Unilateral arm strength training improves contralateral peak force and rate of force development

Transcription

1 DOI 1.17/s ORIGINAL ARTICLE Unilateral arm strength training improves contralateral peak force and rate of force development Michael Adamson Æ Niall MacQuaide Æ Jan Helgerud Æ Jan Hoff Æ Ole Johan Kemi Accepted: 16 April 28 Ó Springer-Verlag 28 Abstract Neural adaptation following maximal strength training improves the ability to rapidly develop force. Unilateral strength training also leads to contralateral strength improvement, due to cross-over effects. However, adaptations in the rate of force development and peak force in the contralateral untrained arm after one-arm training have not been determined. Therefore, we aimed to detect contralateral effects of unilateral maximal strength training on rate of force development and peak force. Ten adult females enrolled in a 2-month strength training program focusing of maximal mobilization of force against nearmaximal load in one arm, by attempting to move the given load as fast as possible. The other arm remained untrained. The training program did not induce any observable hypertrophy of any arms, as measured by anthropometry. Nevertheless, rate of force development improved in the trained arm during contractions against both submaximal and maximal loads by 4 6%. The untrained arm also improved rate of force development by the same magnitude. Peak force only improved during a maximal isometric M. Adamson N. MacQuaide O. J. Kemi (&) Institute of Biomedical and Life Sciences, University of Glasgow, West Medical Building, Glasgow G12 8QQ, UK o.kemi@bio.gla.ac.uk J. Helgerud J. Hoff O. J. Kemi Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, Trondheim, Norway J. Helgerud Hokksund Medical Rehabilitation Center, Hokksund, Norway J. Hoff Department of Physical Medicine and Rehabilitation, St Olavs Hospital, Trondheim, Norway contraction by 37% in the trained arm and 35% in the untrained arm. One repetition maximum improved by 79% in the trained arm and 9% in the untrained arm. Therefore, one-arm maximal strength training focusing on maximal mobilization of force increased rapid force development and one repetition maximal strength in the contralateral untrained arm. This suggests an increased central drive that also crosses over to the contralateral side. Keywords Contralateral Cross-over Neural adaptation Strength Unilateral Introduction It is generally acknowledged that adaptation to a strength or resistance training program is due to two principal, but conceptually different mechanisms; muscle hypertrophy and neural adaptation (Folland and Williams 27; Jones and Rutherford 1987). The results of effective programs are usually observed as increased one repetition maximum (1RM) or improved ability to develop force and power. While muscle hypertrophy is associated with increased cross-section of the myocyte and whole-muscle (Komi 1986; MacDougall et al. 1995; Tesch and Larson 1982), neural adaptation is not. Neural adaptation refers to changes in the nervous control of the muscle. This may include improved neural drive, activation, and control of the muscle fibers (Behm 1995; Behm and Sale 1993; Cannon and Cafarelli 1987; Duchateau et al. 26; Enoka 1997; Freund 1983; Griffin and Cafarelli 25; Hakkinen et al. 1985, 1998; Hakkinen and Komi 1986; Rich and Cafarelli 2; Semmler 22). Moreover, motor units are recruited by impulses from the central nervous system to the motor neurons. It has been

2 suggested that strength training may increase firing frequency and thereby increase the potential for force development (Van Cutsem et al. 1998), whereas electromyography studies also have suggested that more motor units may be recruited along with increased motor unit firing after programs of strength training that focus on maximal mobilization of force (Hakkinen and Komi 1986; Hakkinen et al. 1985; Komi et al. 1978; Moritani and de Vries 1979; Narici et al. 1989). However, electromyographic evidence of strength training not affecting neural adaptation also exists (Narici et al. 1996). Neural adaptation has generally been observed after strength training programs utilizing heavy loads (85 95% of 1RM) and maximal mobilization of force in the concentric phase. The rationale has been that this stresses the high-threshold motor units that activate the fast glycolytic muscle fibers (Behm and Sale 1993). This has been achieved by subjects attempting to lift heavy loads as fast as possible. However, experimental evidence also suggests that strength training loads down to 3 4% of 1RM also may induce neural adaptation (Van Cutsem et al. 1998). Since the nervous system is involved in the training adaptation, unilateral strength training may also affect the contralateral muscles, either because the neural drive is spilled-over, or because adaptation in the neuromuscular system may be accessible to the untrained side (Carroll et al. 26). However, the exact mechanisms for contralateral effects remain unknown. Nonetheless, contralateral effects in the homologous muscle have been observed after unilateral strength training (Cannon and Cafarelli 1987; Lee and Carroll 27; Moritani and de Vries 1979; Zhou 2). Improved rate of force development (RFD) in the muscle has been reported to coincide with neural adaptation after strength training with heavy loads and maximal mobilization of force (Hoff and Almasbakk 1995). However, it is not known whether the neural cross-talk may affect the RFD of the contralateral muscle. The present study was therefore designed to detect contralateral effects of a unilateral maximal strength training program on force development. The strength training sought to induce neural adaptation by maximal mobilization of force against high resistance. The hypothesis was that one-arm maximal strength training improves RFD during maximal arm tests with submaximal and maximal loads in both the trained and untrained arms. Methods Subjects Ten healthy females volunteered to this study; age 2.8 ± 2.7, height ± 4.4 cm, body mass 68.3 ± 8.3 kg, and body fat 27.1 ± 3.1%. The subjects were familiar with various forms of physical activity, but those with a history of specific arm strength training were excluded. Also, all subjects presented with dominant right arms. After being informed about the test and training protocols and possible risks of participating in the study, each subject reviewed and signed consent forms prior to enrolment. The study conformed to the Declaration of Helsinki and was approved by the ethics committee. Anthropometry Anthropometry measurements were recorded with the subjects in the anatomical position, as described previously by Durnin and Womersley (1974). Circumferences were measured at axilla, maximum circumference of the upper arm with relaxed musculus (m) biceps brachii, minimum circumference above the elbow, maximum circumference at relaxed forearm, and minimum circumference above styloid processes; all at 9 to the longitudinal axis. Skinfold thickness was recorded at m biceps brachii, m triceps brachii, posterior forearm, subscapular, and suprailiac sites in order to calculate body fat % and fat volume of the arm. The bone diameter was measured at the humeral intercondyle with a Vernier caliper, whereas a skinfold thickness recording at the elbow medial epicondyle was used to predict bone volume independent of overlying fat. Arm length was measured from acromion to minimum circumference above the styloid processes. All measurements were made with a standard anthropometry kit and a skinfold caliper (Holtain, Pembs, UK). Anthropometric data of both arms and body sides were recorded twice at each time point and averaged, and by the same person throughout the study to minimize error. Equations for calculating body fat % for women were originally established by Durnin and Womersley (1974) and Siri (1961): Body density ¼ 1:1567 :717ðlog 1 RSÞ Body fat ¼ð4:95=body density 4:5Þ1 RS is the sum of biceps, triceps, subscapular and suprailiac skinfold readings (in mm). The following arm volume calculations were made, established by Shephard et al. (1988): Total arm volume ¼ðRC 2 ÞL=62:8 Fat volume ¼ðRC=5ÞðRS=2nÞL Bone volume ¼ 3:14R 2 L Musclevolume¼Totalvolume ðfatvolumeþbonevolumeþ C 2 is the square of an individual circumference reading, L is arm length, RC is the sum of the five circumferences, RS is the sum of arm skinfold readings, n is the number of arm

3 skinfold readings, and R is average bone radius. Bone volume was calculated from humeral intercondylar diameter, corrected for overlying fat. Average arm bone radius has been reported to be 21% of corrected humeral intercondylar diameter (Shephard et al. 1988). The abovementioned procedures for recording skinfold thicknesses, circumferences, and bone diameters have been reported to be in agreement with other equations or scan-corrected methods for adult normal-weight females (Garcia et al. 25). The standard error of estimates for circumference and skinfold-based protocols has been reported to be ±3 11% (Wang et al. 2). In this study, the precision of the anthropometry measurements between duplicate recordings at each site at each time point was within the 95% confidence interval; see Results. Finally, based on muscle volume calculations, the mass of mammalian muscle can be estimated on the basis of a muscle density of 1.67 g cm 3, which appears consistent across a variety of muscles (Mendez and Keys 196). Test protocols The subjects did not perform any arm-specific or highintensity exercise, or consume any alcohol within the last 2 days before presenting to the laboratory. Food was not consumed within the last 3 h prior to the tests. Subjects warmed up voluntarily and with a specific focus on the arm exercise, by using the test and training apparatus. Prior to the test day, subjects practiced 2 4 days on the equipment to avoid confounding learning factors, and each subject also completed the test and training protocols at least once each, before the study commenced. Upper arm strength and force was measured unilaterally in both arms while the subjects lay supine on a bench and with the exercising arm supported in the extended position to allow the flexion to start from a resting position without any pre-movement tension. The arm exercise was standardized to range 1 from full arm extension at 18 by cushioned bars restricting further movement. Additional cushioned bars were used to stabilize the shoulder and trunk. From a resting position with the arm extended, the subjects performed flexion contractions with maximal intended velocity at submaximal (1, 2, 3, and 4 kg) loads and isometric contraction at 1 elbow angle [load was set to 1 kg; maximal voluntary contraction (MVC)] with a cable pulley exercise apparatus in this order, with 2 3 min of rest between each attempt. Subjects were asked to each time move the given load as fast as possible. Because of the learning period prior to the test day and to avoid any fatigue, we based our protocol on single contractions at each load. RFD and peak force were analyzed from the same contractions. Force was recorded with an integrated force and displacement transducer (Model 363-D3-5-2P1, Revere Transducers, Tustin, CA, USA) that responds linearly within a load range of 25 kg with a reproducibility error of.1%. Recordings at 2 Hz were converted to a digital format by an A/D converter and captured (MoveIt 1.64, Arntzen Engineering, Trondheim, Norway), whereby the unfiltered force signal was analyzed with custom-made software written in the Borland Delphi programming language, which measured amplitude of the change of force and the peak RFD, i.e. the maximal of the differentiated force signal. Finally, 1RM was measured separately in the same flexion exercise for both arms by increasing the load in.1.5 kg steps until the maximum was reached and the subject was unable to lift heavier loads. The results were withheld from the subjects until after the completion of the study. Maximal strength training program The subjects performed a single-arm (left, non-dominant arm) unilateral strength training program for a period of 8 weeks, consisting of three training sessions/week, five sets/session, and maximally five repetitions/set (5RM). The subjects rested for 2 3 min between each set, and 2 3 s between each repetition, to avoid substantial fatigue, which would have the potential to affect muscle activation patterns (de Ruiter et al. 27). The load was approximately 85% of the 1RM, which corresponded to 5RM; when subjects managed to perform 6RM, the load was increased by.5 kg, regardless of the set. Emphasis was on the maximum mobilization of force during the concentric part of the arm movement, i.e. the subjects were encouraged to lift the load with the highest possible velocity during the flexion. The other (right) arm remained untrained. The training sessions were conducted in the supine position to mirror the testing protocols, and all sessions were supervised by the investigators to ensure that subjects focused on maximal mobilization of force. Statistics Results are presented as means ± standard deviations (SD). The Shapiro Wilks test of normality indicated that data were normally distributed. A 2-way ANOVA test was used to investigate the differences between the pre- and post-tests, differences between the trained and untrained arms, and the interaction effects between training and time. The repeated measures general linear model ANOVA was used to investigate the differences between the pre- and post-tests and the differences between the trained and untrained arms during the submaximal 1 4 kg loads. Differences between pre- and post-tests were also analyzed with the paired samples t test and the Wilcoxon Signed Rank test; no differences occurred between the approaches. The single measures intraclass correlation coefficient was used to assess the reliability of duplicate anthropometry measurements. Significance level was set to P B.5.

4 Results Altogether, the subjects performed 85.6 ± 13.8% of the prescribed strength training over the course of 8 weeks. Hence, the observed effects came after a total of 2 ± 3 strength training sessions. The anthropometrical measurements detected no hypertrophy of the trained arm over the course of the training program, and nor in the untrained arm (Fig. 1a). The calculated muscle masses for the trained and untrained arms were 1.58 ±.22 and 1.65 ±.28 kg before the training program, respectively, whereas after the training program, the calculated muscle masses were 1.56 ±.2 and 1.63 ±.22 kg for the trained and untrained arms. No statistically significant differences occurred between arms or from pre- to post-test. The intraclass correlation coefficient for duplicate anthropometry measurements at each site at each time point was.94, P B.5. Appreciable effects of the one-arm unilateral strength training program were observed in both arms. Strength, Upper Arm Muscle Volume (L) 1RM(kg) 2. a ** b Muscle Volume 1RM * ** P.1 * P.5 P.5 Fig. 1 a Shows the muscle volumes of the trained and untrained arms before (pre-test) and after (post-test) the strength training program, as determined by anthropometry; see Methods. Muscle hypertrophy was not detected after the strength training program. b Shows one repetition maximum (1RM) of the trained and untrained arms at pretest and post-test; improved strength was detected in both arms. * and ** 2-way ANOVA within-group differences between pre-test and post-test, including confirmation by the paired samples t test. Interaction effect of the 2-way ANOVA analysis showed that 1RM increased with a greater magnitude in the trained than the untrained arm measured as 1RM, increased by 3.4 ± 1.6 kg (range kg) in absolute terms and by 79 ± 54% (range 29 2%) in relative terms in the trained arm, whereas the untrained arm improved strength by.4 ±.5 kg (range. 1.5 kg) or 9 ± 15% (range 5%), respectively (Fig. 1b). Although the mean change in the untrained arm was small, the effect reached significant level (P B.5, within group comparison of 2-way ANOVA), probably since no negative changes were observed. Although both arms increased 1RM, the magnitude of increase was significantly different between them (P B.5, interaction effect of 2-way ANOVA). An example trace of a force recording at submaximal load is presented in Fig. 2a. Peak force during submaximal loads did not increase with strength training in either of the arms, although a small general tendency toward increase was noted in both the trained and untrained arm (Fig. 2b). In contrast, the peak RFD improved consistently by 4 6% at 1 4 kg loads in the trained arm (Fig. 2c). Similarly, peak RFD increased by 3 55% in the untrained arm. Repeated measures analysis indicated that the untrained arm increased peak RFD during submaximal loads with equal magnitude as the trained arm and that there was no difference in the adaptation between the two arms. Peak force and peak RFD were also measured during an isometric maximal voluntary contraction (MVC); an example trace is shown in Fig. 3a. Peak force increased by 37% and peak RFD by 43% in the trained arm during the isometric MVC test (Fig. 3b, c). In the untrained arm, peak force and peak RFD increased by 35 and 49%, respectively. The 2-way ANOVA analysis indicated that the untrained arm increased peak force and peak RFD with equal magnitude as the trained arm, as no difference was detected in the adaptation between the two arms during the experimental period. When peak RFD was normalized to peak force during dynamic or isometric contractions, no changes occurred from pre- to post-test or between the trained and untrained arms (data not shown). Discussion It has been known for some time that a strength training program in which the focus is on dynamic exercise with few repetitions against heavy loads, but with maximal mobilization of force during contractions, is effective for improving strength and force in the trained muscles (Folland and Williams 27; Jones and Rutherford 1987). This was confirmed in the present study. The present study also demonstrated that the unilateral strength training program increased the ability to rapidly generate force the RFD, also in the contralateral untrained arm. The magnitude of

5 a 75 Force Recording at Submaximal Load 125 a Force Recording at Isometric Load 1 Force (N) 5 25 Force (N) s 1s b Peak Force (N) c Rate of Force Development (N.s -1 ) Peak Force at Submaximal Loads 1Kg 2Kg 3Kg 4Kg 1Kg 2Kg 3Kg 4Kg Peak RFD at Submaximal Loads 1Kg 2Kg 3Kg 4Kg 1Kg 2Kg 3Kg 4Kg change of peak RFD was similar between the trained and untrained arms. Improved peak RFD also permitted for increased strength (1RM) and peak force during maximal isometric contractions in the contralateral untrained arm. Contralateral effects of unilateral strength training * P.5 P.5 Peak RFD improved in the untrained arm during both dynamic and isometric measurements, whereas peak force only increased during isometric measurements. No change Fig. 2 a Shows a representative trace of force recordings during submaximal dynamic loads (4 kg). b shows the peak force during submaximal loads of the trained and untrained arms before (pre-test) and after (post-test) the strength training program, whereas c Shows the respective peak rate of force development (RFD) values. * differences between pre-test and post-test (paired samples t test). repeated measures general linear model ANOVA analysis showed that both arms increased peak RFD with similar magnitude over the range 1 4 kg Peak Force (N) Rate of Force Development (N.s -1 ) b c Peak Force at Isometric Load * ( * ) of peak force at dynamic submaximal loads in either arm probably echoes the fact that the absolute submaximal loads did not change from before to after the training period. Hence, only improved RFD may be identified during the submaximal tests. In contrast, it is conceivable that the nature of the isometric MVC test permitted for increased peak force, since the exercise task was not limited to moving a specific load, but in fact challenged peak force. The fact that no changes occurred to the ratio between RFD and peak force further suggests that they mechanistically may be related to each other and/or that only faster RFD permits peak force to increase if peak Peak RFD at Isometric Load ** * P.5 ( * )P=.1 No difference 2-way ANOVA interaction effect ** P.1 * P.5 No difference 2-way ANOVA interaction effect Fig. 3 a Shows a representative trace of force recordings during isometric loads (maximal voluntary contractions, MVC). b Shows the peak force during maximal load of the trained and untrained arms before (pre-test) and after (post-test) the strength training program, whereas, c Shows the respective peak rate of force development (RFD) values. * and ** 2-way ANOVA within-group differences between pre-test and post-test, including confirmation by the paired samples T-test. : Interaction effect of the 2-way ANOVA analysis showed that both arms increased peak force and peak RFD with similar magnitude (no difference occurred between the trained and the untrained arms)

6 force is challenged. Increased RFD and peak force during maximal loads are in line with previous results of maximal strength training for neural adaptation (Hoff et al. 1999), but contralateral improvement of RFD after unilateral strength training has not been reported previously; only increased peak force (Cannon and Cafarelli 1987). In our study, RFD surprisingly increased with similar magnitude in both the trained and untrained arms, in line with the changes in peak force. This is in contrast to previous studies reporting greater effect of unilateral training on the trained versus the untrained limb; however, only strength, power, and peak force have been measured previously (Cannon and Cafarelli 1987; Carroll et al. 26; Hakkinen et al. 1996; Taniguchi 1997; Weir et al. 1997). The reasons for why the trained and untrained arms improved with similar magnitude are unclear. Although possible, it is unlikely that systematic error, resolution, or sensitivity of the recordings would account for this, since the effects were consistent, and the recorded force uniformly showed the expected pattern of increasing levels of peak force during increasing loads. Therefore, it suggests that the cause of the improvement is of biological origin. A configuration where the dominant arm was untrained may have favored a neural discharge that also largely affected the untrained arm due to previously established neural discharge pathways. It is also conceivable that because the dominant arm was the recipient of the contralateral effects, it responded more effectively to stimuli and hence amplified the signal effect, compared to the non-dominant arm. Although this remains to be studied, neural cross-over effects have been suggested by previous reports (Carroll et al. 26; Hortobagyi 25; Lee and Carroll 27). However, it cannot be conclusively excluded that muscle, anabolic, or hormonal changes may have caused the contralateral adaptation (Carroll et al. 26), though this would be unlikely since contralateral effects have been observed only in the homologous muscles (Zhou 2), whereas muscle, anabolic, or hormonal changes would not be confined to homologous muscles. The increased 1RM in the untrained arm suggests that the cross-over effect of unilateral strength training also had a functional benefit, albeit the improved strength in the untrained arm was nine-fold smaller compared to the trained arm. However, adaptations in the same order of magnitude were not expected. An updated meta-analysis of 16 studies reported that contralateral strength improved by 7.6% of initial strength after unilateral strength training ranging from 55 1% of 1RM (Carroll et al. 26), whereas the contralateral effects of unilateral elbow flex training at 6 8 RM amounted to *25% of the effects of the trained arm (Munn et al. 25). Training the nondominant arm may have accentuated the magnitude of the adaptation of 1RM in the trained arm. It should also be noted that the 79% improved strength in the trained arm surpasses previous studies that are comparable to the present. Effects in the order of 15 3% have been reported following similar strength training programs, though the involved mass of the active muscle overall has been larger in the comparable studies (Berger 1963; Hakkinen et al. 1996; Hickson et al. 1988; Hoff and Almasbakk 1995; Hoff et al. 1999). The close control of the training sessions, continuous consistency of the relative load, and a small active muscle mass in a previously untrained arm without any history of specific training may also have contributed to near-optimal conditions for a large adaptation in the trained arm in the present study. Neural adaptation versus muscular hypertrophy The anthropometry recordings suggest that muscular hypertrophy was absent in this study, although it cannot be ruled out that a minor degree of hypertrophy occurred undetected or that a longer experimental period would have induced hypertrophy. Although the precision of our anthropometry measurements was good and a close agreement was reached to previously published results (Shephard et al. 1988) in terms of arm volumes when accounting for differences in body mass, length and fat percentage, it should however be noted that anthropometry is only an indirect measure of muscle size. In general, our anthropometry measurements and equations compare well to other studies (Garcia et al. 25). Standard errors of estimates for skinfold and circumference measurements have been recorded to range ±3 11% (Wang et al. 2), but the measurement error is less prevalent when comparing subjects serially, as compared to between-subject comparisons (Martin et al. 1992). Therefore, together with the cross-over contralateral effects, this suggests that increased RFD and peak force in the present study were mainly due to neural adaptation. Conclusion We demonstrate that a unilateral strength training program that focused on maximal mobilization of force against heavy loads associated with contralateral improvement in RFD during maximal tests with both submaximal and maximal loads. RFD increased similarly in the trained and untrained arms. Improved RFD was associated with both increased peak force during maximal isometric contractions, and maximal strength, measured by 1RM, in both arms. However, whereas RFD improved to a similar degree in the trained and untrained arms, 1RM improved nine-fold more in the trained versus the untrained arm. Acknowledgments The authors are indebted to the subjects who participated in the study.

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