Scand J Med Sci Sports 2015: ••: ••–•• doi: 10.1111/sms.12481

© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Associated decrements in rate of force development and neural drive after maximal eccentric exercise J. Farup1, S. K. Rahbek1, J. Bjerre1, F. de Paoli2, K. Vissing1 Section for Sports Science, Department of Public Health, Aarhus University, Aarhus, Denmark, 2Department of Biomedicine, Aarhus University, Aarhus, Denmark Corresponding author: Jean Farup, Section of Sport Science, Department of Public Health, Aarhus University, Dalgas Avenue 4, Aarhus DK-8000, Denmark. Tel: +45 8716 8178, Fax: +45 8715 0201; E-mail: [email protected]

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Accepted for publication 23 March 2015

The present study investigated the changes in contractile rate of force development (RFD) and the neural drive following a single bout of eccentric exercise. Twenty-four subjects performed 15 × 10 maximal isokinetic eccentric knee extensor contractions. Prior to and at 24, 48, 72, 96, and 168 h during post-exercise recovery, isometric RFD (30, 50 100, and 200 ms), normalized RFD [1/6,1/2, and 2/3 of maximal voluntary contraction (MVC)] and rate of electromyography rise (RER; 30, 50, and 75 ms) were measured. RFD decreased by 28–42% peaking at 48 h (P < 0.01–P < 0.001) and remained depressed at 168 h (P < 0.05). Normalized RFD at 2/3 of MVC decreased by

22–39% (P < 0.01), peaked at 72 h and returned to baseline at 168 h. These changes in RFD were associated with a decrease in RER at 48 h–96 h (P < 0.05–P < 0.001). Accumulated changes (area under curve) revealed a greater relative decrease in accumulated RFD at 100 ms by −2727 ± 309 (%h; P < 0.05) and 200 ms by −3035 ± 271 (%h; P < 0.001) compared with MVC, which decreased, by −1956 ± 234 (%h). In conclusion, RFD and RER are both markedly reduced following a bout of maximal eccentric exercise. This association suggests that exerciseinduced decrements in RFD can, in part, be explained decrements in neural drive.

Unaccustomed eccentric exercise is known to result in a temporary decrease in skeletal muscle function in animal (Lieber et al., 1996, 2002) as well as human models (Newham et al., 1983; Crameri et al., 2007; Paulsen et al., 2012). The extent of actual muscle damage (e.g., judged by z-line disruption) in human exercise models is much less severe than that observed in animal models (Lieber et al., 1996) or when utilizing electrical muscle activation in humans (Crameri et al., 2007). Consequently, eccentric exercise in humans has been suggested to induce muscle remodeling adaptations rather than inflicting muscle damage (Yu et al., 2003, 2004). Nonetheless, the recovery period following eccentric exercise in humans is often associated with impaired muscle performance such as increased muscle soreness (Crameri et al., 2007; Vissing et al., 2008; Gibson et al., 2009) and substantial decrements in maximal voluntary contraction force (i.e. MVC) (Vissing et al., 2008; Jackman et al., 2010; Kirby et al., 2012; Paulsen et al., 2012; Penailillo et al., 2014). Accordingly, MVC is considered a valid and reliable measure of muscle function and recovery and may even be associated with the degree of myofibrillar remodeling at the ultra-structural level following eccentric exercise (Raastad et al., 2010; Paulsen et al., 2012). However, with regard to MVC, it is important to note that this contractile feature is most often obtained

when exceeding 300 ms following contraction onset (Thorstensson et al., 1976). This is in distinct contrast to what generally occurs during several types of athletic performances, where muscle force needs to be developed in less than 250 ms (Luhtanen & Komi, 1979; Kuitunen et al., 2002). Therefore, the ability to rapidly generate force, i.e., the rate of force development (RFD) within 250 ms, likely constitute a very important outcome measure on how muscle function is influenced by maximal, potentially muscle-damaging, eccentric exercise. In accordance, RFD has been reported to decrease following eccentric exercise in the knee extensor muscles (Crameri et al., 2007; Behrens et al., 2012; Molina & Denadai, 2012; Vila-Cha et al., 2012; Penailillo et al., 2014). However, from these reports it is not entirely clear if RFD actually displays a greater decrease than MVC, as Molina and Denadai (2012) reported a smaller decrement and a faster recovery of RFD compared with MVC. In contrast, Crameri et al. (2007) reported reductions in both normalized RFD (%MVCs−1) and absolute RFD (Nms−1), with the latter displaying a numerically greater decrease than MVC, in particular for the early RFD interval (50 ms) compared with the later (100 ms). Moreover, Penailillo et al. (2014) recently reported a greater decrease in RFD compared with MVC; however, this was observed specifically at the 100 to 200 ms intervals (i.e., the late RFD

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Farup et al. intervals). Consequently, although RFD is decreased following eccentric exercise, it is unclear whether RFD is more pronouncedly decreased than MVC and if early and late RFD intervals are equally affected. Furthermore, it is yet to be described which mechanisms may underlie the decreased RFD. RFD is influenced by a number of factors, such as passive mechanical properties of the muscle-tendon complex (Bojsen-Moller et al., 2005), proportion of fast twitch fibers (Harridge et al., 1996) and output from the central nervous system (Van Cutsem et al., 1998; Aagaard et al., 2002; Aagaard, 2003). With regard to the influence of fast twitch fibers, eccentric exercise has been demonstrated to induce remodeling or damage in type II fiber in particular (Vijayan et al., 2001; Cermak et al., 2012), which consequently could lead to a substantial decrease in RFD. This fiber type-specific damage/remodeling may especially influence the later RFD intervals (e.g., 100 to 200 ms) as the rise in force in the later time-intervals is increasingly influenced by the myofiber cross-bridge kinetics (Edman & Josephson, 2007) and as the larger motor units (type II fibers) will expectedly be recruited later than the smaller motor units (type I fibers; Henneman et al., 1965). However, it has not yet been investigated if the early and later RFD time intervals are in fact differentially affected by eccentric exercise (Penailillo et al., 2014). As for the changes in the output from the central nervous system in the early phase of contraction onset, evaluated as the rate of electromyography rise (RER), this has been reported to increase following a strength training period and profoundly affect RFD (Aagaard et al., 2002; Aagaard, 2003). Accordingly, if RFD indeed displays greater decrements after maximal eccentric contractions than MVC, this may relate to a reduction in RER. This hypothesis is supported by observations of decreased voluntary muscle activation following eccentric exercise (Prasartwuth et al., 2005). Interestingly, in the recent study by Penailillo et al. (2014), no changes were observed in RER following moderate intensity eccentric exercise (eccentric cycling exercise), despite a substantial decrease in RFD. However, this may in part relate to the type of selected exercise protocol, which may be considered moderate in comparison to other protocols (Crameri et al., 2007; Raastad et al., 2010). Additionally, the limited post-exercise time course (immediately, 1 and 2 days post-exercise) may have impaired the authors ability to determine if the neural drive was affected in the entire post-exercise period required to obtain full recovery (Penailillo et al., 2014). Therefore, the aim of the present study was to investigate if maximal eccentric exercise produce greater decrements in late RFD (100 and 200 ms) compared with MVC and early RFD (30 and 50 ms) and if such decrements in RFD could be related to a decreased neural drive (i.e. RER). We hypothesized (a) that late RFD (100 and 200 ms) would be substantially reduced in the days

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following eccentric exercise and more so than both MVC and early RFD (30 and 50 ms); and (b) that the decrease in RFD would be associated with a reduction in RER. Methods Participants Twenty-four healthy young recreationally active men were included in the study (n = 24, age 23.3 ± 0.5 years, height 181.8 ± 1.3 cm, weight 75.5 ± 1.9 kg). All subjects were informed of the purpose and risks of the study and provided written informed consent in accordance with the Declaration of Helsinki and approved by The Central Denmark Region Committees on Health Research Ethics (ref no. M-20110179). Exclusion criteria were (a) participation in systematic resistance training or eccentrically dominated activities for lower extremity muscles within 6 months prior to participation, (b) a history of lower extremity musculo-skeletal injuries, (c) vegan diet; and (d) use of dietary supplements or medication that potentially could influence muscle recovery or function. All subjects were instructed to avoid any strenuous physical activity 48 h before the exercise day and throughout the testing period. Furthermore, subjects were asked to refrain from taking any type of nonsteroidal anti-inflammatory drugs or alcohol during the entire experimental protocol.

General study design The study design has been described in detail previously (Farup et al., 2014a). In brief, approximately 2 weeks prior to the exercise day, the subjects reported to the laboratory where anthropometric measurements were conducted, and the individual settings for the isokinetic dynamometer used in the exercise protocol were determined. On the day of the exercise trial, all subjects completed an eccentric exercise protocol (described below). Muscle contractile function and neuromuscular activity were determined before and during the initial 7 days of post-exercise recovery. The initial study objective was to examine the effect of whey protein supplementation during the recovery from eccentric exercise. However, as reported earlier (Farup et al., 2014a), there was no effect of supplementation on the rate of regain of MVC or serum creatine kinase during post-exercise recovery. Since no effects of supplementation were observed on any of the variables reported in the present paper, the supplementation groups were merged.

Experimental protocol On the exercise day (day 0), subjects reported to the laboratory at 07:30 h after an overnight fast. Before commencing the eccentric exercise protocol, knee extensor muscle contractile function and vastus lateralis electromyography (EMG) were assessed. Following pre tests on day 0, the subjects commenced the exercise protocol, which lasted approximately 30 min. The exercise protocol consisted of 15 × 10 repetitions of maximal isokinetic eccentric knee extensor contractions performed in an isokinetic dynamometer (Humac Norm, CSMI, Stoughton, Massachusetts, USA) comparable with previous studies (Crameri et al., 2004, 2007). Knee joint range of motion was set at 70° and contraction velocity at 30°/s to ensure standardized conditions for all subjects. Individual dynamometer settings were identical to settings during muscle contractile function testing. During exercise subjects received standard verbal and visual feedback and encouragement to ensure maximal effort during exercise. Exercise repetitions and sets were interspaced with 3- and 60-s recovery, respectively. Force and work data during exercise were recorded and saved for later offline

Eccentric exercise, neural drive, and RFD analysis. Muscle contractile function and neuromuscular activity were recorded at 24, 48, 72, 96, and 168 h in a standardized order and with the subjects remaining in a fasting condition.

Muscle contractile performance measures Subsequent to a standardized warm-up consisting of 3-min lowintensity exercise on a stationary ergometer cycle (Monark, Varberg, Sweden), the subjects were seated in an isokinetic dynamometer (Humac Norm, CSMI) as previously described (Farup et al., 2012). Isometric MVC was measured at 70° knee flexion (0° equals full extension). Subjects were allowed four attempts (although, if a subject continuously improved, additional attempts were conducted), with all contractions interspaced by 1 min of recovery. Each MVC trial lasted 2.5–3 s to ensure maximal torque was obtained. Before each trial, a verbal instruction to contract as “fast and forcefully as possible” was given. Subjects were not allowed to use a counter-movement (stretch-shortening cycle movement) before exerting a maximal knee extension. All trials were sampled at 1500 Hz. The offline analyses were performed in custom-made software (Labview 2011, National Instruments Corporation, Austin, Texas, USA). MVC was determined as the highest peak torque from the best trial and this trial was utilized for the RFD analysis as follows. RFD (Nm/s) was defined as the slope of the torque-time curve in incrementing time periods of 0–30, 0–50, 0–100, and 0–200 ms, and normalized RFD was defined as the slope at 1/6, 1/2, and 2/3 of MVC normalized to MVC (%MVCs−1) from the onset of contraction in accordance with earlier studies (Aagaard et al., 2002; Blazevich et al., 2008; Farup et al., 2014b). Normalized RFD calculations were conducted in order to determine if changes in RFD were dependent on the change in MVC or if other factors (e.g., early onset neural drive) contributed to the change in RFD (Aagaard et al., 2002). Onset was defined as the instant when the knee extensor torque exceeded baseline by 7.5 Nm (Aagaard et al., 2002).

Vastus lateralis muscle EMG Vastus lateralis was chosen as a representative muscle for m. quadriceps muscle activity based on data from previous studies (Aagaard et al., 2000, 2002). Following careful preparation of the skin (shaving and cleaning with ethanol), a pair of surface EMG electrodes (Blue sensor R-00-S/25, AMBU, Ballerup, Denmark) was placed at the thickest part of vastus lateralis muscle belly

(35 mm center-to-center interelectrode distance). The position of the EMG electrodes was carefully replicated during all testing days during post-exercise recovery to ensure identical recording positions. The electrodes were connected to a wireless probe placed on the skin, in accordance with manufacturer instructions, which preamplified and transmitted the signal in real time to a PC interface receiver (TeleMyo™ 2400T DTS, Noraxon Inc, Scottsdale, Arizona, USA). All EMG sampling were recorded online at 1500 Hz with a bandwidth of 10–500 Hz, passed through a digital first-order high-pass filter with a 10 Hz cutoff, synchronized to the force signal from the dynamometer and saved in EMG sampling software (MyoResearch XP, Noraxon Inc). During the offline analysis EMG data were filtered using a moving root-mean-square filter with a time constant of 50 ms (Robertson, 2004). From each trial, the rate of EMG rise (RER) was identified as the slope of the filtered EMG curve calculated in time periods of 0–30, 0–50, and 0–75 ms (Aagaard et al., 2002). EMG onset was initiated at 70 ms prior to muscle contraction onset to account for electromechanical delay (Aagaard et al., 2002) and 75 ms was chosen instead of 100 ms since previous research has shown a decrease in EMG amplitude following 80–100 ms (Aagaard et al., 2002).

Date presentation and statistical analysis Following check for normality of distribution and tests of equal variance, data were expressed as individual and mean changes in figures and mean ± standard error of the mean in text. RER data were log-transformed for statistical analyses and presented as individual and median changes in figures or median and range in text. To evaluate association between RFD and log-transformed RER, a Pearson product-moment correlation analysis was performed. In order to determine the overall decrease in MVC and RFD during the initial 96 h (in contrast to only examining individual time points), we generated an area under curve (AUC) measure by integrating the relative change in MVC and RFD (%) with respect to time (h). The differences in AUC were evaluated using paired t-tests. The effect of time (pre, 24, 48, 72, 96, and 168 h) on dependent variables (total work, peak eccentric torque, RFD, RER, and MVC) were assessed using a mixed-effect one-way analysis of variance with repeated measures for time, using subject as random effects. Linear comparison post-hoc analysis was used to evaluate pairwise differences within each dependent variable. MVC was used as a continuous covariate to account for potential influence of MVC on changes in RFD. Alpha level was set to ≤ 0.05. All

Fig. 1. Force characteristics and neural drive. Summary of the mean change in maximal voluntary contraction (MVC), rate of force development (RFD) (a) and rate of electromyography rise (RER) (b) at 24, 48, 72, 96, and 168 h following eccentric exercise. Data are shown as mean change (% change with pre = 0).

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Farup et al. statistical analyses were performed using Stata (Stata v 12, StataCorp LP, College Station, Texas, USA).

Results Exercise performance In general, the total work and eccentric peak torque per exercise set decreased as the number of exercise sets progressed; from set two to set 15, total work and eccentric peak torque decreased by 15.2 ± 3.2% (P < 0.01) and 11.6 ± 3.0% (P < 0.01), respectively. Rate of force development Mean relative changes in absolute RFD are shown in Fig. 1(a) and individual relative changes in absolute and normalized RFD are shown in Figs 2 and 3, respectively. Overall time effects were observed for RFD30 (P < 0.01, Fig. 2(a)) as well as for RFD50, RFD100, and RFD200 (P < 0.001, Fig. 2(b–d)). RFD30 was 2240 ± 158Nms−1 pre-exercise and decreased to 1730 ± 156, 1768 ± 160, and 1807 ± 155Nms−1 at 48, 72, and 96h, respectively (P < 0.01). RFD50 was 2230 ± 142Nms−1 pre-exercise and decreased to 1862 ± 119, 1583 ± 138, 1583 ± 122,

1716 ± 125, and 1857 ± 148Nms−1 at 24, 48, 72, 96, and 168 h, respectively (P < 0.01). RFD100 was 1745 ± 79Nms−1 pre-exercise and decreased to 1309 ± 71, 1053 ± 87, 1113 ± 73, 1317 ± 73, and 1562 ± 70Nms−1 at 24, 48, 72, 96, and 168 h, respectively (P < 0.05). RFD200 was 1171 ± 34Nms−1 preexercise and decreased to 778 ± 36, 684 ± 44, 760 ± 41, 885 ± 44, and 1064 ± 36Nms−1 at 24, 48, 72, 96, and 168 h, respectively (P < 0.01). To examine the influence of MVC on the decrease in the RFD, we used MVC as a continuous covariate in the analysis of variance model. This reduced the time effect on RFD30 (P = 0.197), however, for RFD50, RFD100, and RFD200, the time effects remained significant (P < 0.01). To further support the greater decrease in RFD compared with MVC, relative RFD (%MVCs−1) at 1/6, 1/2, and 2/3 of MVC was calculated (Fig. 3(a–c)). No changes were observed for RFD1/6MVC (P = 0.06, Fig. 3(a)). For RFD1/2MVC, we observed an overall time effect (P < 0.01), with a decrease from 472 ± 35 %MVCs−1 pre-exercise to 369 ± 45 %MVCs−1 72 h postexercise (P < 0.05, Fig. 3(b)). For RFD2/3MVC, an overall time effect was observed (P < 0.001) with decreases from 408 ± 29 %MVCs−1 pre-exercise to 291 ± 46,

Fig. 2. Changes in absolute RFD. Individual changes in rate of force development [RFD (% change with pre = 0)] changes at (a) 30, (b) 50, (c) 100, and (d) 200 ms at 24, 48, 72, 96, and 168 h following eccentric exercise. Data are shown as individual changes and mean (black bar). Overall effect of time is shown in upper left corner. Significant difference from pre-exercise are denoted by *P < 0.05, **P < 0.01, or ***P < 0.001.

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Eccentric exercise, neural drive, and RFD (P < 0.01), RER50 (P < 0.001) and RER75 (P < 0.001). RER30 decreased from 8774 [1766; 30 124] mv×s−1 to 6531 [92; 17 817], 5491 [247; 19 249], and 6207 [1509; 22 451] mv×s−1 at 48, 72, and 96 h, respectively (P < 0.05, Fig. 4(a)). RER50 decreased from 7771 [1751; 23 066] mv×s−1 to 5853 [65; 13 648], 5074 [107; 14 286], and 5646 [246; 19 244] mv×s−1 at 48, 72, and 96 h, respectively (P < 0.05, Fig. 4(b)). RER75 decreased from 6995 [1855; 19 228] mv×s−1 to 4838 [48; 9859], 4101 [600; 9135], and 5162 [720; 14 648] mv×s−1 at 48 h, 72 h, and 96 h respectively (P < 0.01, Fig. 4(c)). Significant associations were observed between RFD (30, 50, and 100 ms) and the corresponding RER (30, 50, and 75 ms) at all time points; e.g. at 48 h significant associations were observed at 30 ms (r2 = 0.46, P < 0.01), 50 ms (r2 = 0.53, P < 0.001), and 75–100 ms (r2 = 0.50, P < 0.001). Maximal voluntary contraction The mean change in MVC has been previously reported (Farup et al., 2014a). The mean relative change is shown together with RFD in Fig. 1(a) and individual relative changes are shown in Fig. 5(a). MVC decreased from 292 ± 10 Nm pre-exercise to 218 ± 9, 212 ± 10, 236 ± 10, 246 ± 11, and 269 ± 11 Nm at 24, 48, 72, 96, and 168 h, respectively (P < 0.001, Fig. 5(a)). Accumulated change and RFD and MVC

Fig. 3. Changes in normalized RFD. Individual changes in normalized rate of force development [normalized RFD (% change with pre = 0)] changes at (a) 1/6, (b) 1/2, and (c) 2/3 of MVC obtained at 24, 48, 72, 96, and 168 h following eccentric exercise. Data are shown as individual changes and mean (black bar). Overall effect of time is shown in upper left corner. Significant difference from pre-exercise are denoted by *P < 0.05, **P < 0.01, or ***P < 0.001.

243 ± 29, and 313 ± 33 %MVCs−1 at 48, 72, and 96 h post-exercise, respectively (P < 0.01, Fig. 3(c)). Rate of EMG rise During the early phase of vastus lateralis muscle contraction, the surface EMG was quantified at specific time points. Mean relative change in RER is displayed in Fig. 1(b) and individual relative changes are shown in Fig. 4. Overall time effects were observed for RER30

To compare the accumulated relative decreases in RFD30, RFD50, RFD100, RFD200, and MVC, we investigated AUC, by integrating the relative decrease with respect to time from pre-exercise to 96 h post-exercise (Fig. 5(b)). The 96 h time point was selected rather than 168 h since no data were collected at 120 and 144 h. This revealed a greater reduction in AUC (%h) for RFD100 by −2727 ± 309 (P < 0.05) and RFD200 by −3035 ± 271 (P < 0.001) compared with MVC (−1956 ± 234). Furthermore, the AUC for RFD100 and RFD200 displayed a greater reduction compared with the RFD30 AUC (−1316 ± 485, P < 0.01) and RFD50 AUC (−1861 ± 422, P < 0.01). Finally, the RFD50 AUC was lower compared with RFD30 AUC (P < 0.01). No differences were noted between RFD at 30 and 50 ms compared with MVC. Discussion In the present study, we evaluated the decrements in RFD following maximal eccentric exercise and rate of regain during the subsequent 7 days of post-exercise recovery. Furthermore, we investigated if RFD decrements were associated with decrements in neural drive. By this approach, we found (a) that late RFD intervals (i.e., in the 100–200 ms interval) were markedly impaired following eccentric exercise and that the accumulated decrease in the late RFD intervals were greater

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Fig. 4. Changes in RER. Individual changes in rate of electromyography rise [RER (% change with pre = 0)] changes at (a) 30, (b) 50, and (c) 75 at 24, 48, 72, 96, and 168 h following eccentric exercise. Data are shown as individual changes and median (black bar). Overall effect of time is shown in upper left corner. Significant difference from pre-exercise are denoted by *P < 0.05, **P < 0.01, or ***P < 0.001.

than the decrease observed in MVC as well as in RFD30 and RFD50; and (b) that the decrease in RFD was associated with an attenuation in the efferent neural drive, as quantified by RER. In relation to force generation, the eccentric exercise bout resulted in a temporary decrease in the early and in particular the late RFD intervals, which gradually returned to pre-level. However, RFD at 50, 100, and 200 ms remained depressed 7 days post-exercise (168 h). In the context of functional muscle performance, these findings may be important as the ability to

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rapidly generate muscle force (i.e. RFD), rather than the maximal force (i.e. MVC), is essential (Luhtanen & Komi, 1979; Kuitunen et al., 2002; Suetta et al., 2007). Furthermore, acute decreases in RFD may contribute to an increased risk of sustaining an injury (Zebis et al., 2011), since a lowered RFD in the knee flexor muscles has been associated with future risks for anterior cruciate ligament injuries (Zebis et al., 2011). In addition to a general decrease in RFD, our results indicate that the decrease in late RFD is greater compared with the decrease in MVC during the initial 96 h post-exercise. These results are supported by Penailillo et al. (2014) who observed a greater decrease in RFD compared with MVC specifically in the 100–200 ms interval; however, these authors did not observe a greater decrease in RFD100 and RFD200 compared with MVC. This discrepancy could be related to intensity of the eccentric exercise bout, which might have been greater in the present study (150 maximal eccentric contractions) compared with the eccentric cycling bout utilized by Penailillo et al. (2014). This speculation is supported by the somewhat lower decrease in MVC reported by these authors compared with the present study (Penailillo et al., 2014). In support of the greater decrease in RFD compared with MVC, Crameri et al. (2007) reported a substantial decrease in RFD compared with MVC, although this was primarily evident in the early (50 ms) RFD interval, in contrast to the present study. The latter discrepancy may relate to differences in testing time course as the greatest decrease in the 50 ms RFD in the latter study was observed quite early (4 and 24 h post-exercise). Despite the differences in which RFD interval displayed the greatest decrease, these results collectively suggest that RFD is severely impaired following eccentric exercise and more so than MVC. In addition to the post-exercise decrement in MVC, the accumulated decrease in RFD100 and RFD200 was also greater than the decrease in RFD30 and RFD50. The difference between the decrease in early and late RFDs may relate to the relative influence of passive stiffness in serial/lateral force transmission structures, myofiber cross-bridge kinetics and neural drive. In accordance, as hypothesized by Penailillo et al. (2014), it is possible that the late RFD is predominantly influenced by cross-bridge kinetics, rather than by stretch of passive structures (Edman & Josephson, 2007). Therefore, the late RFD may be greatly affected by the fiber type composition, as faster fiber types are associated with faster cross-bridge kinetics. In relation to the primary determinant of the late RFD, earlier studies have reported these to also be closely related to MVC (Andersen & Aagaard, 2006; Andersen et al., 2010). However, this relationship could, in part, be dictated by type II fiber content as type II fibers in young subjects often displays the largest cross-sectional area and are reported to be more responsive to strength training (in particular type IIa fibers; Folland & Williams, 2007; Farup et al., 2012). Therefore, the content and size of type

Eccentric exercise, neural drive, and RFD

Fig. 5. Changes in MVC and accumulated decrease in RFD and MVC. Individual changes in maximal voluntary contraction [MVC (% change with pre = 0)] at 24, 48, 72, 96, and 168 h following eccentric exercise (a). Data are shown as individual changes and mean (black bar). Overall effect of time is shown in upper left corner. Significant difference from pre-exercise are denoted by ***P < 0.001. Accumulated relative changes (from pre to 96 h post-exercise) in RFD at 30, 50, 100, and 200 ms as well as in MVC (b, reported in %h). Significant difference between parameters are denoted by #P < 0.05), ##P < 0.01, or ###P < 0.001.

II fibers may, in part, dictate magnitude of exerciseinduced changes in both MVC and late RFD. Interestingly, earlier reports have indicated maximal eccentric exercise to be associated with a greater susceptibility of damage to type II fibers compared with type I fibers (Vijayan et al., 2001; Cermak et al., 2012). Moreover, we have recently shown that our eccentric exercise protocol is associated with proliferation of myogenic stem cells (satellite cells) located in the type II fiber niche (Farup et al., 2014a). While the latter result does not provide direct evidence of muscle damage or remodeling, it does indicate that the demand for regeneration or remodeling following eccentric exercise is more pronounced in type II fibers. In additional support, hypertrophic signaling specifically in type II fibers following eccentric exercise has been reported (Tannerstedt et al., 2009), indicating a fiber type specific initiation of muscle protein synthesis following eccentric exercise. Collectively, our current findings favor the contention that type II fibers undergo a greater degree of remodeling following eccentric exercise (Farup et al., 2014a), and the decrements in RFD100 and RFD200 may, in part, be a functional consequence of the fiber type specific remodeling. In addition to fiber type specific remodeling, a second explanation for the greatly lowered RFD may relate to a

reduced neural drive, evaluated as rate of EMG rise (RER), which is known to exert substantial influence on RFD (Aagaard, 2003). In agreement, we observed that the decrease in RFD was accompanied by a reduction in RER at 30, 50, and 75 ms. Similar observations of a reduction in voluntary activation following eccentric exercise has previously been reported by Prasartwuth et al. (2005), which the authors related to inhibition at the motor cortex and/or spinal level. The decrements in RER at 48–96 h in the present study are temporally overlapping the observed decrements is RFD, even when accounting for the decrease in MVC. With regard to the somewhat delayed response in RER compared with RFD, it should be noted that an altered EMG–torque relationship has previously been observed during fatiguing exercise in general (Burd et al., 2012; Farup et al., 2015) as well as following eccentric exercise, in which a higher EMG is observed for a given submaximal torque (Prasartwuth et al., 2005). Thus, a somewhat linear relationship between EMG and torque, as observed under normal conditions (i.e., nonfatigued and nondamaged muscle), should not be expected. The delayed decrease in RER may partly explain why Penailillo et al. (2014) did not detect any changes in RER following eccentric exercise since the latest time point in their study was 48 h post-exercise. Also worth noticing, performance decrements (i.e., decrease in MVC) following eccentric exercise is known to be highly variable between subjects (Paulsen et al., 2012), and as indicated in our plots of individual changes in RER, this parameter may in particular be prone to variability, increasing the ability to detect a significant change. Notably, the study by Penailillo et al. (2014) was powered to detect an 8% difference in MVC; therefore, it may have been underpowered to detect a difference in RER. In conclusion, the ability to generate rapid force is markedly reduced during the post-exercise recovery from maximal eccentric muscle exercise and to a greater extent than the MVC. More specifically, late RFD displayed a greater decrease than early RFD as well as MVC. Furthermore, RFD decrements were observed to be associated with decrements in neural drive, suggesting this to partly explain the decrease in RFD. Perspectives In the present study, we show that knee extensor RFD is significantly impaired during recovery from maximal eccentric exercise. Since the decrement and rate of regain of RFD and efferent neural drive were observed to follow a very similar time course, this suggest that the two are interrelated. In addition to impaired neural drive, the greater decrease in late RFD could be speculated to be a functional consequence of the potential damage or remodeling specifically in type II fibers. However, the latter warrants more direct evidence to substantiate the speculation.

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Farup et al. In a functional context, our findings suggest that the ability to rapidly generate force (which is of paramount importance for many athletic events) will be substantially hampered by a lowered neural drive. Consequently, the damage and remodeling processes of contractile and cytoskeletal proteins are not the only factors in relation to RFD impairment following eccentric exercise. Therefore, since intense exercise affects the neuromuscular system any recovery strategies (e.g. supplementation with ergogenic aids) aimed to improve RFD should influence both the neural and the muscular components of the recovery process to be successful.

Key words: Eccentric exercise, maximal voluntary contraction force, rate of electromyography rise.

Acknowledgements We thank Arla Foods Ingredients Group P/S DK for funding the project and the participants for their effort in the project. Cuno Rasmussen is thanked for engineering assistance.

Funding The study was funded by Arla Foods Ingredients Group P/S, DK.

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