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Strength training, but not endurance training, reduces motor unit discharge rate variability
Accepted Manuscript Strength training, but not endurance training, reduces motor unit discharge rate variability Carolina Vila-Chã, Deborah Falla PII: DOI: Reference:
S1050-6411(15)00206-0 http://dx.doi.org/10.1016/j.jelekin.2015.10.016 JJEK 1912
To appear in:
Journal of Electromyography and Kinesiology
Received Date: Revised Date: Accepted Date:
13 July 2015 29 September 2015 27 October 2015
Please cite this article as: C. Vila-Chã, D. Falla, Strength training, but not endurance training, reduces motor unit discharge rate variability, Journal of Electromyography and Kinesiology (2015), doi: http://dx.doi.org/10.1016/ j.jelekin.2015.10.016
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STRENGTH TRAINING, BUT NOT ENDURANCE TRAINING, REDUCES MOTOR UNIT DISCHARGE RATE VARIABILITY
Carolina Vila-Chã1,2*, Deborah Falla3 1
Research Unit for Inland Development - Polytechnic Institute of Guarda, Av. Dr. Francisco Sá Carneiro, n. 50, 6300-559, Portugal 2
Research Center in Sports Sciences, Health and Human Development (CIDESD), Quinta de Prados, 5001-801 Vila Real, Portugal.
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Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Von-Siebold-Str. 6 Göttingen, Germany
Address for correspondence: * Carolina Vila-Chã Polytechnic Institute of Guarda, Av. Dr. Francisco Sá Carneiro, n. 50, 6300-559,Portugal Tel: +351 271220135 Email: [email protected]
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STRENGTH TRAINING, BUT NOT ENDURANCE TRAINING, REDUCES MOTOR UNIT DISCHARGE RATE VARIABILITY
Carolina Vila-Chã1,2*, Deborah Falla3 1
Research Unit for Inland Development - Polytechnic Institute of Guarda, Av. Dr. Francisco Sá Carneiro, n. 50, 6300-559, Portugal 2
Research Center in Sports Sciences, Health and Human Development (CIDESD), Quinta de Prados, 5001-801 Vila Real, Portugal.
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Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Von-Siebold-Str. 6 Göttingen, Germany
Address for correspondence: * Carolina Vila-Chã Polytechnic Institute of Guarda, Av. Dr. Francisco Sá Carneiro, n. 50, 6300-559,Portugal Tel: +351 271220135 Email: [email protected]
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ABSTRACT
This study evaluates and compares the effects of strength and endurance training on motor unit discharge rate variability and force steadiness of knee extensor muscles. Thirty sedentary healthy men (age, 26.0 ± 3.8 yrs) were randomly assigned to strength training, endurance training or a control group. Conventional endurance and strength training was performed 3 days per week, over a period of 6 weeks. Maximum voluntary contraction (MVC), time to task failure (at 30% MVC), coefficient of variation (CoV) of force and of the discharges rates of motor units from the vastus medialis obliquus and vastus lateralis were determined as subjects performed 20 and 30% MVC knee extension contractions before and after training. CoV of motor unit discharges rates was significantly reduced for both muscles following strength training (P<0.001), but did not change in the endurance (P=0.875) or control groups (P=0.995). CoV of force was reduced after the strength training intervention only (P<0.01). Strength training, but not endurance training, reduces motor unit discharge rate variability and enhances force steadiness of the knee extensors. These results provide new insights into the neuromuscular adaptations that occur with different training methods.
Keywords: force steadiness, discharge rate variability; strength training, endurance training.
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INTRODUCTION During submaximal voluntary contractions, the force produced is not constant but rather force fluctuates around an average level (Enoka et al. , 2003, Laidlaw et al. , 1999, Latash, 1998, Schiffman and Luchies, 2001, Slifkin and Newell, 1999). Such variability of force affects the capacity of an individual to accurately achieve a desired force level or move their limb through an intended trajectory (Latash, 1998, Slifkin and Newell, 1999). The variability of force output is determined by several mechanisms related to motoneuron properties and the synaptic inputs that they receive, which may influence the amount of synaptic noise imposed on the membrane potential during the afterhyperpolarization trajectory (Heckman and Enoka, 2004, Moritz et al. , 2005). These mechanisms can be modulated by several conditions including training, aging and disuse (Duchateau et al. , 2006, Kernell, 2006). Such alterations would not only affect the control scheme by which motor unit activity grades the amount of muscle force exerted (recruitment and rate-coding properties), but may also change the interspike interval (ISI) variability which may further affect the extent of force fluctuations (Enoka et al. , 2003). Although several studies have shown that motor unit discharge rate variability has a significant effect on the extent of force fluctuations during isometric voluntary contractions (Enoka et al. , 2003, Laidlaw et al. , 1999, Moritz et al. , 2005), the results are not unanimous (Beck et al. , 2011). This observation suggests that the amplitude of the force fluctuations can be also influenced by mechanisms other than motor unit discharge variability such as the muscle group performing the task (Kornatz et al. , 2005, Krishnan et al. , 2011), the type of load supported by the limb (Mottram et al. , 2005), the type and intensity of the muscle contraction (Christou et al. , 2003a, Laidlaw et al. , 1999), the aging process (Tracy and Enoka, 2002) and the physical activity status of the individual (Carville et al. , 2007, Enoka et al. , 2003). Also, the degree of force steadiness can be affected by different forms of training (Hortobagyi et al. , 2001, Keen et al. , 1994).
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Studies have shown that skill training contributes to improved force steadiness of hand (Kornatz et al. , 2005) and knee extensors muscles (Christou et al. , 2003b, Hart and Tracy, 2008). Nevertheless, the effects of other forms of training on force steadiness remain unclear. For instance, Beck et al. (2011), did not observe changes in force fluctuations of the knee extensors following 8 weeks of strength training. Conversely, Kornatz et al. (2005) showed increased force steadiness following 2 weeks of isometric training with a light load but no further increase following 4 weeks of training with a higher load. Even less is known about the effects of endurance training on force steadiness. It has been shown that endurance training changes single motor unit behavior (Kernell, 2006, Vila-Cha et al. , 2010), which potentially could affect motor output variability, including force fluctuations. However, the impact of such changes on force steadiness has not been assessed. The degree of force steadiness is an important parameter since it provides meaningful information on motor coordination and movement control (Christou et al. , 2003a, Seynnes et al. , 2005). Therefore, understanding how different training programs can affect force steadiness and subsequently functional movement, it is of extreme importance. Hence, the purpose of this study was to evaluate and compare the effects of strength and endurance training on motor unit discharge rate variability and force steadiness of knee extensor muscles. We hypothesized that force steadiness would improve following both training programs, which would be accompanied by reduced motor unit discharge rate variability. The knowledge gained will help to further clarify the neuromuscular adaptations to both strength and endurance training, which is relevant for rehabilitation, exercise and sports science. METHODS This study was part of a longitudinal study on neuromuscular adaptations to training and the experimental protocol has been partially described in Vila-Chã et al. (2010). The common methodology to both studies will be briefly reported here.
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Subjects Thirty healthy men (age, mean ± SD, 26.0 ± 3.8 yrs) with no history of lower limb disorders participated in the study. None of the subjects were involved in regular strength or endurance training. All subjects gave their informed consent to the procedures of the study. The study was conducted in accordance with the Declaration of Helsinki and approved by the local ethics committee (20090032). After the first experimental session (pre-training session), the subjects were randomly assigned to one of three groups: strength training (n = 10); endurance training (n = 10); or a control group (no exercise intervention) (n = 10). One subject from the strength group and two subjects from the control group did not complete the final experimental session and were excluded from the analysis. Thus, the results are presented for 9 subjects in the strength group (age, 25.4 ± 4.2 yrs; height, 183.4 ± 6.9 cm; weight, 80.3 ± 16.3 kg), 10 subjects in the endurance group (age, 26.1 ± 2.8 yrs; height, 180.6 ± 6.2 cm; weight, 78.3 ± 14.1 kg) and 8 subjects in the control group (age, 27.0 ± 5.0 yrs; height, 175.3 ± 3.4 cm; weight, 78.0 ± 13.0 kg).
Training programs The training regimes have been described in detail previously (Vila-Cha et al. , 2010). Briefly, endurance or strength training was performed over 6 weeks including a total of 18 sessions. Load intensity was progressively increased over the training period in both programs. Endurance training was performed on a bicycle ergometer and the exercise intensity was prescribed based on the percent of the heart rate reserve (HRR) according to the Karvonen method (Karvonen et al. , 1957). The load intensity ranged between 50 to 70% of the HRR and the duration of the sessions between 20 and 50 min. The strength training included three bilateral leg exercises (leg press, leg extension, and leg curl) and a set of additional exercises for other main muscles groups of the body ( lateral
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pull down, bench press, exercises for trunk muscles) . The subjects trained with loads of 60-85% of the one-repetition maximum (1RM) and performed 3-4 sets of 8-15 repetitions. All training sessions were supervised by a training expert who continuously monitored the training programs allowing the necessary adjustments to keep the intensity at the required level.
Procedure The subjects attended two laboratory sessions, immediately before (session 1 – pre) and after completion of the 6-week training period (session 2 – post). In order to avoid an effect of the fatigue on the results, session 2 was conducted at least 48h after the last training session. For each laboratory session, the subject was comfortably seated on an Isokinetic dynamometer (KinCom Dynamometer – Chattanooga, TN, USA) with the trunk reclined to 15º in an adjustable chair and the hip and distal thigh firmly strapped to the chair. The rotational axis of the dynamometer was visually aligned with the lateral femoral epicondyle. The right leg was secured to the dynamometer’s attachment above the lateral malleolus with the knee in 90º of flexion. Progressive maximal voluntary contractions (MVC) of the knee extensors were measured twice, with 2-min rest in between. The maximum of the two force measures was used as a reference for the definition of the submaximal force levels. In both experimental sessions, the submaximal forces were relative to the MVC measured during the same session. Subjects were then asked to perform two repetitions of isometric contractions at 10, 20 and 30% MVC (random order) for 15 s whilst maintaining the force as steady as possible. Subjects were provided with online visual feedback of the force exerted which was displayed on an oscilloscope positioned 100 cm in front of the subject. After 2-min of rest, the subjects performed an isometric knee extension at 30% MVC maintaining the force for as long as possible (endurance task). Time to task failure was defined as a drop in force greater than 5% of the target force level for more than 5 s, despite strong verbal
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encouragement to the subject to maintain the target force. During all submaximal contractions, knee extension force and intramuscular electromyography (EMG) were recorded concurrently.
EMG and Force Recordings Single motor unit action potentials were recorded using two pairs of hook wire electrodes (50-µm-diameter) made of Teflon coated stainless steel (A-M Systems, Carls, WA, USA) and inserted with a 23 G needle into the vastus lateralis (VL) and vastus medialis obliquus (VMO) muscles. The electrodes were inserted distally to the innervation zone of the respective muscles, which was inspected in advance using a liner array of 8 equi-spaced silver electrodes (OT Bioelettronica, Torino, Italy), as previously described (Farina et al. , 2002, Masuda et al. , 1983). The wires were uninsulated for ~1mm at the tip. The angle of insertion of the needle was ~ 45°, and the depth was a few millimeters below the muscle fascia. The needles were removed after insertion and the wire electrodes were left inside of the muscle for the duration of the measurement session. The force produced by the knee extensor muscles during the isometric contractions was measured with a load cell incorporated in the Isokinetic dynamometer (KinCom Dynamometer – Chattanooga, TN, USA, 0.0048 V/N). Intramuscular EMG signals (bipolar derivations) were amplified (Counterpoint EMG, DANTEC Medical, Skovlunde, Denmark), band-pass filtered (500 Hz – 4 kHz), sampled at 10,000 Hz, and stored after 12-bit A/D conversion. Force signals were sampled at 10,000 Hz.
Signal analysis The recorded intramuscular signals were decomposed into the constituent motor unit action potentials by a decomposition algorithm previously validated (McGill et al. , 2005). Unusually short (<20 ms) or long (>200 ms) time intervals between subsequent detected discharges of the
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individual motor units were manually reanalyzed to check potential discrimination errors and then corrected when necessary. The mean discharge rate [pulses per second (pps)] and interspike interval variability (ISI) were computed from the motor unit spike trains. The force signals were low passfiltered (10Hz) and coefficients of variation (CoV) for the ISI and for the force signal were computed as a ratio (%) between the standard deviation and the mean values during time intervals of 10s duration. The contractions at 10% were excluded since the CoV of force at 10% MVC could not be computed in a reliable manner due to the presence of electrical noise for these low force contractions.
Statistical analysis The effects of the endurance and strength training programs on the CoV of the ISI for the VL and VMO were evaluated with four-way repeated measures analysis of variance (ANOVA) with factors group (control, endurance, and strength), training period (pre and post), load (20, 30% MVC) and muscle (VL, VMO). A three-way repeated measures ANOVA was applied to the CoV of force with factors group, training period and load. Two-way repeated measures ANOVA with factors group and training period was applied to assess changes in the MVC and time to task failure. The normality and equality of covariance matrices were tested prior to performing the repeated measures ANOVA. To investigate associations between the variables affected by training, a regression analysis was performed with the percent change (from baseline) in the CoV of the ISI for the vasti muscles as the independent variable and the percent change in force steadiness as the dependent variable. The regression analysis was performed separately for each training group. Statistical significance was designated at P < 0.05 for all comparisons. Results are reported as means and standard deviation (SD) in the text and mean and standard error (SE) in the figures.
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RESULTS Maximum Force and Time to Task Failure Strength training led to an increase of the knee extension MVC force by 17.5 ±7.5% (from 532.1 ±107.9 N to 622.7 ± 118.6 N, P < 0.05) but did not influence time to task failure (from 177.2 ± 68.2 s to 174.6 ± 63.4 s). Conversely, 6 weeks of endurance training increased the time to task failure by 29.1 ± 11.9% (from 131.0 ± 26.9 s to 160.2 ± 33.7 s, P < 0.05) but did not affect knee extension MVC force (from 531.3 ± 95.3 N to 507.7 ± 126.5 N). Motor output did not change in the control group (MVC: from 549.5 ± 68.5 N to 554.4 ± 47.2 N; time task failure: from 128.8 ± 69.1 s to 123.7 ± 73.3 s).
Force Steadiness Force steadiness of the knee extensors improved with strength training but not with endurance training (group x time: P < 0.05; Fig. 1). After six weeks of strength training the CoV of the force during the submaximal contractions decreased by 27.2±17.1% overall (P < 0.01; Fig. 1). Although a reduction in the CoV of the force occurred following endurance training, this was not significant (P = 0.11; Fig. 1). No changes were observed in the control group (P = 0.99; Fig. 1).
Figure 1 about here
Motor Unit Discharge Rate Variability Discharge rate variability was computed from a total of 1017 motor units identified from the contractions at 20 and 30% MVC in both experimental sessions (pre and post training).
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The loads used in this study did not significantly influence motor unit discharge rate variability (P = 0.33), nevertheless during the contraction at 20% MVC, vasti motor unit discharge rate variability was higher than at 30% MVC (13.1± 3.5% vs 12.4± 2.9%, respectively). The results showed that the motor unit discharge rate variability in the VMO was significantly higher than in the VL muscle (13.3 ± 3.3% vs 12.1± 3.1%; P = 0.01). No interaction between time and muscle was observed, which indicates that motor unit discharge rate variability for both muscles followed similar trends over time. A group by time interaction was observed for motor unit discharge rate variability (P < 0.001; Fig. 2). Discharge rate variability was significantly reduced for both muscles following strength training (P = 0.001; Fig. 2), but did not change in the endurance training (P = 0.875; Fig. 2) or control group (P = 0.995; Fig. 2). Figure 2 about here
Relations between Discharge Rate Variability and Force Steadiness Although motor unit discharge rate variability showed similar trends over time for both muscles, in the strength training group, only the percent change in discharge rate variability of VMO motor units was significantly associated with the percent change in CoV of force at 20% (P = 0.04; r2 =0.51, Fig. 3(A)) and 30% MVC (P = 0.02; r2 =0.49, Fig. 3(B)). There was no correlation between MVC and force steadiness at 20% MVC (P = 0.377) or 30% MVC (P = 0.190) for this group. No relation between the percent change of discharge rate variability of the vasti motor units and the percent change of CoV of force at 20 and 30% MVC were observed for the endurance group or the control group.
Figure 3 about here
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DISCUSSION This study evaluated the effect of different forms of training on motor unit discharge rate variability and force fluctuations during submaximal isometric contractions of the knee extensors. The results demonstrate that 6 weeks of strength training, but not endurance training, reduces motor unit discharge rate variability of the vasti muscles and enhances force steadiness. Only the reduction of discharge rate variability for VMO motor units was significantly correlated with the decline in the CoV of force. These alterations represent early adaptations to training, since the subjects were not involved in regular physical activity before the study.
Training and force steadiness The force fluctuations of the knee extensors during low-level submaximal contractions decreased by approximately 27% following six weeks of strength training, but did not change significantly after endurance training. Previous studies have mostly examined the influence of strength training (Hortobagyi et al. , 2001, Laidlaw et al. , 1999, Tracy and Enoka, 2006) or skill training (Christou et al. , 2003b, Hart and Tracy, 2008, Kornatz et al. , 2005) on force steadiness in older adults. Although endurance training is known to induce a number of early neuromuscular adaptations, little is known about the influence of this form of training on force steadiness. To the best of our knowledge, only the study of Cracaft et al. (1975) investigated the effect endurance-type training on motor unit discharge rate variability. This study showed that a 6-week protocol of local endurance training of the dorsiflexor muscles (three times per week of dynamic low load intensity and long duration exercise) produced a decrease in tibialis anterior motor unit discharge rate variability, however the impact of such an alteration on force steadiness was not measured
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(Cracraft, 1975). In the current study, we observed a reduction of the CoV of the force by 13% following endurance training, yet this change was not statistically significant. Moreover there was no significant change in motor unit discharge rate variability. Thus, although studies have confirmed that endurance training alters motor unit behavior and neural circuits (Kernell, 2006, Perot et al. , 1991, Vila-Cha et al. , 2010), these alterations do not seem to influence the mechanisms that control force output variability during submaximal isometric contractions. We hypothesized that, following a short period of endurance training, the negative effects of a decline in motor unit discharge rate on force steadiness, may have been compensated by an increase in the number of active motor units due to lower and clustered recruitment thresholds (Adam et al. , 1998). This reorganization may contribute to improve energy efficiency, and subsequently resistance to fatigue, without compromising the motor output. Some studies support the importance of strength training for promoting improvement in force steadiness (Christou et al. , 2003b, Hart and Tracy, 2008, Keen et al. , 1994). Nonetheless, the results are contradictory. For example, Laidlaw et al. (1999), showed that 4 weeks of resistance training of the hand muscles of older adults significantly improved maximal strength and force steadiness during isometric, concentric, and eccentric muscle actions. Conversely, Hortobágyi et al. (2001), demonstrated that 10 weeks of strength training of the knee extensors muscles of older adults, increased muscle strength and increased force steadiness during dynamic but not during isometric submaximal contractions. On the other hand, Beck et al. (2011) showed that 8 weeks of knee extensor strength training resulted in a significant increase in maximal strength of the knee extensors of young adults but force steadiness during isometric contractions at 80% MVC remained unchanged. In the current study, we observed an improvement of both knee extensor muscle strength and force steadiness during submaximal isometric contractions (20 and 30% MVC) after 6weeks of strength training yet no correlations were found between these variables. This suggests
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that for young adults, increments in muscle strength and force steadiness are likely mediated by distinct mechanisms. The differences between the results obtained in the current study and that of Beck et al. (2011), might be explained by differences in the load intensity applied in each study to evaluate force steadiness (i.e. 80% versus a maximum of 30% MVC). Although the standard deviation of force during an isometric contraction increases with the target force level, the CoV presents a nonmonotonic relation with higher values observed at lower force levels, intermediate values at intermediate forces and moderate values at forces greater than 50% MVC (Enoka et al. , 2003). Therefore, the different findings in these studies might be partly explained by the different range of load intensities used to evaluate force steadiness.
Discharge rate variability and force steadiness Motor unit recruitment and discharge rate modulation can influence force fluctuations by changing the degree of twitch fusion (Taylor et al. , 2003). Nevertheless, changes in force steadiness have been associated with alterations of motor unit discharge rate variability rather than changes of other parameters of motor unit behavior (Enoka, 1997, Kornatz et al. , 2005, Moritz et al. , 2005). Our previous studies showed that strength and endurance training programs elicit early and opposite adjustments in motor unit behavior (Vila-Cha et al. , 2010) and neural circuits (VilaCha et al. , 2012). The results confirmed that short periods of endurance training induces a decline in the motor unit discharge rate and enhances motor neuron excitability. However these alterations do not seem to influence the mechanisms that control motor unit discharge rate variability and force fluctuations. Motor unit discharge variability and force fluctuations can be modulated by common inputs to a motor unit pool which are governed by central descending pathways (Taylor et al. , 2003). Nonetheless, previous work showed that following endurance training, the enhanced motor
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unit pool excitability appears to be mediated by spinal circuits rather than by descending pathways. This may partially explain why motor unit discharge rate variability and force fluctuations remained unchanged despite early changes in recruitment and rate-coding properties of the motor unit population. Contrary to endurance training, strength training elicited a decrease of vasti motor unit discharge rate variability which was associated with an improvement of the force steadiness of the knee extensors. Previous work has shown that strength training increases motor unit discharge rates (Vila-Cha et al. , 2010) and these early adaptations can be explained by increased excitability of the motor neuron pool governed by descending pathways (Vila-Cha et al. , 2012). Although the changes in the motor unit recruitment and discharge rates may have contributed to reduced motor unit discharge variability, it is very likely that other mechanisms, such as synchronization and the common modulation of motor unit discharge rates may be involved. In the present study, a moderate association was observed between motor unit discharge rate variability and force steadiness during isometric contractions at 20 and 30%MVC, supporting the association between the extent of motor unit discharge rate variability and the degree of force steadiness. Konartz et al. (2005), also observed a weak association between fluctuations in index finger acceleration and motor unit discharge rate variability. Moreover, this relation was characterized by a parallel decline of motor unit discharge rate variability and the standard deviation of acceleration fluctuations of hand muscles in response to training. These observations are strengthened by computer modeling approaches, which show that when the discharge rate variability of a motor unit pool is manipulated, significant alterations in force steadiness occur (Moritz et al, 2005).Nonetheless such an association was only observed for the VMO muscle. This might be explained by a different time course of vasti muscle adaptations to strength training. Some studies have reported differences in the magnitude and time course of muscle architecture
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adaptations of the VL and VMO to high-intensity strength training (Blazevich et al. , 2007, Seynnes et al. , 2007). This dissimilarity may be related to differences in the activation of these muscles depending on the speed and angle of the contraction (Blazevich et al. , 2007). Such alterations, in particular in the muscle contractile properties may act as a twitch (temporal) and summation (spatial) filtering to minimize the influence of synaptic noise, and subsequently of the discharge rate variability, on motor output (Dideriksen et al. , 2012).
Conclusion Six weeks of strength training, but not endurance training, reduces motor unit discharge rate variability of the vasti muscles and enhances force steadiness. These results provide new insights into the neuromuscular adaptations that occur with different training methods.
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Schiffman JM, Luchies CW. The effects of motion on force control abilities. Clinical biomechanics. 2001;16:505-13. Seynnes O, Hue OA, Garrandes F, Colson SS, Bernard PL, Legros P, et al. Force steadiness in the lower extremities as an independent predictor of functional performance in older women. Journal of aging and physical activity. 2005;13:395-408. Seynnes OR, de Boer M, Narici MV. Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol. 2007;102:368-73. Slifkin AB, Newell KM. Noise, information transmission, and force variability. Journal of experimental psychology Human perception and performance. 1999;25:837-51. Taylor AM, Christou EA, Enoka RM. Multiple features of motor-unit activity influence force fluctuations during isometric contractions. Journal of neurophysiology. 2003;90:1350-61. Tracy BL, Enoka RM. Older adults are less steady during submaximal isometric contractions with the knee extensor muscles. Journal of applied physiology. 2002;92:1004-12. Tracy BL, Enoka RM. Steadiness training with light loads in the knee extensors of elderly adults. Medicine and science in sports and exercise. 2006;38:735-45. Vila-Cha C, Falla D, Correia MV, Farina D. Changes in H reflex and V wave following short-term endurance and strength training. Journal of applied physiology. 2012;112:54-63. Vila-Cha C, Falla D, Farina D. Motor unit behavior during submaximal contractions following six weeks of either endurance or strength training. J Appl Physiol. 2010;109:1455-66.
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CAPTIONS TO ILLUSTRATIONS
Figure 1 - Coefficient of variation (CoV) of force measured during isometric knee extension performed at % MVC 20 (a) and 30% MVC (b), for all subjects, pre and post- training. Each line represents 1 subject. Thick black line represents the mean of the group. *- P < 0.05 from pre to post strength training.
Figure 2 - Coefficient of variation (CoV) of the motor unit interspike interval variability (ISI) of the (a) vastus medialis obliquus (VMO) and (b) vastus lateralis (VL) recorded during isometric knee extension performed at 20 and 30% MVC, for all subjects, pre and post- training. Each line represents 1 subject. Thick black line represents the mean of the group. *- P < 0.05 from pre to post strength training.
Figure 3 – Relations between the percent change in coefficient of variation (ΔCoV) for the discharge rate (ISI) of vastus medialis obliquus (VMO) and vastus lateralis (VL) motor units and ΔCoV for force recorded during isometric knee extension performed at 20 and 30% MVC, pre and post- training. Each symbol represents the ΔCoV for the ISI of the VMO (black circles) and the VL (open circles) vs ΔCoV for the force at 20% MVC (A) and at 30% MVC (B). At 20%MVC the adjusted r2 was equal to 0.510(VMO: β = 0.730; P < 0.05; VL: β = -0.220; P > 0.05) whilst at 30% MVC the adjusted r2 was equal 0.49 (VMO: β = 0.705; P < 0.05; VL: β = -0.230; P > 0.05).
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FIGURE 1
ENDURANCE
CONTROL 3,5
STRENGTH
(A) 20%MVC
Coefficient of variation of the force (%)
3,0 2,5 2,0
* 1,5 1,0 Pre 4,0
Post
Pre
Post
Pre
Post
(B) 30%MVC
3,5 3,0 2,5
*
2,0 1,5 1,0 Pre
Post
Pre
Post
Pre
Post
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FIGURE 2
ENDURANCE
CONTROL
20
STRENGTH
(A) VMO
Coefficient of variation of the ISI (%)
18 16 14 *
12 10 8 6 Pre
20 18
Post
Pre
Post
Pre
Post
(B) VL
16 14 *
12 10 8 6 Pre
Post
Pre
Post
Pre
Post
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FIGURE 3
120
120
(A) 20% MVC
80 60 40 20
VMO VL
ΔCV for the force (%)
100 Δ CV for the force (%)
(B) 30% MVC
VMO (R 2 = 0.51)
VMO (R 2 = 0.49)
100
80
60
VMO VL
0 20
40
60
80
Δ CV of the ISI (%)
100
120
50
60
70
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90
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110
120
ΔCV of the ISI (%)
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Author biography Carolina Vila-Chã received a B.Sc. and M.Sc. in Sports Science and the PhD in Biomedical Engineering from the University of Porto, Portugal. In 2007-2010, she has been a guest researcher at the Center for Sensory-Motor Interaction, Aalborg University, Denmark. Since 2012 she has been adjunct professor at Sports Department of the Polytechnic Institute of Guarda, Portugal and researcher at Research Center in Sports, Health and Human Development (CIDESD), Portugal. Her research is focused on the assessment of neuromuscular adaptations to training by means of advanced EMG techniques. Her scientific interests also include exploration of neuromuscular alterations induced by muscle fatigue, delayed muscle onset soreness and their impact on motor control. Within these areas, she has several peer-review publications journals and conference papers/abstracts.
Deborah Falla received her PhD in Physiotherapy from The University of Queensland, Australia in 2003. In 2005 she was awarded Fellowships from the International Association for the Study of Pain and the National Health and Medical Research Council of Australia to undertake postdoctoral research at the Center for Sensory-Motor Interaction, Aalborg University, Denmark. From 2007 to 2010 she was an Associate Professor at the Faculty of Medicine, Department of Health Science and Technology, Aalborg University, Denmark. Since 2012 she is a Professor at the Center for Anesthesiology, Emergency and Intensive Care Medicine and Department of Neurorehabilitation Engineering, University Hospital Göttingen, Germany. Her research focus involves the integration of neurophysiological and clinical research to evaluate neuromuscular control of the spine in people with chronic pain. Her research interests also include motor skill learning and training for musculoskeletal pain disorders. In this field she has published over 100 papers in international, peer-reviewed journals, more than 100 conference papers/abstracts including 30 invited/keynote lectures. She has received several recognitions and awards for her work. Among these she was awarded the German Pain Prize in 2014, the George J. Davies - James A. Gould Excellence in Clinical Inquiry Award in 2009 and the Delsys Prize for Electromyography Innovation in 2004. Prof. Falla is co-author of the book entitled “Whiplash, Headache and Neck Pain: Research Based Directions for Physical Therapies”, co-editor of the 4th Edition of “Grieve’s Modern Musculoskeletal Physiotherapy” and is Associate Editor of the journal Manual Therapy. Since 2014, she is vicepresident of the International Society of Electrophysiology and Kinesiology (ISEK).
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S1050-6411(15)00206-0 http://dx.doi.org/10.1016/j.jelekin.2015.10.016 JJEK 1912
To appear in:
Journal of Electromyography and Kinesiology
Received Date: Revised Date: Accepted Date:
13 July 2015 29 September 2015 27 October 2015
Please cite this article as: C. Vila-Chã, D. Falla, Strength training, but not endurance training, reduces motor unit discharge rate variability, Journal of Electromyography and Kinesiology (2015), doi: http://dx.doi.org/10.1016/ j.jelekin.2015.10.016
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
STRENGTH TRAINING, BUT NOT ENDURANCE TRAINING, REDUCES MOTOR UNIT DISCHARGE RATE VARIABILITY
Carolina Vila-Chã1,2*, Deborah Falla3 1
Research Unit for Inland Development - Polytechnic Institute of Guarda, Av. Dr. Francisco Sá Carneiro, n. 50, 6300-559, Portugal 2
Research Center in Sports Sciences, Health and Human Development (CIDESD), Quinta de Prados, 5001-801 Vila Real, Portugal.
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Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Von-Siebold-Str. 6 Göttingen, Germany
Address for correspondence: * Carolina Vila-Chã Polytechnic Institute of Guarda, Av. Dr. Francisco Sá Carneiro, n. 50, 6300-559,Portugal Tel: +351 271220135 Email: [email protected]
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STRENGTH TRAINING, BUT NOT ENDURANCE TRAINING, REDUCES MOTOR UNIT DISCHARGE RATE VARIABILITY
Carolina Vila-Chã1,2*, Deborah Falla3 1
Research Unit for Inland Development - Polytechnic Institute of Guarda, Av. Dr. Francisco Sá Carneiro, n. 50, 6300-559, Portugal 2
Research Center in Sports Sciences, Health and Human Development (CIDESD), Quinta de Prados, 5001-801 Vila Real, Portugal.
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Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Von-Siebold-Str. 6 Göttingen, Germany
Address for correspondence: * Carolina Vila-Chã Polytechnic Institute of Guarda, Av. Dr. Francisco Sá Carneiro, n. 50, 6300-559,Portugal Tel: +351 271220135 Email: [email protected]
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ABSTRACT
This study evaluates and compares the effects of strength and endurance training on motor unit discharge rate variability and force steadiness of knee extensor muscles. Thirty sedentary healthy men (age, 26.0 ± 3.8 yrs) were randomly assigned to strength training, endurance training or a control group. Conventional endurance and strength training was performed 3 days per week, over a period of 6 weeks. Maximum voluntary contraction (MVC), time to task failure (at 30% MVC), coefficient of variation (CoV) of force and of the discharges rates of motor units from the vastus medialis obliquus and vastus lateralis were determined as subjects performed 20 and 30% MVC knee extension contractions before and after training. CoV of motor unit discharges rates was significantly reduced for both muscles following strength training (P<0.001), but did not change in the endurance (P=0.875) or control groups (P=0.995). CoV of force was reduced after the strength training intervention only (P<0.01). Strength training, but not endurance training, reduces motor unit discharge rate variability and enhances force steadiness of the knee extensors. These results provide new insights into the neuromuscular adaptations that occur with different training methods.
Keywords: force steadiness, discharge rate variability; strength training, endurance training.
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INTRODUCTION During submaximal voluntary contractions, the force produced is not constant but rather force fluctuates around an average level (Enoka et al. , 2003, Laidlaw et al. , 1999, Latash, 1998, Schiffman and Luchies, 2001, Slifkin and Newell, 1999). Such variability of force affects the capacity of an individual to accurately achieve a desired force level or move their limb through an intended trajectory (Latash, 1998, Slifkin and Newell, 1999). The variability of force output is determined by several mechanisms related to motoneuron properties and the synaptic inputs that they receive, which may influence the amount of synaptic noise imposed on the membrane potential during the afterhyperpolarization trajectory (Heckman and Enoka, 2004, Moritz et al. , 2005). These mechanisms can be modulated by several conditions including training, aging and disuse (Duchateau et al. , 2006, Kernell, 2006). Such alterations would not only affect the control scheme by which motor unit activity grades the amount of muscle force exerted (recruitment and rate-coding properties), but may also change the interspike interval (ISI) variability which may further affect the extent of force fluctuations (Enoka et al. , 2003). Although several studies have shown that motor unit discharge rate variability has a significant effect on the extent of force fluctuations during isometric voluntary contractions (Enoka et al. , 2003, Laidlaw et al. , 1999, Moritz et al. , 2005), the results are not unanimous (Beck et al. , 2011). This observation suggests that the amplitude of the force fluctuations can be also influenced by mechanisms other than motor unit discharge variability such as the muscle group performing the task (Kornatz et al. , 2005, Krishnan et al. , 2011), the type of load supported by the limb (Mottram et al. , 2005), the type and intensity of the muscle contraction (Christou et al. , 2003a, Laidlaw et al. , 1999), the aging process (Tracy and Enoka, 2002) and the physical activity status of the individual (Carville et al. , 2007, Enoka et al. , 2003). Also, the degree of force steadiness can be affected by different forms of training (Hortobagyi et al. , 2001, Keen et al. , 1994).
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Studies have shown that skill training contributes to improved force steadiness of hand (Kornatz et al. , 2005) and knee extensors muscles (Christou et al. , 2003b, Hart and Tracy, 2008). Nevertheless, the effects of other forms of training on force steadiness remain unclear. For instance, Beck et al. (2011), did not observe changes in force fluctuations of the knee extensors following 8 weeks of strength training. Conversely, Kornatz et al. (2005) showed increased force steadiness following 2 weeks of isometric training with a light load but no further increase following 4 weeks of training with a higher load. Even less is known about the effects of endurance training on force steadiness. It has been shown that endurance training changes single motor unit behavior (Kernell, 2006, Vila-Cha et al. , 2010), which potentially could affect motor output variability, including force fluctuations. However, the impact of such changes on force steadiness has not been assessed. The degree of force steadiness is an important parameter since it provides meaningful information on motor coordination and movement control (Christou et al. , 2003a, Seynnes et al. , 2005). Therefore, understanding how different training programs can affect force steadiness and subsequently functional movement, it is of extreme importance. Hence, the purpose of this study was to evaluate and compare the effects of strength and endurance training on motor unit discharge rate variability and force steadiness of knee extensor muscles. We hypothesized that force steadiness would improve following both training programs, which would be accompanied by reduced motor unit discharge rate variability. The knowledge gained will help to further clarify the neuromuscular adaptations to both strength and endurance training, which is relevant for rehabilitation, exercise and sports science. METHODS This study was part of a longitudinal study on neuromuscular adaptations to training and the experimental protocol has been partially described in Vila-Chã et al. (2010). The common methodology to both studies will be briefly reported here.
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Subjects Thirty healthy men (age, mean ± SD, 26.0 ± 3.8 yrs) with no history of lower limb disorders participated in the study. None of the subjects were involved in regular strength or endurance training. All subjects gave their informed consent to the procedures of the study. The study was conducted in accordance with the Declaration of Helsinki and approved by the local ethics committee (20090032). After the first experimental session (pre-training session), the subjects were randomly assigned to one of three groups: strength training (n = 10); endurance training (n = 10); or a control group (no exercise intervention) (n = 10). One subject from the strength group and two subjects from the control group did not complete the final experimental session and were excluded from the analysis. Thus, the results are presented for 9 subjects in the strength group (age, 25.4 ± 4.2 yrs; height, 183.4 ± 6.9 cm; weight, 80.3 ± 16.3 kg), 10 subjects in the endurance group (age, 26.1 ± 2.8 yrs; height, 180.6 ± 6.2 cm; weight, 78.3 ± 14.1 kg) and 8 subjects in the control group (age, 27.0 ± 5.0 yrs; height, 175.3 ± 3.4 cm; weight, 78.0 ± 13.0 kg).
Training programs The training regimes have been described in detail previously (Vila-Cha et al. , 2010). Briefly, endurance or strength training was performed over 6 weeks including a total of 18 sessions. Load intensity was progressively increased over the training period in both programs. Endurance training was performed on a bicycle ergometer and the exercise intensity was prescribed based on the percent of the heart rate reserve (HRR) according to the Karvonen method (Karvonen et al. , 1957). The load intensity ranged between 50 to 70% of the HRR and the duration of the sessions between 20 and 50 min. The strength training included three bilateral leg exercises (leg press, leg extension, and leg curl) and a set of additional exercises for other main muscles groups of the body ( lateral
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pull down, bench press, exercises for trunk muscles) . The subjects trained with loads of 60-85% of the one-repetition maximum (1RM) and performed 3-4 sets of 8-15 repetitions. All training sessions were supervised by a training expert who continuously monitored the training programs allowing the necessary adjustments to keep the intensity at the required level.
Procedure The subjects attended two laboratory sessions, immediately before (session 1 – pre) and after completion of the 6-week training period (session 2 – post). In order to avoid an effect of the fatigue on the results, session 2 was conducted at least 48h after the last training session. For each laboratory session, the subject was comfortably seated on an Isokinetic dynamometer (KinCom Dynamometer – Chattanooga, TN, USA) with the trunk reclined to 15º in an adjustable chair and the hip and distal thigh firmly strapped to the chair. The rotational axis of the dynamometer was visually aligned with the lateral femoral epicondyle. The right leg was secured to the dynamometer’s attachment above the lateral malleolus with the knee in 90º of flexion. Progressive maximal voluntary contractions (MVC) of the knee extensors were measured twice, with 2-min rest in between. The maximum of the two force measures was used as a reference for the definition of the submaximal force levels. In both experimental sessions, the submaximal forces were relative to the MVC measured during the same session. Subjects were then asked to perform two repetitions of isometric contractions at 10, 20 and 30% MVC (random order) for 15 s whilst maintaining the force as steady as possible. Subjects were provided with online visual feedback of the force exerted which was displayed on an oscilloscope positioned 100 cm in front of the subject. After 2-min of rest, the subjects performed an isometric knee extension at 30% MVC maintaining the force for as long as possible (endurance task). Time to task failure was defined as a drop in force greater than 5% of the target force level for more than 5 s, despite strong verbal
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encouragement to the subject to maintain the target force. During all submaximal contractions, knee extension force and intramuscular electromyography (EMG) were recorded concurrently.
EMG and Force Recordings Single motor unit action potentials were recorded using two pairs of hook wire electrodes (50-µm-diameter) made of Teflon coated stainless steel (A-M Systems, Carls, WA, USA) and inserted with a 23 G needle into the vastus lateralis (VL) and vastus medialis obliquus (VMO) muscles. The electrodes were inserted distally to the innervation zone of the respective muscles, which was inspected in advance using a liner array of 8 equi-spaced silver electrodes (OT Bioelettronica, Torino, Italy), as previously described (Farina et al. , 2002, Masuda et al. , 1983). The wires were uninsulated for ~1mm at the tip. The angle of insertion of the needle was ~ 45°, and the depth was a few millimeters below the muscle fascia. The needles were removed after insertion and the wire electrodes were left inside of the muscle for the duration of the measurement session. The force produced by the knee extensor muscles during the isometric contractions was measured with a load cell incorporated in the Isokinetic dynamometer (KinCom Dynamometer – Chattanooga, TN, USA, 0.0048 V/N). Intramuscular EMG signals (bipolar derivations) were amplified (Counterpoint EMG, DANTEC Medical, Skovlunde, Denmark), band-pass filtered (500 Hz – 4 kHz), sampled at 10,000 Hz, and stored after 12-bit A/D conversion. Force signals were sampled at 10,000 Hz.
Signal analysis The recorded intramuscular signals were decomposed into the constituent motor unit action potentials by a decomposition algorithm previously validated (McGill et al. , 2005). Unusually short (<20 ms) or long (>200 ms) time intervals between subsequent detected discharges of the
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individual motor units were manually reanalyzed to check potential discrimination errors and then corrected when necessary. The mean discharge rate [pulses per second (pps)] and interspike interval variability (ISI) were computed from the motor unit spike trains. The force signals were low passfiltered (10Hz) and coefficients of variation (CoV) for the ISI and for the force signal were computed as a ratio (%) between the standard deviation and the mean values during time intervals of 10s duration. The contractions at 10% were excluded since the CoV of force at 10% MVC could not be computed in a reliable manner due to the presence of electrical noise for these low force contractions.
Statistical analysis The effects of the endurance and strength training programs on the CoV of the ISI for the VL and VMO were evaluated with four-way repeated measures analysis of variance (ANOVA) with factors group (control, endurance, and strength), training period (pre and post), load (20, 30% MVC) and muscle (VL, VMO). A three-way repeated measures ANOVA was applied to the CoV of force with factors group, training period and load. Two-way repeated measures ANOVA with factors group and training period was applied to assess changes in the MVC and time to task failure. The normality and equality of covariance matrices were tested prior to performing the repeated measures ANOVA. To investigate associations between the variables affected by training, a regression analysis was performed with the percent change (from baseline) in the CoV of the ISI for the vasti muscles as the independent variable and the percent change in force steadiness as the dependent variable. The regression analysis was performed separately for each training group. Statistical significance was designated at P < 0.05 for all comparisons. Results are reported as means and standard deviation (SD) in the text and mean and standard error (SE) in the figures.
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RESULTS Maximum Force and Time to Task Failure Strength training led to an increase of the knee extension MVC force by 17.5 ±7.5% (from 532.1 ±107.9 N to 622.7 ± 118.6 N, P < 0.05) but did not influence time to task failure (from 177.2 ± 68.2 s to 174.6 ± 63.4 s). Conversely, 6 weeks of endurance training increased the time to task failure by 29.1 ± 11.9% (from 131.0 ± 26.9 s to 160.2 ± 33.7 s, P < 0.05) but did not affect knee extension MVC force (from 531.3 ± 95.3 N to 507.7 ± 126.5 N). Motor output did not change in the control group (MVC: from 549.5 ± 68.5 N to 554.4 ± 47.2 N; time task failure: from 128.8 ± 69.1 s to 123.7 ± 73.3 s).
Force Steadiness Force steadiness of the knee extensors improved with strength training but not with endurance training (group x time: P < 0.05; Fig. 1). After six weeks of strength training the CoV of the force during the submaximal contractions decreased by 27.2±17.1% overall (P < 0.01; Fig. 1). Although a reduction in the CoV of the force occurred following endurance training, this was not significant (P = 0.11; Fig. 1). No changes were observed in the control group (P = 0.99; Fig. 1).
Figure 1 about here
Motor Unit Discharge Rate Variability Discharge rate variability was computed from a total of 1017 motor units identified from the contractions at 20 and 30% MVC in both experimental sessions (pre and post training).
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The loads used in this study did not significantly influence motor unit discharge rate variability (P = 0.33), nevertheless during the contraction at 20% MVC, vasti motor unit discharge rate variability was higher than at 30% MVC (13.1± 3.5% vs 12.4± 2.9%, respectively). The results showed that the motor unit discharge rate variability in the VMO was significantly higher than in the VL muscle (13.3 ± 3.3% vs 12.1± 3.1%; P = 0.01). No interaction between time and muscle was observed, which indicates that motor unit discharge rate variability for both muscles followed similar trends over time. A group by time interaction was observed for motor unit discharge rate variability (P < 0.001; Fig. 2). Discharge rate variability was significantly reduced for both muscles following strength training (P = 0.001; Fig. 2), but did not change in the endurance training (P = 0.875; Fig. 2) or control group (P = 0.995; Fig. 2). Figure 2 about here
Relations between Discharge Rate Variability and Force Steadiness Although motor unit discharge rate variability showed similar trends over time for both muscles, in the strength training group, only the percent change in discharge rate variability of VMO motor units was significantly associated with the percent change in CoV of force at 20% (P = 0.04; r2 =0.51, Fig. 3(A)) and 30% MVC (P = 0.02; r2 =0.49, Fig. 3(B)). There was no correlation between MVC and force steadiness at 20% MVC (P = 0.377) or 30% MVC (P = 0.190) for this group. No relation between the percent change of discharge rate variability of the vasti motor units and the percent change of CoV of force at 20 and 30% MVC were observed for the endurance group or the control group.
Figure 3 about here
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DISCUSSION This study evaluated the effect of different forms of training on motor unit discharge rate variability and force fluctuations during submaximal isometric contractions of the knee extensors. The results demonstrate that 6 weeks of strength training, but not endurance training, reduces motor unit discharge rate variability of the vasti muscles and enhances force steadiness. Only the reduction of discharge rate variability for VMO motor units was significantly correlated with the decline in the CoV of force. These alterations represent early adaptations to training, since the subjects were not involved in regular physical activity before the study.
Training and force steadiness The force fluctuations of the knee extensors during low-level submaximal contractions decreased by approximately 27% following six weeks of strength training, but did not change significantly after endurance training. Previous studies have mostly examined the influence of strength training (Hortobagyi et al. , 2001, Laidlaw et al. , 1999, Tracy and Enoka, 2006) or skill training (Christou et al. , 2003b, Hart and Tracy, 2008, Kornatz et al. , 2005) on force steadiness in older adults. Although endurance training is known to induce a number of early neuromuscular adaptations, little is known about the influence of this form of training on force steadiness. To the best of our knowledge, only the study of Cracaft et al. (1975) investigated the effect endurance-type training on motor unit discharge rate variability. This study showed that a 6-week protocol of local endurance training of the dorsiflexor muscles (three times per week of dynamic low load intensity and long duration exercise) produced a decrease in tibialis anterior motor unit discharge rate variability, however the impact of such an alteration on force steadiness was not measured
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(Cracraft, 1975). In the current study, we observed a reduction of the CoV of the force by 13% following endurance training, yet this change was not statistically significant. Moreover there was no significant change in motor unit discharge rate variability. Thus, although studies have confirmed that endurance training alters motor unit behavior and neural circuits (Kernell, 2006, Perot et al. , 1991, Vila-Cha et al. , 2010), these alterations do not seem to influence the mechanisms that control force output variability during submaximal isometric contractions. We hypothesized that, following a short period of endurance training, the negative effects of a decline in motor unit discharge rate on force steadiness, may have been compensated by an increase in the number of active motor units due to lower and clustered recruitment thresholds (Adam et al. , 1998). This reorganization may contribute to improve energy efficiency, and subsequently resistance to fatigue, without compromising the motor output. Some studies support the importance of strength training for promoting improvement in force steadiness (Christou et al. , 2003b, Hart and Tracy, 2008, Keen et al. , 1994). Nonetheless, the results are contradictory. For example, Laidlaw et al. (1999), showed that 4 weeks of resistance training of the hand muscles of older adults significantly improved maximal strength and force steadiness during isometric, concentric, and eccentric muscle actions. Conversely, Hortobágyi et al. (2001), demonstrated that 10 weeks of strength training of the knee extensors muscles of older adults, increased muscle strength and increased force steadiness during dynamic but not during isometric submaximal contractions. On the other hand, Beck et al. (2011) showed that 8 weeks of knee extensor strength training resulted in a significant increase in maximal strength of the knee extensors of young adults but force steadiness during isometric contractions at 80% MVC remained unchanged. In the current study, we observed an improvement of both knee extensor muscle strength and force steadiness during submaximal isometric contractions (20 and 30% MVC) after 6weeks of strength training yet no correlations were found between these variables. This suggests
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that for young adults, increments in muscle strength and force steadiness are likely mediated by distinct mechanisms. The differences between the results obtained in the current study and that of Beck et al. (2011), might be explained by differences in the load intensity applied in each study to evaluate force steadiness (i.e. 80% versus a maximum of 30% MVC). Although the standard deviation of force during an isometric contraction increases with the target force level, the CoV presents a nonmonotonic relation with higher values observed at lower force levels, intermediate values at intermediate forces and moderate values at forces greater than 50% MVC (Enoka et al. , 2003). Therefore, the different findings in these studies might be partly explained by the different range of load intensities used to evaluate force steadiness.
Discharge rate variability and force steadiness Motor unit recruitment and discharge rate modulation can influence force fluctuations by changing the degree of twitch fusion (Taylor et al. , 2003). Nevertheless, changes in force steadiness have been associated with alterations of motor unit discharge rate variability rather than changes of other parameters of motor unit behavior (Enoka, 1997, Kornatz et al. , 2005, Moritz et al. , 2005). Our previous studies showed that strength and endurance training programs elicit early and opposite adjustments in motor unit behavior (Vila-Cha et al. , 2010) and neural circuits (VilaCha et al. , 2012). The results confirmed that short periods of endurance training induces a decline in the motor unit discharge rate and enhances motor neuron excitability. However these alterations do not seem to influence the mechanisms that control motor unit discharge rate variability and force fluctuations. Motor unit discharge variability and force fluctuations can be modulated by common inputs to a motor unit pool which are governed by central descending pathways (Taylor et al. , 2003). Nonetheless, previous work showed that following endurance training, the enhanced motor
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unit pool excitability appears to be mediated by spinal circuits rather than by descending pathways. This may partially explain why motor unit discharge rate variability and force fluctuations remained unchanged despite early changes in recruitment and rate-coding properties of the motor unit population. Contrary to endurance training, strength training elicited a decrease of vasti motor unit discharge rate variability which was associated with an improvement of the force steadiness of the knee extensors. Previous work has shown that strength training increases motor unit discharge rates (Vila-Cha et al. , 2010) and these early adaptations can be explained by increased excitability of the motor neuron pool governed by descending pathways (Vila-Cha et al. , 2012). Although the changes in the motor unit recruitment and discharge rates may have contributed to reduced motor unit discharge variability, it is very likely that other mechanisms, such as synchronization and the common modulation of motor unit discharge rates may be involved. In the present study, a moderate association was observed between motor unit discharge rate variability and force steadiness during isometric contractions at 20 and 30%MVC, supporting the association between the extent of motor unit discharge rate variability and the degree of force steadiness. Konartz et al. (2005), also observed a weak association between fluctuations in index finger acceleration and motor unit discharge rate variability. Moreover, this relation was characterized by a parallel decline of motor unit discharge rate variability and the standard deviation of acceleration fluctuations of hand muscles in response to training. These observations are strengthened by computer modeling approaches, which show that when the discharge rate variability of a motor unit pool is manipulated, significant alterations in force steadiness occur (Moritz et al, 2005).Nonetheless such an association was only observed for the VMO muscle. This might be explained by a different time course of vasti muscle adaptations to strength training. Some studies have reported differences in the magnitude and time course of muscle architecture
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adaptations of the VL and VMO to high-intensity strength training (Blazevich et al. , 2007, Seynnes et al. , 2007). This dissimilarity may be related to differences in the activation of these muscles depending on the speed and angle of the contraction (Blazevich et al. , 2007). Such alterations, in particular in the muscle contractile properties may act as a twitch (temporal) and summation (spatial) filtering to minimize the influence of synaptic noise, and subsequently of the discharge rate variability, on motor output (Dideriksen et al. , 2012).
Conclusion Six weeks of strength training, but not endurance training, reduces motor unit discharge rate variability of the vasti muscles and enhances force steadiness. These results provide new insights into the neuromuscular adaptations that occur with different training methods.
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REFERENCES Adam A, Luca CJD, Erim Z. Hand Dominance and Motor Unit Firing Behavior. J Neurophysiol. 1998;80:1373-82. Adkins DL, Boychuk J, Remple MS, Kleim JA. Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J Appl Physiol. 2006;101:1776-82. Beck TW, Defreitas JM, Stock MS, Dillon MA. Effects of resistance training on force steadiness and common drive. Muscle & nerve. 2011;43:245-50. Blazevich AJ, Cannavan D, Coleman DR, Horne S. Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles. J Appl Physiol. 2007;103:156575. Carville SF, Perry MC, Rutherford OM, Smith IC, Newham DJ. Steadiness of quadriceps contractions in young and older adults with and without a history of falling. European journal of applied physiology. 2007;100:527-33. Christou EA, Shinohara M, Enoka RM. Fluctuations in acceleration during voluntary contractions lead to greater impairment of movement accuracy in old adults. Journal of applied physiology. 2003a;95:373-84. Christou EA, Yang Y, Rosengren KS. Taiji training improves knee extensor strength and force control in older adults. The journals of gerontology Series A, Biological sciences and medical sciences. 2003b;58:763-6. Cracraft JD. Effects of Exercise on Firing Patterns of Single Motor Units. Medicine and Science in Sports and Exercise. 1975;7:86-. Dideriksen JL, Negro F, Enoka RM, Farina D. Motor unit recruitment strategies and muscle properties determine the influence of synaptic noise on force steadiness. Journal of neurophysiology. 2012;107:3357-69. Duchateau J, Semmler JG, Enoka RM. Training adaptations in the behavior of human motor units. J Appl Physiol. 2006;101:1766-75. Enoka RM. Neural strategies in the control of muscle force. Muscle & nerve Supplement. 1997;5:S66-9. Enoka RM, Christou EA, Hunter SK, Kornatz KW, Semmler JG, Taylor AM, et al. Mechanisms that contribute to differences in motor performance between young and old adults. J Electromyogr Kinesiol. 2003;13:1-12. Farina D, Arendt-Nielsen L, Merletti R, Graven-Nielsen T. Assessment of single motor unit conduction velocity during sustained contractions of the tibialis anterior muscle with advanced spike triggered averaging. J Neurosci Methods. 2002;115:1-12.
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Hart CE, Tracy BL. Yoga as steadiness training: effects on motor variability in young adults. Journal of strength and conditioning research / National Strength & Conditioning Association. 2008;22:1659-69. Heckman CJ, Enoka RM. Physiology of the motor neuron and the motor unit In: A. E, editor. Clinical Neurophysiology of Motor Neuron Diseases Elsevier; 2004. p. 119-47. Hortobagyi T, Tunnel D, Moody J, Beam S, DeVita P. Low- or high-intensity strength training partially restores impaired quadriceps force accuracy and steadiness in aged adults. The journals of gerontology Series A, Biological sciences and medical sciences. 2001;56:B38-47. Karvonen MJ, Kentala E, Mustala O. The effects of training on heart rate; a longitudinal study. Ann Med Exp Biol Fenn. 1957;35:307-15. Keen DA, Yue GH, Enoka RM. Training-related enhancement in the control of motor output in elderly humans. Journal of applied physiology. 1994;77:2648-58. Kernell D. The motoneurone and its muscle Fibres: Oxford University Press; 2006. Kornatz KW, Christou EA, Enoka RM. Practice reduces motor unit discharge variability in a hand muscle and improves manual dexterity in old adults. Journal of applied physiology. 2005;98:207280. Krishnan C, Allen EJ, Williams GN. Effect of knee position on quadriceps muscle force steadiness and activation strategies. Muscle & nerve. 2011;43:563-73. Laidlaw DH, Kornatz KW, Keen DA, Suzuki S, Enoka RM. Strength training improves the steadiness of slow lengthening contractions performed by old adults. Journal of applied physiology. 1999;87:1786-95. Latash M. Neurophysiological Basis of Movement: Human Kinetics; 1998. Masuda T, Miyano H, Sadoyama T. The distribution of myoneural junctions in the biceps brachii investigated by surface electromyography. Electroencephalogr Clin Neurophysiol. 1983;56:597603. McGill KC, Lateva ZC, Marateb HR. EMGLAB: an interactive EMG decomposition program. J Neurosci Methods. 2005;149:121-33. Moritz CT, Barry BK, Pascoe MA, Enoka RM. Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. Journal of neurophysiology. 2005;93:2449-59. Mottram CJ, Christou EA, Meyer FG, Enoka RM. Frequency modulation of motor unit discharge has task-dependent effects on fluctuations in motor output. Journal of neurophysiology. 2005;94:2878-87. Perot C, Goubel F, Mora I. Quantification of T- and H-responses before and after a period of endurance training. Eur J Appl Physiol Occup Physiol. 1991;63:368-75.
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Schiffman JM, Luchies CW. The effects of motion on force control abilities. Clinical biomechanics. 2001;16:505-13. Seynnes O, Hue OA, Garrandes F, Colson SS, Bernard PL, Legros P, et al. Force steadiness in the lower extremities as an independent predictor of functional performance in older women. Journal of aging and physical activity. 2005;13:395-408. Seynnes OR, de Boer M, Narici MV. Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol. 2007;102:368-73. Slifkin AB, Newell KM. Noise, information transmission, and force variability. Journal of experimental psychology Human perception and performance. 1999;25:837-51. Taylor AM, Christou EA, Enoka RM. Multiple features of motor-unit activity influence force fluctuations during isometric contractions. Journal of neurophysiology. 2003;90:1350-61. Tracy BL, Enoka RM. Older adults are less steady during submaximal isometric contractions with the knee extensor muscles. Journal of applied physiology. 2002;92:1004-12. Tracy BL, Enoka RM. Steadiness training with light loads in the knee extensors of elderly adults. Medicine and science in sports and exercise. 2006;38:735-45. Vila-Cha C, Falla D, Correia MV, Farina D. Changes in H reflex and V wave following short-term endurance and strength training. Journal of applied physiology. 2012;112:54-63. Vila-Cha C, Falla D, Farina D. Motor unit behavior during submaximal contractions following six weeks of either endurance or strength training. J Appl Physiol. 2010;109:1455-66.
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CAPTIONS TO ILLUSTRATIONS
Figure 1 - Coefficient of variation (CoV) of force measured during isometric knee extension performed at % MVC 20 (a) and 30% MVC (b), for all subjects, pre and post- training. Each line represents 1 subject. Thick black line represents the mean of the group. *- P < 0.05 from pre to post strength training.
Figure 2 - Coefficient of variation (CoV) of the motor unit interspike interval variability (ISI) of the (a) vastus medialis obliquus (VMO) and (b) vastus lateralis (VL) recorded during isometric knee extension performed at 20 and 30% MVC, for all subjects, pre and post- training. Each line represents 1 subject. Thick black line represents the mean of the group. *- P < 0.05 from pre to post strength training.
Figure 3 – Relations between the percent change in coefficient of variation (ΔCoV) for the discharge rate (ISI) of vastus medialis obliquus (VMO) and vastus lateralis (VL) motor units and ΔCoV for force recorded during isometric knee extension performed at 20 and 30% MVC, pre and post- training. Each symbol represents the ΔCoV for the ISI of the VMO (black circles) and the VL (open circles) vs ΔCoV for the force at 20% MVC (A) and at 30% MVC (B). At 20%MVC the adjusted r2 was equal to 0.510(VMO: β = 0.730; P < 0.05; VL: β = -0.220; P > 0.05) whilst at 30% MVC the adjusted r2 was equal 0.49 (VMO: β = 0.705; P < 0.05; VL: β = -0.230; P > 0.05).
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FIGURE 1
ENDURANCE
CONTROL 3,5
STRENGTH
(A) 20%MVC
Coefficient of variation of the force (%)
3,0 2,5 2,0
* 1,5 1,0 Pre 4,0
Post
Pre
Post
Pre
Post
(B) 30%MVC
3,5 3,0 2,5
*
2,0 1,5 1,0 Pre
Post
Pre
Post
Pre
Post
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FIGURE 2
ENDURANCE
CONTROL
20
STRENGTH
(A) VMO
Coefficient of variation of the ISI (%)
18 16 14 *
12 10 8 6 Pre
20 18
Post
Pre
Post
Pre
Post
(B) VL
16 14 *
12 10 8 6 Pre
Post
Pre
Post
Pre
Post
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FIGURE 3
120
120
(A) 20% MVC
80 60 40 20
VMO VL
ΔCV for the force (%)
100 Δ CV for the force (%)
(B) 30% MVC
VMO (R 2 = 0.51)
VMO (R 2 = 0.49)
100
80
60
VMO VL
0 20
40
60
80
Δ CV of the ISI (%)
100
120
50
60
70
80
90
100
110
120
ΔCV of the ISI (%)
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Author biography Carolina Vila-Chã received a B.Sc. and M.Sc. in Sports Science and the PhD in Biomedical Engineering from the University of Porto, Portugal. In 2007-2010, she has been a guest researcher at the Center for Sensory-Motor Interaction, Aalborg University, Denmark. Since 2012 she has been adjunct professor at Sports Department of the Polytechnic Institute of Guarda, Portugal and researcher at Research Center in Sports, Health and Human Development (CIDESD), Portugal. Her research is focused on the assessment of neuromuscular adaptations to training by means of advanced EMG techniques. Her scientific interests also include exploration of neuromuscular alterations induced by muscle fatigue, delayed muscle onset soreness and their impact on motor control. Within these areas, she has several peer-review publications journals and conference papers/abstracts.
Deborah Falla received her PhD in Physiotherapy from The University of Queensland, Australia in 2003. In 2005 she was awarded Fellowships from the International Association for the Study of Pain and the National Health and Medical Research Council of Australia to undertake postdoctoral research at the Center for Sensory-Motor Interaction, Aalborg University, Denmark. From 2007 to 2010 she was an Associate Professor at the Faculty of Medicine, Department of Health Science and Technology, Aalborg University, Denmark. Since 2012 she is a Professor at the Center for Anesthesiology, Emergency and Intensive Care Medicine and Department of Neurorehabilitation Engineering, University Hospital Göttingen, Germany. Her research focus involves the integration of neurophysiological and clinical research to evaluate neuromuscular control of the spine in people with chronic pain. Her research interests also include motor skill learning and training for musculoskeletal pain disorders. In this field she has published over 100 papers in international, peer-reviewed journals, more than 100 conference papers/abstracts including 30 invited/keynote lectures. She has received several recognitions and awards for her work. Among these she was awarded the German Pain Prize in 2014, the George J. Davies - James A. Gould Excellence in Clinical Inquiry Award in 2009 and the Delsys Prize for Electromyography Innovation in 2004. Prof. Falla is co-author of the book entitled “Whiplash, Headache and Neck Pain: Research Based Directions for Physical Therapies”, co-editor of the 4th Edition of “Grieve’s Modern Musculoskeletal Physiotherapy” and is Associate Editor of the journal Manual Therapy. Since 2014, she is vicepresident of the International Society of Electrophysiology and Kinesiology (ISEK).
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