Human Movement Science 36 (2014) 58–69

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Frequency and pattern of voluntary pedalling is influenced after one week of heavy strength training M. Sardroodian, P. Madeleine, M. Voigt, E.A. Hansen ⇑ Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Denmark

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Article history:

PsycINFO classification: 2221 Keywords: Movement control Pedal force Preferred pedaling rate Voluntary motor behavior Weight training

a b s t r a c t Changes in voluntary rhythmic leg movement characteristics of freely chosen cadence (reflecting movement frequency) and tangential pedal force profile (reflecting movement pattern) were investigated during 4 weeks of (i) heavy hip extension strength training (HET, n = 9), (ii) heavy hip flexion strength training (HFT, n = 9), and (iii) no intervention (CON, n = 9). Training consisted of three 5RM–10RM sets per session, with two sessions/week. Submaximal ergometer cycling was performed before the training period (pretest) and after every week of training (test A1, A2, A3, and posttest). Strength increased by on average 25% in HET and 33% in HFT. Freely chosen cadence was only changed in HET, occurring already after 1 week of training. Thus, percentage reductions of cadence in HET at test A1, A2, A3, and posttest, with respect to the pretest value, amounted for maximally on average 17%, or 14 rpm, and were larger than the corresponding changes in CON (p = .037). Percentage increases in minimum tangential pedal force in HET at test A1, A2, A3, and posttest, with respect to the pretest value, were larger than the corresponding changes in CON (p = .024). Heavy hip flexion strength training did not cause such alterations. Ó 2014 Elsevier B.V. All rights reserved.

⇑ Corresponding author. Address: Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Fredrik Bajers Vej 7, DK-9220 Aalborg, Denmark. Tel.: +45 99 40 37 22. E-mail address: [email protected] (E.A. Hansen). http://dx.doi.org/10.1016/j.humov.2014.05.003 0167-9457/Ó 2014 Elsevier B.V. All rights reserved.

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1. Introduction Walking has often been used as an exercise model for human rhythmic movement (Dietz, Colombo, & Jensen, 1994; MacLellan, Qaderdan, Koehestanie, Duysens, & McFadyen, 2012; Zehr & Haridas, 2003). Cycling is another model (Balter & Zehr, 2007; De Marchis, Schmid, Bibbo, Bernabucci, & Conforto, 2013; Sakamoto et al., 2007) that offers a more constrained movement, plus a gearing system that allows relatively low and high cadences to be applied. It has been suggested that freely chosen cadence during submaximal cycling represents an innate voluntary rhythmic leg movement frequency, under the primary influence of spinal neural circuits referred to as central pattern generators (Hansen & Ohnstad, 2008; Hartley & Cheung, 2013). In other words, freely chosen cadence may be a good reflection of central pattern generator movement frequency output. Investigations of central pattern generator-generated voluntary rhythmic movement in healthy humans are challenged by researchers’ restricted access to the spinal cord. Furthermore, it should be emphasized for completeness that existence of human central pattern generators is difficult to conclusively prove. Indirect evidence comes from spinal cord injured individuals (Calancie et al., 1994; Dimitrijevic, Gerasimenko, & Pinter, 1998) and infants (Yang, Stephens, & Vishram, 1998). Further, analysis of motor behavior can be used to increase our understanding of how the nervous system is organized and function (Goulding, 2009). Of note is that freely chosen cadence is largely individual, with a considerable range from about 50 to 100 rpm. Moreover, the freely chosen cadence is robust to acute changes such as mechanical loading and cardiopulmonary loading (Hansen & Ohnstad, 2008; Hartley & Cheung, 2013). Finally, internal (e.g., age) and external (e.g., road gradient) factors are known to change freely chosen cadence by on average up to 10 rpm. For an overview, the reader is referred to a previously published review (Hansen & Smith, 2009). The internal organization of central pattern generators is considered to be functionally separated into two components; one responsible for rhythmic movement frequency and another responsible for rhythmic movement pattern (Dominici et al., 2011; Kriellaars, Brownstone, Noga, & Jordan, 1994; McCrea & Rybak, 2008; Perret & Cabelguen, 1980). In the present study, which addressed the voluntary rhythmic leg movement of pedalling, we considered freely chosen cycling cadence to reflect rhythmic movement frequency and tangential pedal force profile to reflect rhythmic movement pattern as it has been done recently (Hansen, Voigt, Kersting, & Madeleine, 2014). Still, it should be acknowledged that both freely chosen cycling cadence and tangential pedal force are outcomes of a complex interaction of the nervous and musculoskeletal systems that include diverse aspects as e.g., movement control and inertia. It has previously been reported that 12 weeks of heavy leg strength training, involving a combination of hip extension and hip flexion exercise, caused recreationally active individuals to reduce their freely chosen cadence by on average 8–11 rpm during submaximal cycling (Hansen, Raastad, & Hallén, 2007; Rønnestad, Hansen, & Raastad, 2012). This constitutes a substantial alteration of human voluntary rhythmic leg movement behavior, which we would like to understand better. The reduced freely chosen cadence was observed after 4 weeks of training (Rønnestad et al., 2012). It is, however, possible that the freely chosen cadence is reduced even earlier than that. Indeed, the reduction of the freely chosen cadence could be hypothesized to occur already in the very initial phase (first couple of weeks) of the strength training period, particularly if the reduction is a result of neural adaptations. Our understanding of the rhythmic leg movement behavior could be enhanced by exploring the hypothesis that, in particular, one of the exercise types of hip extension or hip flexion alters the voluntary rhythmic movement behavior. As a final point, the previous studies did not investigate effects of the heavy strength training on rhythmic movement pattern. Therefore, all this lacking knowledge was investigated in the present study to enhance our understanding. The purpose of the present study was, thus, to investigate the temporal effects of separate heavy hip extension and heavy hip flexion strength training interventions on freely chosen cadence and the tangential pedal force profile over 4 weeks.

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2. Methods 2.1. Participants A total of 27 recreationally active individuals volunteered for the study, which was approved by the ethical committee of The North Denmark Region Committee on Health Research Ethics (Approval No. N-20110025). The study conformed to the standards set by the Declaration of Helsinki. The individuals signed a written informed consent form prior to participation. They were carefully informed about the procedures of the study and the overall aim (‘‘to enlarge our knowledge about control of rhythmic leg movement’’) but at the same time kept naive to the specific purpose of the study. The latter served to avoid any particular conscious control of the performed pedalling. All individuals were well accustomed to cycling as bicycling was occasionally performed for personal transportation. None of the individuals, however, performed so much bicycling that they would be categorized recreational or competitive cyclists. Some of the individuals had previous experience with strength training. However, before the study, none of the individuals had performed any strength training during the preceding 6 months. 2.2. Experimental design The individuals were randomized into three groups. Nine individuals constituted a group that performed progressive heavy hip extension strength training (HET). Other nine individuals composed a group that performed progressive heavy hip flexion strength training (HFT). In addition, nine individuals constituted a control group (CON) that was not exposed to any training. The individuals’ characteristics at the beginning of the study are presented in Table 1. The total duration of the study was 6 weeks. During this period, the individuals completed the following: Familiarization, one repetition maximum (1RM) strength test, pretest session, three additional test sessions during a 4-week training period, posttest session, and an additional 1RM strength test (Fig. 1). Training consisted of two sessions per week that were separated by at least 1 day. Strength training and test sessions were separated by 3 ± 1 days. The last training session and the posttest session (including the last 1RM strength test) was separated by 4 ± 1 days. 2.3. Familiarization The individuals reported to the laboratory and were familiarized with all procedures including 1RM strength testing as well as ergometer cycling. Strength testing was performed using a Plamax Adjustable Pulley (Impulse Health Tech Ltd. Co., Jimo, Qingdao, Shandong Province, China) and described in detail below. Cycling was performed on an SRM cycle ergometer (Schoberer Rad Messtechnik, Jülich, Germany) mounted with two Powerforce system force pedals (Radlabor GmbH, Freiburg, Germany). The cycle ergometer was adjusted according to each participant’s preferences for seat position and distance between seat and handlebars. This resulted in knee angles of approximately 25–35° when the pedals were in the lowest positions (corresponding to a crank angle of 180°). The distance between the tip of the seat and the handlebar was approximately the same as the length of the forearm length plus 10 cm. The handlebar was approximately at the same horizontal level as the seat. Crank arm

Table 1 The participating individuals’ characteristics at the beginning of the study. Data are presented as mean ± SD, unless for gender distribution that is presented as a fraction.

HET HFT CON

Gender distribution (men/women)

Age (years)

Height (m)

Body mass (kg)

5/4 4/5 5/4

23.2 ± 3.2 22.8 ± 2.0 26.4 ± 9.9

1.80 ± 8.9 1.75 ± 9.2 1.78 ± 9.9

69.5 ± 9.5 68.7 ± 8.5 72.5 ± 13.8

HET: group performing heavy hip extension strength training; HFT: group performing heavy hip flexion strength training; CON: control group.

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Fig. 1. Overview of the study design. The total duration of the study was 6 weeks. During this period, the individuals completed the following 5 test sessions: pretest, test A1 (after one week of training), test A2 (after 2 weeks of training), test A3 (after 3 weeks of training), and posttest. Furthermore, 8 training sessions were performed (except for individuals in the control group). Prior to the first session, all individuals were familiarized with all procedures. HET: group performing heavy hip extension strength training; HFT: group performing heavy hip flexion strength training; CON: control group.

length was 170 mm. The individual settings of the cycle ergometer were noted and applied throughout the study. 2.4. Heavy strength training At the start of each training session, individuals performed 10 min warm-up at self-selected intensity on the cycle ergometer. This was followed by two to three warm-up sets with gradually increased load of the exercise that was to be performed. Both legs were trained. Training sets were alternately made with right and left legs. The exercises performed by HET and HFT are illustrated in Fig. 2. The targeted muscle groups in the present hip extension and hip flexion exercises included the gluteus maximus and the iliopsoas muscles. These muscles have an important role in the generation of pedalling (So, Ng, & Ng, 2005) and they are both single joint muscles acting across the hip joint that may be considered the leading joint during pedalling (Dounskaia, 2005). Furthermore, these muscles are reported to contribute with approximately 15% of the mechanical energy generated by the muscles during pedalling (Neptune, Kautz, & Zajac, 2000). During the first three weeks of the training period, individuals trained with 10RM sets (i.e., with a load that only barely can be lifted 10 times in a set) at the first weekly session and 6RM sets at the second weekly session. During the last week of the training period, the loads in the sets were set to 8RM and 5RM for the first and second weekly sessions, respectively. During each training session, three sets of the relevant training exercise were performed as previously practiced (Rønnestad et al., 2012) (Table 2). 2.5. Determination of maximal strength The maximal load that could be lifted in one repetition (1RM) was determined for leg extension in HET (Fig. 2A) and for leg flexion in HFT (Fig. 2B). 1RM was also determined in CON in a way that five

Fig. 2. Heavy strength training was performed two days per week for 4 weeks, with both legs. (A) HET performed hip extension training. (B) HFT performed hip flexion training.

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Table 2 Training program for the individuals who performed heavy strength training. Week 1–3

HET HFT

Week 4

1 Weekly session

2 Weekly session

1 Weekly session

2 Weekly session

3  10RM 3  10RM

3  6RM 3  6RM

3  8RM 3  8RM

3  5RM 3  5RM

individuals in this group performed leg extension and four performed leg flexion. Strength tests were always preceded by 10 min warm-up on the cycle ergometer. Following warm-up, the individuals performed a standardized protocol consisting of three sets with gradually increased load (70%, 75%, and 80% of the estimated 1RM load) and decreased number of repetitions (10, 7, and 5). The first 1RM attempt was then performed with a load approximately 5% below the estimated 1RM load. After each successful attempt, the load was increased by 2–5% until the participant failed to lift the same load for 2–3 consecutive attempts. This procedure was inspired by previous work (Walker, Peltonen, Ahtiainen, Avela, & Häkkinen, 2009). The increment on the Plamax Adjustable Pulley was 0.5 kg. Individuals rested for 1 min between each attempt. All strength tests throughout the study were conducted using the same equipment with identical positioning of the participant and monitored by the same investigator. The individuals were given verbal encouragement throughout the testing of maximal strength. 2.6. Test of rhythmic movement To test the rhythmic movement pattern and frequency during pedalling, the individuals reported to the laboratory for submaximal ergometer cycling. All test sessions were performed at the beginning of each week at the same time of the day for each participant. The latter was to avoid any influence of circadian rhythm on the results. The cycle ergometer was mounted with pedals with toe clips and the individuals wore their own sports shoes. The individuals performed 11 min of continuous ergometer cycling at 100 W (light to moderate intensity). During cycling, gear 8 and ‘‘constant watt’’ operating mode were used on the SRM cycle ergometer. This setting ensures a constant power output regardless of the cycling cadence. For the first 6 min, a freely chosen cycling cadence was applied. The individuals were encouraged to try to cycle in a preferred and relaxed way without focusing on the actual pedalling. They were for example suggested to imagine themselves cycling outside on a road. Cycling cadence was blinded to the participant. The freely chosen cadence was noted at the end of each minute and an average across 2nd to 6th min was calculated. During the 7th to 11th min of the test, individuals cycled at a target cadence of 60 rpm. During the latter, individuals were allowed visual feedback on cadence. Tangential pedal forces were sampled using the two Powerforce system force pedals mounted on the cycle ergometer. Both the ergometer and the Powerforce system force pedals were calibrated before testing and controlled after each test according to the manufacturers’ recommendations. The data sampling was performed at 2000 Hz using a 16 bit A/D converter during the last minute of each of the two cycling conditions. For sampling, a data acquisition LabVIEW-based software, IMAGO Record (part of the Powerforce system), was used. The power force system uses a trigger to generate a square wave pulse when the left crank arm passes a vertical position with the pedal in top position. This pulse was used to cut the data into single cycles of pedal force data and subsequently allowing the IMAGO software to calculate average crank cycle tangential pedal force profiles for left and right pedal, respectively. For each participant and cycling condition, a single set of selected key characteristics from the tangential pedal force profiles could then be calculated as an average of data from left and right force pedal. The five selected key characteristics consisted of maximum tangential pedal force (Fmax) and minimum tangential pedal force (Fmin) measured in N, crank angles at Fmax and at Fmin measured in degrees, as well as phase with negative tangential pedal force (Phneg) measured in degrees. Fig. 3 illustrates a data example of a tangential pedal force profile.

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2.7. Statistical analyses To test for differences between groups at pretest, one-way analysis of variance (ANOVA) was used. For each group, absolute values across the study period were compared using one-way repeated measures ANOVA. If the ANOVA reached significance level, a least significant difference (LSD) test was performed as post hoc analysis. To test for differences between CON and each of the training groups in percentage changes from baseline, two-way repeated measures ANOVA with test number as within-subject factor and group as between-subject factor were performed. Difference between CON and each of the training groups in percentage change from baseline of 1RM was compared using independent-sample t-test. A Pearson correlation coefficient was calculated for the correlation between percentage changes in 1RM strength and percentage changes in freely chosen cadence for HET. Statistics were calculated in SPSS 21.0 (SPSS Inc., Chicago, IL, USA) and Excel 2010 (Microsoft Corporation, Bellevue, WA, USA) and presented as mean ± SD, unless otherwise indicated. p < .05 was considered statistically significant. 3. Results 3.1. Pretest There were no significant differences between HET, HFT, and CON at pretest with regard to age, height, body mass, freely chosen cadence, Fmax, Fmin, crank angles at Fmax and at Fmin, as well as Phneg (p = .09–.91) (Tables 1, 3 and 4). 3.2. Maximal strength 1RM was 46.9 ± 12.5, 50.1 ± 16.5, and 47 ± 11.1 kg before the training period for HET, HFT, and CON, respectively. After the training period it was 62.2 ± 10.9, 62.5 ± 20.9, and 50.2 ± 13.3 kg for HET, HFT, and CON respectively. The percentage increases in HET and HFT were significantly larger than in CON (p = .001 and p = .003, respectively) (Fig. 4). 3.3. Voluntary rhythmic movement frequency Absolute values of freely chosen cadence for HET was influenced by test number (i.e., time) across the study period (p = .005) (Table 3). The post hoc test showed that cadence at test A1, A2, and A3 was

Fig. 3. A data example showing a tangential pedal force profile for the right pedal. Characteristics of the profile are illustrated.

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Table 3 Cadence and selected tangential pedal force profile characteristics during cycling at freely chosen cadence. Data are presented as mean ± SD.

a b c

Cadence (rpm)

Fmax (N)

HET (n = 9) Pretest Test A1 Test A2 Test A3 Posttest

79.4 ± 13.0 69.4 ± 10.6a 68.0 ± 10.7a 65.6 ± 12.0a 70.0 ± 12.1

144 ± 23 154 ± 17 154 ± 13 154 ± 16 153 ± 16

HFT (n = 9) Pretest Test A1 Test A2 Test A3 Posttest

73.7 ± 14.1 73.2 ± 13.1 68.9 ± 14.4 70.3 ± 16.6 69.2 ± 12.8

CON (n = 9) Pretest Test A1 Test A2 Test A3 Posttest

78.5 ± 5.9 79.2 ± 9.0 76.8 ± 10.7 79.7 ± 9.1 82.3 ± 9.3

Fmin (N)

Crank angle at Fmax (°)

Crank angle at Fmin (°)

Phneg (°)

51 ± 11 48 ± 11 47 ± 11 44 ± 9b 46 ± 10

92 ± 5 92 ± 6 93 ± 5 91 ± 5 93 ± 5

270 ± 19 275 ± 16 279 ± 16c 283 ± 15c 283 ± 9c

161 ± 11 162 ± 9 162 ± 9 160 ± 10 160 ± 11

158 ± 16 155 ± 16 162 ± 18 157 ± 20 157 ± 21

47 ± 12 49 ± 7 47 ± 10 47 ± 9 47 ± 6

89 ± 10 91 ± 6 92 ± 6 94 ± 10 92 ± 4

272 ± 12 279 ± 17 282 ± 9 280 ± 11 282 ± 8

162 ± 8 161 ± 7 162 ± 8 163 ± 7 162 ± 7

153 ± 13 148 ± 17 151 ± 15 151 ± 19 148 ± 20

54 ± 17 55 ± 16 53 ± 15 56 ± 15 59 ± 14

96 ± 4 94 ± 10 94 ± 4 94 ± 4 93 ± 3

269 ± 14 273 ± 17 277 ± 9 274 ± 11 274 ± 15

163 ± 6 163 ± 4 163 ± 5 165 ± 6 166 ± 4

Lower than at pretest (p = .017–.033). Higher than at pretest (p = .031). Larger than at pretest (p = .009–.025).

Table 4 Cadence and selected tangential pedal force profile characteristics during cycling at a pre-set target cadence of 60 rpm. Data are presented as mean ± SD. Cadence (rpm)

Fmax (N)

Fmin (N)

HET (n = 9) Pretest Test A1 Test A2 Test A3 Posttest

Crank angle at Fmax (°)

Crank angle at Fmin (°)

Phneg (°)

60.3 ± 0.3 60.4 ± 0.3 60.5 ± 0.4 60.6 ± 0.5 60.0 ± 0.7

158 ± 14 159 ± 12 158 ± 13 158 ± 11 159 ± 13

41 ± 8 42 ± 7 41 ± 7 42 ± 7 42 ± 6

91 ± 10 91 ± 6 93 ± 6 92 ± 5 91 ± 4

286 ± 12 284 ± 6 287 ± 9 288 ± 7 288 ± 7

156 ± 13 161 ± 7 159 ± 10 159 ± 10 158 ± 14

HFT (n = 9) Pretest Test A1 Test A2 Test A3 Posttest

60.6 ± 0.4 60.2 ± 0.3 60.3 ± 0.3 60.5 ± 0.4 60.3 ± 0.5

154 ± 20 163 ± 10 161 ± 9 162 ± 10 163 ± 11

45 ± 7 45 ± 6 44 ± 6 44 ± 6 46 ± 8

90 ± 10 91 ± 7 92 ± 7 92 ± 6 93 ± 5

276 ± 6 279 ± 9 280 ± 11 280 ± 12 285 ± 8

159 ± 8 160 ± 7 159 ± 8 161 ± 8 162 ± 7

CON (n = 9) Pretest Test A1 Test A2 Test A3 Posttest

60.4 ± 0.4 60.3 ± 0.3 60.5 ± 0.2 60.4 ± 0.3 60.3 ± 0.4

165 ± 19 165 ± 17 167 ± 11 165 ± 13 169 ± 13

46 ± 11 46 ± 12 47 ± 11 45 ± 9 48 ± 9

93 ± 5 92 ± 6 92 ± 5 91 ± 6 91 ± 5

285 ± 12 285 ± 12 285 ± 11 287 ± 10 284 ± 11

163 ± 9 164 ± 5 165 ± 6 165 ± 8 168 ± 5

lower than cadence at pretest (p = .017–.033). Cadence at posttest was not significantly different from cadence at pretest (p = .115). For comparison, absolute values of freely chosen cadence in HFT and CON remained similar across the whole study period (p = .633 and p = .422, respectively). Percentage reductions of cadence in HET at test A1, A2, A3, and posttest, with respect to the pretest value, were significantly larger than the corresponding changes in CON (p = .037) (Fig. 5). This was not the case when comparing HFT and CON (p = .563). For individuals in HET, there was no significant correlation

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Fig. 4. Percentage differences from pretest values of maximal strength for training groups (HET and HFT) and control group (CON). On repetition-maximum (1RM) increased significantly more in HET and HFT than CON (p = .001 and p = .003, respectively).

between percentage improvement of 1RM strength and percentage reduction in freely chosen cadence from test A1 to posttest (p = .253). 3.4. Rhythmic movement pattern During cycling at freely chosen cadence, absolute values of Fmin and crank angle at Fmin for HET changed significantly with test number (time) (p = .012 and p = .001, respectively) (Table 3). The post hoc test showed that Fmin at test A3 was significantly less negative (i.e., was larger) as compared to the pretest value (p = .031). Fmin at the rest of the tests was not significantly different from Fmin at pretest (p = .097–.253). Further, crank angle at Fmin at test A2, A3, and posttest was larger than the pretest value (p = .009–.025). The rest of the tangential pedal force profile characteristics in HET (Fmax, crank angle at Fmax, and Phneg) were not significantly influenced by time (p = .217–.856). The percentage increases in Fmin in HET at test A1, A2, A3 and posttest, with respect to the pretest value, were significantly different than the corresponding changes in CON (p = .024). This was not the case when comparing the percentage changes in crank angle at Fmin in HET and CON (p = .481). For both HFT and CON, there was no effect of time on tangential pedal force profile characteristics during cycling at freely chosen cadence (p = .066–.798). During cycling at the pre-set target cadence of 60 rpm, there was no effect of time on tangential pedal force profile characteristics for HET, HFT, and CON (p = .077–.930) (Table 4).

Fig. 5. Percentage differences from pretest values of cadence in training groups (HET and HFT), and control group (CON) at the following five test sessions: Pretest, test A1 (after 1 week of training), test A2 (after 2 weeks of training), test A3 (after 3 weeks of training), and posttest. ⁄HET significantly different from CON (p = .037).

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4. Discussion A novel finding of the present study was that 4 weeks of heavy hip extension strength training, rather than heavy hip flexion strength training, caused recreationally active individuals to reduce their freely chosen cadence during submaximal cycling. In addition, this reduction in voluntary rhythmic movement frequency occurred in the very early phase of the strength training period, that is, after 1 week of training. Finally, the rhythmic movement pattern was also changed in HET as reflected by a less negative Fmin after 3 weeks of training and a later occurrence of Fmin within the crank cycle after 2 weeks of training and throughout the rest of the study period. On the contrary, no significant changes were found in HFT and at fixed cycling cadence. The maximal strength in the present study increased for both HET and HFT (on average 33% and 25%, respectively). That was more than strength improvements in some of the other studies (between 12% and 22%) referred to here (Falvo, Sirevaag, Rohrbaugh, & Earhart, 2010; Hansen et al., 2007). Still, it should be mentioned that neither in the studies by Rønnestad et al. (2012) and Hansen et al. (2007), nor in the present study, was there found a correlation between strength improvement and reduction of the freely chosen cadence. Furthermore, the fact that freely chosen cadence did not decrease for HFT, despite increased strength, supports the suggestion that muscle strength in itself is apparently not a key factor influencing the choice of cadence. Hip flexors lift most of the mass of the leg in the upstroke phase. Obviously, the lift performed by the hip flexors is not complete, which is the reason why some negative effective force occurs in the upstroke phase during submaximal cycling. However, it still suggests that increased strength of the hip flexors would have a comparable potential to change the freely chosen cadence as increased strength of hip extensors. It follows that the effects of the strength training on other systems of the body than the muscular, most likely the nervous system, should be considered when attempting to explain the observed reduction of freely chosen cadence. The present study adds new knowledge on the temporal effects of heavy strength training on the freely chosen cadence. We found that heavy hip extension strength training caused recreationally individuals to choose an approximately 10–14 rpm lower cadence during submaximal cycling within the period from the second test throughout the study. Similar reductions following a combination of hip flexion and hip extension strength training has been reported for comparable individuals previously (Hansen et al., 2007; Rønnestad et al., 2012). Indeed, such a reduction constitutes a substantial change. But notably, the present reduction in cadence was observed 3 weeks earlier than what has been reported before (Rønnestad et al., 2012). And it can be argued that this fast reduction in cadence, already after 1 week of training, occurs as a result of an adaptation in the nervous system since the role of neural factors is primordial during the early phase of strength training (Gabriel, Kamen, & Frost, 2006). The question is which neural factors could explain the observed change in voluntary rhythmic movement behavior? Strength training is suggested to down-regulate Ib afferent feedback (autogenous inhibitory feedback) from the force sensitive Golgi tendon organs at a given constant load (Aagaard et al., 2000). Such a down regulation may reduce the part of the sensed effort (related to the muscle/tendon load), thereby causing subjects to choose to decrease the freely chosen pedal rate, despite the fact that this increases the force in each pedal thrust. Another, and possibly more likely, theory is that the movement frequency output of the central pattern generator is somehow reduced by the heavy strength training. During human rhythmic movement, motor coordination is most likely delegated to neural networks located in the spinal cord and termed central pattern generators (Duysens & Van de Crommert, 1998; Zehr, 2005; Zehr & Duysens, 2004). A suggested model for this control is that oscillating neural circuitry, i.e., half-centers, is resided in the lumbar spinal cord. Further, that this half-center (one half for flexor activation, one half for extensor) model suggests that discrete rhythm or pattern generating networks are responsible for producing the basic locomotor rhythm and muscle activity seen in locomotion (Zehr, 2005). Descending supraspinal drive and sensory feedback is known to assist in fine-tuning the output of the human central pattern generators, though the details of this mechanism are not known (Van de Crommert, Mulder, & Duysens, 1998; Zehr & Duysens, 2004). A reduced frequency output of the central pattern generator after heavy strength training could be caused by a reduced net excitability of the central pattern generator. It could also be caused by reduced common drive from supraspinal centers

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(De Luca & Erim, 1994) to the central pattern generator (Minassian et al., 2007). After resistance training, individual motor units are capable of producing more force, and then fewer motor neurons are required to accomplish a given physical task. Presumably, a reduction in recruitment would be reflected in diminished cortical activation (Carroll, Selvanayagam, Riek, & Semmler, 2011). Indeed, less muscle has been reported to be required to lift the same load after short-term resistance training (Ploutz, Tesch, Biro, & Dudley, 1994). Further, it has been reported previously that following 3 weeks of leg extensor resistance training, movement tasks were performed with attenuated cortical demand, which was interpreted as evidence for enhanced neural efficiency (Falvo et al., 2010). According to the suggested model by Brown (1911), the oscillating neural circuitry in form of halfcenters (one half for flexor activation and one half for extensor activation) resided in the lumbar spinal cord is responsible for producing the basic locomotor rhythm and muscle activity (Brown, 1911). Interactions within and between flexor and extensor half-centers of a given limb underlie the fine coordination of muscle activity during locomotion (Orlovsky, Deliagina, & Grillner, 1999). The reduction in the freely chosen cadence after a period of strength training for HET, while not for HFT, may suggest that the half-center for extensor activation was more susceptible in the present experiment. Furthermore, since the tangential pedal force was not influenced during cycling at the preset target cadence of 60 rpm, it may be suggested that the strength training performed by individuals in HET primarily influenced the component of the central pattern generator that is considered to be responsible for rhythmic movement frequency. In the present study, Fmin and crank angle at Fmin during cycling at freely chosen cadence were changed by the heavy strength training in HET. It could intuitively be expected that hip extension training would increase Fmax first and foremost. In fact, we propose that the observed change in the tangential pedal force profile is more a consequence of the changed cadence than a result of an altered movement pattern in itself. Indeed, it has previously been reported that the peak negative crank torque (here reflecting tangential pedal force) is getting systematically less negative and occurs later in the crank cycle as cadence is decreased from 120 rpm to 60 rpm (Neptune & Herzog, 1999). That is in line with the present results. Further, the explanation is most likely that with slower pedalling, it is easier for an individual to coordinate the pedalling movement including lifting the leg in the upstroke phase. We acknowledge that the present study did not apply assessments of brain and neuromuscular adaptation e.g., in form of brain activity or muscle activation measurements. On the other hand, such methods can now be applied in an attempt to elucidate the potential mechanisms that may be responsible for the observed significant changes in rhythmic movement. Still, we are at present greatly limited in our possibilities of investigating the influence of the central pattern generators on voluntary human rhythmic movement. And therefore, studies like the present contributes to the understanding of human voluntary rhythmic leg movement behavior. 5. Conclusion The present study showed that heavy hip extension strength training caused recreationally active individuals to reduce their freely chosen cadence by on average 10–14 rpm, corresponding to a decrease of on average 13–17%, during submaximal cycling. This reflects a substantial change in rhythmic movement frequency. Furthermore, it was shown that the reduction of the cadence occurred during the very early adaptation phase to strength training, i.e., already after 1 week. Finally, the rhythmic movement pattern was also changed by the hip extension training in a way that Fmin became less negative after 3 weeks of training and that Fmin occurred later in the crank cycle in the test performed after 2 weeks of training and throughout the rest of the study period. For comparison, heavy hip flexion strength training did not cause such changes. Acknowledgements The authors express their thanks to the participating individuals for their time and effort. The present study was supported by The Ministry of Culture Committee on Sports Research in Denmark and The Obel Family Foundation.

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References Aagaard, P., Simonsen, E., Andersen, J., Magnusson, S., Halkjaer-Kristensen, J., & Dyhre-Poulsen, P. (2000). Neural inhibition during maximal eccentric and concentric quadriceps contraction: Effects of resistance training. Journal of Applied Physiology, 89, 2249–2257. Balter, J. E., & Zehr, E. P. (2007). Neural coupling between the arms and legs during rhythmic locomotor-like cycling movement. Journal of Neurophysiology, 97, 1809–1818. Brown, T. G. (1911). The intrinsic factors in the act of progression in the mammal. Proceedings of the Royal Society of London Series B, 84, 308–319 [Containing Papers of a Biological Character]. Calancie, B., Needham-Shropshire, B., Jacobs, P., Willer, K., Zych, G., & Green, B. A. (1994). Involuntary stepping after chronic spinal cord injury. Evidence for a central rhythm generator for locomotion in man. Brain, 117, 1143–1159. Carroll, T. J., Selvanayagam, V., Riek, S., & Semmler, J. (2011). Neural adaptations to strength training: Moving beyond transcranial magnetic stimulation and reflex studies. Acta Physiologica, 202, 119–140. De Luca, C. J., & Erim, Z. (1994). Common drive of motor units in regulation of muscle force. Trends in Neurosciences, 17, 299–305. De Marchis, C., Schmid, M., Bibbo, D., Bernabucci, I., & Conforto, S. (2013). Inter-individual variability of forces and modular muscle coordination in cycling: A study on untrained subjects. Human Movement Science [Epub ahead of print]. Dietz, V., Colombo, G., & Jensen, L. (1994). Locomotor activity in spinal man. The Lancet, 344, 1260–1263. Dimitrijevic, M. R., Gerasimenko, Y., & Pinter, M. M. (1998). Evidence for a spinal central pattern generator in humans. Annals of the New York Academy of Science, 860, 360–376. Dominici, N., Ivanenko, Y. P., Cappellini, G., d’Avella, A., Mondì, V., Cicchese, M., et al (2011). Locomotor primitives in newborn babies and their development. Science, 334, 997–999. Dounskaia, N. (2005). The internal model and the leading joint hypothesis: Implications for control of multi-joint movements. Experimental Brain Research, 166, 1–16. Duysens, J., & Van de Crommert, H. W. A. A. (1998). Neural control of locomotion; part 1: The central pattern generator from cats to humans. Gait & Posture, 7, 131–141. Falvo, M. J., Sirevaag, E. J., Rohrbaugh, J. W., & Earhart, G. M. (2010). Resistance training induces supraspinal adaptations: Evidence from movement-related cortical potentials. European Journal of Applied Physiology, 109, 923–933. Gabriel, D. A., Kamen, G., & Frost, G. (2006). Neural adaptations to resistive exercise. Sports Medicine, 36, 133–149. Goulding, M. (2009). Circuits controlling vertebrate locomotion: Moving in a new direction. Nature Reviews Neuroscience, 10, 507–518. Hansen, E. A., & Smith, G. (2009). Factors affecting cadence choice during submaximal cycling and cadence influence on performance. International Journal of Sports Physiology and Performance, 4, 3–17. Hansen, E. A., & Ohnstad, A. E. (2008). Evidence for freely chosen pedalling rate during submaximal cycling to be a robust innate voluntary motor rhythm. Experimental Brain Research, 186, 365–373. Hansen, E. A., Raastad, T., & Hallén, J. (2007). Strength training reduces freely chosen pedal rate during submaximal cycling. European Journal of Applied Physiology, 101, 419–426. Hansen, E. A., Voigt, M., Kersting, U. G., & Madeleine, P. (2014). Frequency and pattern of rhythmic leg movement in humans after fatiguing exercises. Motor Control. http://dx.doi.org/10.1123/mc.2013-0044 [Epub ahead of print]. Hartley, G. L., & Cheung, S. S. (2013). Freely chosen cadence during a covert manipulation of ambient temperature. Motor Control, 17, 34–47. Kriellaars, D., Brownstone, R., Noga, B., & Jordan, L. (1994). Mechanical entrainment of fictive locomotion in the decerebrate cat. Journal of Neurophysiology, 71, 2074–2086. MacLellan, M., Qaderdan, K., Koehestanie, P., Duysens, J., & McFadyen, B. (2012). Arm movements during split-belt walking reveal predominant patterns of interlimb coupling. Human Movement Science, 32, 79–90. McCrea, D. A., & Rybak, I. A. (2008). Organization of mammalian locomotor rhythm and pattern generation. Brain Research Reviews, 57, 134–146. Minassian, K., Persy, I., Rattay, F., Pinter, M., Kern, H., & Dimitrijevic, M. (2007). Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Human Movement Science, 26, 275–295. Neptune, R., & Herzog, W. (1999). The association between negative muscle work and pedaling rate. Journal of Biomechanics, 32, 1021–1026. Neptune, R., Kautz, S., & Zajac, F. (2000). Muscle contributions to specific biomechanical functions do not change in forward versus backward pedaling. Journal of Biomechanics, 33, 155–164. Orlovsky, G. N., Deliagina, T. G., & Grillner, S. (1999). Neuronal control of locomotion: From mollusc to man. New York: Oxford University Press Inc.. Perret, C., & Cabelguen, J. (1980). Main characteristics of the hindlimb locomotor cycle in the decorticate cat with special reference to bifunctional muscles. Brain Research, 187, 333–352. Ploutz, L. L., Tesch, P. A., Biro, R. L., & Dudley, G. A. (1994). Effect of resistance training on muscle use during exercise. Journal of Applied Physiology, 76, 1675–1681. Rønnestad, B. R., Hansen, E. A., & Raastad, T. (2012). Strength training affects tendon cross-sectional area and freely chosen cadence differently in noncyclists and well-trained cyclists. The Journal of Strength & Conditioning Research, 26, 158–166. Sakamoto, M., Tazoe, T., Nakajima, T., Endoh, T., Shiozawa, S., & Komiyama, T. (2007). Voluntary changes in leg cadence modulate arm cadence during simultaneous arm and leg cycling. Experimental Brain Research, 176, 188–192. So, R. C., Ng, J. K., & Ng, G. Y. (2005). Muscle recruitment pattern in cycling: A review. Physical Therapy in Sport, 6, 89–96. Van de Crommert, H. W. A. A., Mulder, T., & Duysens, J. (1998). Neural control of locomotion: Sensory control of the central pattern generator and its relation to treadmill training. Gait & Posture, 7, 251–263. Walker, S., Peltonen, J., Ahtiainen, J. P., Avela, J., & Häkkinen, K. (2009). Neuromuscular fatigue induced by an isotonic heavyresistance loading protocol in knee extensors. Journal of Sports Sciences, 27, 1271–1279. Yang, J. F., Stephens, M. J., & Vishram, R. (1998). Infant stepping: a method to study the sensory control of human walking. Journal of Physiology, 507, 927–937.

M. Sardroodian et al. / Human Movement Science 36 (2014) 58–69

69

Zehr, E. P. (2005). Neural control of rhythmic human movement: The common core hypothesis. Exercise and Sport Sciences Reviews, 33, 54–60. Zehr, E. P., & Duysens, J. (2004). Regulation of arm and leg movement during human locomotion. The Neuroscientist, 10, 347–361. Zehr, E. P., & Haridas, C. (2003). Modulation of cutaneous reflexes in arm muscles during walking: Further evidence of similar control mechanisms for rhythmic human arm and leg movements. Experimental Brain Research, 149, 260–266.

Frequency and pattern of voluntary pedalling is influenced after one week of heavy strength training.

Changes in voluntary rhythmic leg movement characteristics of freely chosen cadence (reflecting movement frequency) and tangential pedal force profile...
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