± 0.38, 2.91 ± 0.50, and 2.98 ± 0.51 N·m, P > 0.5; and 79 ± 5, 73 ± 6, and 81 ± 5 ms, P > 0.3, respectively) or the tibial nerve (6.59 ± 0.70, 6.10 ± 0.74, and 6.23 ± 0.91 N·m, P > 0.5; and 108 ± 9, 115 ± 11, and 104 ± 11 ms, P > 0.3, respectively) were of the same size in all three sessions (pretest, posttest, and retest).
DRI
Figure 4 illustrates the time course of the inhibition of the Sol H reflex at rest following single stimuli at 1.1 x MT to the CPN expressed relative to the unconditioned H-reflex size. The inhibition was apparent when the conditioning CPN stimulation preceded the PTN test stimulus by 2 ms (87.0 ± 3.5, 85.3 ± 3.0, 82.4 ± 3.1%), 3 ms (85.8 ± 2.7%, 84.1 ± 4.1, 83.4 ± 3.4%), and 4 ms (88.8 ± 3.1, 88.8 ± 4.9%, 89.2 ± 4.5%) in the pre-, post-, and retest, respectively (Fig. 4). No differences in DRI were observed between the pre-, post-, and retest data at rest at any of the CT intervals (P = 0.49–1.0).
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DISCUSSION |
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Increased RTD and MVC
Strength training of the ankle dorsiflexors has only been investigated in a few previous studies (12, 20, 25), and to our knowledge changes in RTD of the ankle dorsiflexors with strength training have not been reported previously. The increases in RTD and MVC with strength training observed in this study were similar to those reported in previous studies in which isometric training of the ankle plantar flexors for a similar duration were investigated (5, 21, 24). They are also similar to the improvements in muscle strength reported for the quadriceps muscle observed in numerous studies (1, 6, 41).
We decided to use a 4-wk training period in the present study to increase the likelihood that significant changes in RTD and MVC would be obtained, although this may seem rather long when the purpose is to determine neural plastic changes. Such changes may be seen after only 30 min of training and may diminish with prolonged training (28, 37). However, the training period is similar to that used in other studies on changes in rate of force and EMG development following strength training (7, 24, 28).
We decided to make a retest 2 wk after the end of the training, because we expected that possible changes in DRI in relation to the training would be gone at this time (28, 37). It was the hope that the retest could thereby also serve as a control measurement.
We cannot exclude that changes in muscular properties (i.e., muscle fiber type changes, increased cross-sectional area, etc.) contributed to the changes in MVC and RTD following the training. The lack of change in the muscle twitch evoked by supramaximal nerve stimulation in either the TA or the Sol muscle suggests that significant changes in muscle properties did not take place following this relatively short training period. This is also supported by most other studies that have found that significant changes in muscle fiber types and cross-sectional area take considerably longer to develop (19). Although we cannot rule out that muscular changes contributed, we believe that the most likely explanation of the increased RTD is that the voluntary drive to the muscle increased following training. In the retest, MVC was still significantly higher than before training, but the RTD was not. This may indicate that RTD depends more on changes in neural drive than MVC, but because there were no statistical differences between the post- and retest RTD, a more likely explanation is that it simply reflects the larger variability in the retest data. The values for the RTD were thus numerically of an almost similar magnitude in the retest as in the posttest (Table 1).
Antagonist coactivation. Very little EMG activity was observed in the antagonist (Sol) muscle during the dorsiflexion contraction even before training (see Fig. 2), and it is therefore not surprising that there was no reduction of coactivation following the strength training. The low level of coactivation is probably explained by the use of isometric contractions (in which there is little risk of stretching the antagonist at the onset of contraction), and it may be argued that we might have observed significant changes in coactivation if subjects had performed concentric dorsiflexions instead. Significant changes in coactivation have indeed been observed in some studies (6, 23) but not in others (3, 11, 26). It seems obvious that at least in the present study reduced coactivation at the onset of dorsiflexion does not explain the increase in RTD with strength training. The other way around it does, however, seem likely that increased DRI (see below) may be of importance to maintain the amount of coactivation constant while increasing RTD in relation to the training.
Increased Facilitation of DRI at Onset of Dorsiflexion Following Strength Training
To our knowledge, the present study is the first to demonstrate adaptive training-related changes in reciprocal inhibition during a functional motor task in humans. In the rat, adaptive changes in DRI from TA to Sol have recently been demonstrated following a period of operant conditioning (8). Previous studies in humans have demonstrated training-related changes in presynaptic inhibition of Ia afferents, whereas no change in reciprocal inhibition was observed even following training that involved improvement in the coordination of antagonistic muscle pairs (39). Reciprocal inhibition appears to be smaller in professional ballet dancers than in other people with a similar daily activity level, but it is unclear whether this difference is due to specific training (32). Transmission in the DRI pathway has been shown to be influenced by activity in sensory afferents in some studies (17, 38) but not in others (42).
Our observation of increased DRI at the onset of dorsiflexion relative to rest has been reported in several previous studies (13, 15), in which it has also been demonstrated that the increase of DRI precedes the onset of EMG activity in the dorsiflexors by 50 ms. This demonstrates that the increase of DRI is caused by central (descending) facilitation of transmission in the DRI pathway. As mentioned already in METHODS it is a prerequisite for this conclusion that the Sol H-reflex size and the intensity of the conditioning stimulation of the peroneal nerve are comparable at rest and at the onset of dorsiflexion (13, 14, 16). This was the case in the present study.
The lack of change in DRI at rest suggests that the training did not induce any plastic changes in the reciprocal inhibitory pathway itself. The larger facilitation of DRI at the onset of dorsiflexion following the training is therefore more likely explained by increased supraspinal drive to the ankle dorsiflexors and, through collaterals, also to the inhibitory interneurons responsible for reciprocal inhibition of the antagonistic Sol motoneurons. Several descending pathways may contribute to this increased parallel drive to motoneurons and their corresponding reciprocal inhibitory interneurons, but one important pathway is the corticospinal tract. It has thus been demonstrated that a large proportion of corticomotoneuronal cells, of which many have collaterals to reciprocal inhibitory interneurons, increase their discharge around EMG onset and show a clear correlation to the rate of force development during the subsequent movement (9). In human subjects, an increase of corticospinal excitability, which is related to both the speed and acceleration of the subsequent contraction, has likewise been demonstrated (33).
It would therefore be expected that the increased facilitation of DRI at the onset of dorsiflexion had been correlated to the increase of RTD following the training, but this was not the case. There may be several reasons for this. The increase in RTD following the training likely not only reflects not only the supraspinal drive to the dorsiflexor motoneurons but also changes in the spinal motoneurons (43), the motoneuronal pool [i.e., recruitment gain (29)], the muscle (4) or sensory feedback mechanisms (3). Furthermore, only part of the supraspinal drive to agonist motoneurons is coupled to the inhibition of the antagonists, and it would therefore be conceivable that an increased drive to the agonists may be unaccompanied by changes in reciprocal inhibition. Finally, the variability of both the measurement of DRI and RTD may obscure any correlation between the two in a small population of subjects as in the present study.
Functional Significance of Findings
All measurements and training in the study were performed under isometric conditions (because the measurements of DRI would otherwise not be possible), where the risk of eliciting stretch reflexes in the antagonist muscle is relatively little. This makes it difficult to evaluate the functional significance of the increased reciprocal inhibition of the ankle plantar flexors following the training. However, if measurements during actual movement had been possible, we find it likely that at least a similar if not even larger increase in DRI would have been observed, and we would argue that such an increase could be of importance for reducing the risk of eliciting stretch reflexes in the plantar flexors at the onset of the rapid dorsiflexion. It is also not possible to make any conclusions regarding the role of the increase in DRI for preventing coactivation of the antagonists, because no or very little coactivation of the Sol muscle was seen even before training. However, as already mentioned, we find it likely that the increased DRI following the training may help to reduce antagonist motoneuronal excitability and coactivation of antagonists when the speed and force of dorsiflexion are increased in relation to the training.
In most earlier studies on neural plasticity in relation to motor learning, measurements have been performed at rest (7, 10, 36). Although such studies certainly document plastic changes in the investigated networks, they do not necessarily reveal adaptations that are of functional importance for the performance of the trained task. It is thus a strength of the present study that we were able to document that DRI was unchanged at rest, but it increased at the onset of dorsiflexion following strength training. Aagaard et al. (2) similarly found that the H reflex only increased during contraction, not at rest, following strength training (2).
The conclusion of the study is thus that 4 wk of explosive isometric strength training may induce changes in the central facilitation of transmission in the spinal reciprocal inhibitory pathway at the onset of dorsiflexion. We speculate that this may help to ensure efficient suppression of the antagonist muscles as the dorsiflexion movement becomes faster.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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), posttest (
), and retest (
). The intensity of the conditioning CPN stimulation was adjusted to 1.1 x motor threshold, and the size of the control H reflex was adjusted to 
