Changes in upper body muscle activity with increasing ... - Springer Link

Eur J Appl Physiol (2009) 106:353–363 DOI 10.1007/s00421-009-1018-5

ORIGINAL ARTICLE

Changes in upper body muscle activity with increasing double poling velocities in elite cross-country skiing Stefan Josef Lindinger Æ Hans-Christer Holmberg Æ Erich Mu¨ller Æ Walter Rapp

Accepted: 12 February 2009 / Published online: 11 March 2009 Ó Springer-Verlag 2009

Abstract The purpose of this study was to investigate whether the stretch-shortening cycle (SSC) contraction is integrated in neuromuscular activation in upper body muscles during double poling in cross-country skiing. Thirteen elite skiers performed double poling roller-skiing at increasing treadmill velocities of 9, 15, 21, 27 km h-1 and their individual maximal velocity. Elbow angle, axial pole force and surface EMG in the triceps brachii, pectoralis major, latissimus dorsi and teres major muscle were recorded. Increases in peak pole force, rate of force development and elbow flexion angular velocities were identified (P \ 0.05). The mean MVC-normalized EMG amplitudes increased during the pre-activation phase before pole plant, elbow flexion and the reflex-mediated

S. J. Lindinger (&) E. Mu¨ller Department of Sport Science and Kinesiology, University of Salzburg, Salzburg, Austria e-mail: [email protected] S. J. Lindinger E. Mu¨ller Christian Doppler Laboratory ‘‘Biomechanics in Skiing’’, University of Salzburg, Salzburg, Austria H.-C. Holmberg Swedish Winter Sports Research Centre, Department of Health Sciences, ¨ stersund, Sweden Mid Sweden University, O H.-C. Holmberg Swedish Olympic Committee, Stockholm, Sweden W. Rapp Department of Sports Medicine, Medical University Clinic, University of Tu¨bingen, Tu¨bingen, Germany

phase between 30 and 120 ms after pole plant due to velocity increases (P \ 0.05). It is thus suggested that elite cross-country skiers use SSC during double poling, particularly in the triceps muscle in order to generate high forces. Keywords Nordic skiing EMG Pre-activation Stretch-shortening cycle Elbow joint Muscle stiffness

Introduction Cross-country skiing imposes extensive physiological as well as biomechanical challenges with the use of a multitude of complex skiing techniques, involving both upper and lower body. Double poling (DP), one of the most advanced techniques of the last two decades, plays a crucial role in performance in a classical race, particularly in mass start and sprint competitions (Stoeggl et al. 2006). These new events have increased demands on skiers’ abilities to create high DP velocities, something confirmed by recent studies that have demonstrated a strong relationship between the level of maximal DP velocity as well as specific upper body strength, and classical sprint performance over race distances (Stoeggl et al. 2007a, b). Additionally, it has been shown that modern high performance DP is characterized by higher pole forces that are generated during shorter ground contacts and more dynamic flexion– extension patterns in the elbow joint, altogether providing more explosive pole thrusts (Holmberg et al. 2005). Several studies have examined kinematics and kinetics (for refs see Holmberg et al. 2005), whereas only a few have investigated muscle activity during DP (Holmberg et al. 2005; Komi and Norman 1987) and other crosscountry skiing techniques (Perrey et al. 1998; Vahasoyrinki

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et al. 2008). Consequently, there is currently a lack of knowledge of neuromuscular control patterns during DP at various velocities. The current development of the DP technique motivates an examination of muscle activity patterns during the crucial pole to ground contact, hypothesizing that arm and shoulder extensor muscle actions may take place in a stretch-shortening cycle (SSC), as well as having a functional role in DP performance, as has been proven for leg extensor muscles in several other sports (Komi 2000). An effective SSC is characterized by: (1) a well-timed pre-activation of extensor muscles before ground contact; (2) a following short and fast flexion (eccentric) phase (lengthening of muscle–tendon complex); (3) an immediate transition (short delay) between stretch (eccentric) and the subsequent shortening (concentric) phase (Komi 1984; Komi and Gollhofer 1997). An SSC action involves a release of high forces caused mainly by eccentric action, favoring the storage of elastic strain energy in the muscle– tendon complex, which is partly recovered during the subsequent shortening phase and used for performance potentiation (Cavagna 1977; Komi 2000). Stretch reflexes play an important role in muscle stiffness regulation (Hoffer and Andreassen 1981) during an SSC action and can also contribute to a rapid and pronounced force generation during the touch-down phase in different locomotions (Komi 2000). The phenomenon of SSC has, at present, been demonstrated in cross-country skiing only for lower limb muscles (Komi and Norman 1987; Perrey et al. 1998). Based on measured kinematic characteristics, Smith et al. (1996) briefly discussed the possibility of muscle stretch-shortening during DP in the elbow and shoulder joint, but have not confirmed such patterns with EMG data. Compared to cross-country skiing, the use of SSC is well documented in running (Kyro¨laïnen et al. 2005; Mero and Komi 1987) and jumping (Avela et al. 2006; Gollhofer and Kyrolainen 1991) and has been shown to be highly functional in explosive movements (Gollhofer et al. 1992). However, studies of SSC in upper body muscles are rare and designed as laboratory studies analyzing simulated explosive pushing (Bober et al. 1980; Gollhofer et al. 1987) or throwing movements (Grezios et al. 2006; Newton et al. 1997). Based on current technique developments, SSC in upper limb extensor muscles may play a beneficial role in modern DP. Therefore, the present study was designed to examine the neuromuscular activity and use of SSC in arm and shoulder extensor muscles during DP on a treadmill at submaximal to maximal velocities, as this wide range of velocities should provide different possibilities for the occurrence of SSC-like upper body muscle action.

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Eur J Appl Physiol (2009) 106:353–363

Methods Subjects Thirteen elite male cross-country skiers volunteered as subjects. They were (mean ± SE) 24 ± 1 (21–29) years old, 180.9 ± 1.5 (167–187) cm tall, weighed 74.2 ± 1.2 _ 2max was 73.7 ± 0.9 (69–81) (61–79) kg and their VO -1 -1 mL kg min . All the subjects were familiar with rollerskiing on a treadmill during training as well as testing and were fully acquainted with the nature of the study before they gave their written informed consent to participate. The research techniques and experimental protocol were approved by the Ethics Committee of Umea˚ University, Umea˚, Sweden (# 03-080). Experimental conditions Combined electromyographic (EMG), kinetic and kinematic analyses of the DP technique were performed on a motor-driven treadmill (Rodby, Sodertalje, Sweden) using roller skis at four separate submaximal velocities (vsm: 9, 15, 21, 27 km h-1) and at each individual’s maximum velocity (vmax: 30.7 ± 1.1 km h-1). To exclude variations in rolling resistance, all the subjects used the same pair of roller skis (Pro-Ski C2, Sterners, Nyhammar, Sweden). DP analyses were performed at a treadmill inclination of 1° like in several previous studies (Holmberg et al. 2005; Mittelstadt et al. 1995). The individual vmax was determined using a DP incremental test until voluntary exhaustion and calculated using methods specified in Holmberg et al. (2005, 2006). Before measurements, a standardized warm-up of 10 min (60–75% of vmax) was performed by all subjects. Each measurement trial included a data recording phase including 20 complete DP cycles at each velocity. A 4-min rest period was taken between each trial to avoid fatigue. All the physiological and biomechanical tests in the study were performed on separate days over a period of 15 days. Measurements Pole force measurements All the subjects used telescopically adjustable carbon racing poles, specifically constructed for axial force measurements. Axial ground reaction forces at the right pole were recorded (2,000 Hz) by an uniaxial strain gauge load cell (Biovision, Werheim, Germany; range 0.5–50 kN, weight 15 g) embedded in a light weight (65 g) aluminium body, mounted in the carbon tube directly below the grip. The load cell was calibrated by using standard weights (5–50 kg) placed on an iron platform, mounted above the measuring unit and perpendicular to the pole’s tube during calibration. The validation


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of the system was performed by a comparison with AMTI force plate data (AMTI, Watertown, MA, USA) during 30-DP imitations with a mean absolute measurement error of 2.9%, a procedure described more in detail in Holmberg et al. (2005). Absolute and relative [% body weight (BW)] -1 peak pole force, time to peak pole force and the mean rate of force development (local force minimum after impact up to peak pole force) were analyzed. Poling time was determined from pole force data and defined as the duration of pole ground contact (Polein - Poleout). Elbow angle measurements Elbow angles were measured by flexible electrogoniometers (2,000 Hz) based on strain gauge technology with an indicated accuracy of ±2° measured over a range of ±90° and a repeatability of 1° measured over a range of 90° (Penny & Giles Controls Ltd, Cmwfelinfach, UK). Earlier studies demonstrated measurement errors from 0.04° (Piriyaprasarth et al. 2008) to maximally 2° (Rowe et al. 2001). Reliability tests were carried out with 10 subjects on two occasions performing 40 repetitive elbow flexions (110°–70°) and extensions (70°–160°) at high angular velocities of 10 rad s-1 under controlled conditions on an isokinetic device (IsoMed 2000, D&R GmbH, Hernau, Germany). Intraclass correlation coefficients (ICCs) were calculated and ranged from 0.96 (elbow flexion range of motion) to 0.99 (elbow extension angular velocity), reflecting high agreement between repeated measurements and thus high reliability for the flexible electrogoniometers used at high angular velocities. Calibration measurements were performed five times at 90° (forearm perpendicular to the upper arm) as well as at 180° (fully extended elbow). Angle values were calculated from the corresponding mean voltage data. Elbow flexion was defined as the phase from pole plant (Polein) to the elbow angle minimum (EAmin) during the poling phase and elbow extension from EAmin to the end of pole ground contact (Poleout) (Fig. 1). Elbow flexion time, range of motion and mean angular velocity (range of motion/flexion time) were calculated from each of these movement events. EMG measurements Neuromuscular activity in the triceps brachii (caput longum) (TRI), pectoralis major (PMa), latissimus dorsi (LD) and teres major (TMa) was recorded using surface EMG. Pre-gelled bipolar electrodes (AG/ AgCl discs; diameter = 10 mm; inter-electrode distance = 20 mm; Skintact, Innsbruck, Austria) were placed on the corresponding muscle belly aligned with the fiber direction, according to international standards (Hermens et al. 1999). A reference electrode was attached to the sternum. Before electrode placement, the skin surface was shaved, slightly abraded, and degreased using alcohol. Electrode–skin impedance was accepted at a level of \5 kX.

Fig. 1 Example of pole force, elbow angle, filtered (50 Hz low-pass) EMG and raw EMG (teres major) curves with the (1) marked phases of pre-activity (pre; 100-ms time window), elbow flexion (fl) and extension (ext) during pole ground contact for the calculation of the average EMG amplitudes, and (2) the defined EMG threshold (10% MVC; dashed line/arrow) for the determination of pre-activation time (muscle onset). PoleIN and PoleOUT = beginning and end of pole ground contact; EAMIN = minimum elbow angle during ground contact; PPF peak pole force

For EMG amplitude normalization, maximum voluntary isometric contraction (MVC) obtained from exercises for which all subjects had previously practiced, was performed for each muscle (Acierno et al. 1995). The MVC test for TRI was performed in a seated position with the trunk properly fixed in an upright posture. The elbow was placed and fixed on a stable support (bench) in front of the subject; this was adjusted in height so that the shoulder and elbow joints were flexed at 90°. The subjects were asked to maximally contract each muscle during arm extension against the manual resistance provided by the experimenter. For the MVCs of LD and TMa the subjects sat on a bench with hips and thighs properly fixed. The upper arm was in a neutral position (0° shoulder angle) and the elbow joint flexed to 90°. The task was to create maximal pressure against a resistance board mounted on the right hand side of the bench using retroversion in the shoulder joint. For the MVC of PMa, the subjects simulated maximal bench pressing (supine position) with proper shoulder and back resistance and a 90° elbow position. Each MVC lasted between 2 and 3 s and was performed three times with 30 s rest between each trial. All the EMG signals were amplified (differential amplifier, Biovision, Werheim, Germany), hardware band-pass filtered (10–500 Hz at 3 dB), converted to digital units (DAQ 700 A/D card -12 bit, National Instruments, USA) and sampled at 2,000 Hz. EMG data processing All EMG data were analyzed by Myoresearch software version 1.06.50 (Noraxon, Scottsdale, USA). Prior to further processing, all EMG signals were

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full-wave rectified. For the EMG pattern analysis ten subsequent pole ground contacts were averaged at each performed velocity and for each subject. A trigger was set at 1% of peak pole force and all ground contact phases were synchronized to this point. In the averaged curves, further triggers were set at Polein, Poleout and EAmin representing the turning point from elbow flexion (Polein to EAmin) to elbow extension (EAmin to Poleout) (Fig. 1). Based on these triggers the average EMG amplitudes (aEMG) for all muscles were calculated for elbow flexion (FLEX), elbow extension (EXT) and for a constant time window of 100 ms before pole plant (PRE) in order to quantify the pre-activation level. Additionally, according to Gollhofer et al. (1990) the aEMG in the TRI muscle was calculated for (1) a constant time window of 30–120 ms after pole plant, defined as reflex induced muscle activation (RIA) phase during a SSC and (2) the phase from 120 ms to the end of pole ground contact, defined as the phase of late EMG response (LER). The RIA and LER phase definitions are based on earlier findings (Allum 1975), whereby the phase directly following a muscle’s fast stretch has been defined as being characterized by a short, medium and long latency reflex component. For the determination of pre-activation time (tpre) the rectified EMG signal was 50 Hz low-pass filtered (Butterworth-2nd order) in order to create a linear envelope and the threshold for muscle onset was defined as 10% of previously recorded MVCs (Konrad 2005). The calculation of MVC values for EMG amplitude normalization was performed by using the moving-window technique (stepwise value for value; window size 250 ms) applied to the full-wave rectified EMG signals of each MVC exercise. Mean EMG values were calculated for each window and the highest one of all was used for amplitude normalization. Data collection and data analysis All data were collected at 2,000 Hz using a complete measurement system (Biovision, Werheim, Germany) consisting of an input box with eight channels connected to an A/D converter card (DAQ 700 A/D card -12 bit, National Instruments, USA) and a portable pocket PC (Compaq iPAQ H3800) to store the EMG, kinetic and kinematic data in ASCII-format. For

Fig. 2 a, b Representative elbow angle (a) and pole force (b) curves of one elite crosscountry skier across the analyzed double poling velocities (9 km h-1, vmax). Time courses are mean. Group data are presented in text

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further data analyses Myoresearch software version 1.06.50 (Noraxon, Scottsdale, USA) was used.

Statistics All data were checked for normal distribution and presented as mean values ( x) and standard errors (SE). Repeated measures ANOVA were calculated to analyze changes in all defined variables across the five different DP velocities. When global significance over time was determined, Bonferroni post hoc analysis was employed in order to determine changes across velocities. The aEMG amplitudes were compared between the flexion and extension phase and between RIA and LER phase for each velocity using Student’s t tests for paired samples. The statistical level of significance was set at P \ 0.05 for all analyses. All statistical tests were processed using SPSS 14.0 Software (SPSS Inc, Chicago, IL, USA).

Results Kinematics and kinetics Changes in elbow joint kinematics and pole force characteristics across velocities are shown in representative curves (Fig. 2a, b). Poling time gradually shortened almost threefold from 702 ± 33 ms at 9 km h-1 to 243 ± 9 ms (P \ 0.05) at vmax. Simultaneously, axial peak pole force doubled from 132 ± 11 N (18 ± 2%BW) to 269 ± 16 N (37 ± 2%BW) at vmax, while time to peak pole force shortened from 223 ± 14 down to 70 ± 4 ms, both resulting in an almost sevenfold increase in the rate of force development from 560 ± 158 to 3,826 ± 275 N s-1 at vmax (all P \ 0.05). The phase from pole plant to peak pole force was accompanied by an elbow flexion with distinct changes in all the elbow angle variables with increasing DP velocity. Elbow angle minimum, occurring around peak


pole force decreased from 74° ± 7° at 9 km h-1 to 58° ± 4° at vmax (P \ 0.05). At the same time, the elbow flexion range of motion increased from 26° ± 4° to 45° ± 5°, while elbow flexion time gradually shortened from 229 ± 16 to 131 ± 28 ms at 21 km h-1, and further down to 93 ± 4 ms at vmax (both P \ 0.05). Consequently, flexion angular velocity increased about fourfold from 2.0 ± 0.5 up to 8.4 ± 0.7 rad s-1 (P \ 0.05). Muscle pre-activity Pre-activation times (tpre) for arm and shoulder muscles are shown in Fig. 3a, d. The arm extensor muscle TRI showed increases in tpre from the lowest to the highest velocities (P \ 0.05) with the longest maximal tpre of all muscles, with 244 ± 20 ms occurring at vmax. PMa demonstrated a gradual increase in tpre through 27 km h-1 (all P \ 0.05) up to 175 ± 24 ms at vmax. At the lowest velocity this muscle showed a negative tpre and a muscle onset ([10% MVC) after pole plant, respectively. LD increased tpre from the first two to the last three velocities and from 21 km h-1 to vmax (all P \ 0.05), with the shortest maximal tpre of all muscles at 137 ± 21 ms. For TMa increases of tpre from 9 km h-1 to all higher velocities and from 15 km h-1 to vmax (all P \ 0.05) were observed up to 173 ± 27 ms at vmax. The muscle pre-activity patterns of TRI, PMa and LD demonstrated increases of aEMG from the lowest up to the highest velocities (all P \ 0.05) with activation maxima of 36 ± 5, 56 ± 6, and 61 ± 10%MVC, respectively (Figs. 4, 5, 6). TMa showed the highest pre-activation of all muscles with 89 ± 26% MVC at vmax, but significant increases in aEMG (all P \ 0.05) were observed only during the first three velocities (Fig. 7).

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Muscle activity during pole ground contact The elbow flexion phase, occurring simultaneous to pole force increase up to peak force (Fig. 1), was characterized by the greatest increases (all P \ 0.05) of aEMG in all muscles (three- to four-fold) due to increasing DP velocities (Figs. 4, 5, 6, 7). During this phase the maximum TRI activity reached 73 ± 7% MVC and occurred at vmax, whereas the activities of PMa, LD and TMa even exceeded MVC activation at velocities over 15 and 21 km h-1, respectively. The aEMG maxima ranged from 114 ± 11% MVC for PMa to 177 ± 47% MVC for TMa. The muscle activity patterns during the subsequent elbow extension phase demonstrated only trends of increase in aEMG across the velocities, except for LD and TMa from 9 to 15 and 21 km h-1 (all P \ 0.05), respectively (Figs. 4, 5, 6, 7). On analyzing the differences in aEMG between the flexion and extension phase separately for each velocity, for TRI, we found a shift from slight (non-significant) increases at 9 and 15 km h-1 to cumulative decreases (-11 to -25%MVC) at the higher velocities (all P \ 0.05) (Fig. 4). All the other muscles showed similar patterns with slight increases or decreases in aEMG at lower velocities and with cumulative but even greater decreases (all P \ 0.05) in muscle activity across the three highest velocities, with -32 to -71% MVC for LD, -59 to -80% MVC for PMa and -47 to -110% MVC for TMa (Figs. 5, 6, 7). The aEMG in TRI during the RIA phase increased almost threefold from 27 ± 4% MVC at 9 km h-1 up to 81 ± 8% MVC at vmax (all P \ 0.05) (Fig. 8). Compared to the RIA phase, the aEMG in the LER phase started to decrease at velocities higher than 21 km h-1 (all P \ 0.05), with the greatest reduction of TRI muscle activity at vmax.

Fig. 3 a–d Changes in preactivity times for (a) TRI (triceps brachii), (b) PMa (pectoralis major), (c) LD (latissimus dorsi) and (d) TMa (teres major) across double poling velocities (9 km h-1, vmax). The data are mean ? SE. *P \ 0.05

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Fig. 4 Changes in TRI (triceps brachii) pre-activation (PRE), and activation during flexion (FLEX) and extension phase (EXT) across double poling velocities (9 km h-1, vmax). The data are mean ? SE. *P \ 0.05. The solid arrows indicate significant changes and the dashed arrows nonsignificant changes (P \ 0.05) from the FLEX to EXT phases separately for each velocity

Fig. 5 Changes in PMa (pectoralis major) pre-activation (PRE), and activation during flexion (FLEX) and extension phases (EXT) across double poling velocities (9 km h-1, vmax). The data are mean ? SE. *P \ 0.05. The solid arrows indicate significant changes (P \ 0.05) from the FLEX to EXT phases separately for each velocity

Fig. 6 Changes in LD (latissimus dorsi) pre-activation (PRE), and activation during flexion (FLEX) and extension phases (EXT) across double poling velocities (9 km h-1, vmax). The data are mean ? SE. *P \ 0.05. The solid arrows indicate significant changes (P \ 0.05) from the FLEX to EXT phases separately for each velocity

Discussion The main findings of the study were: (1) A stretch-shortening cycle during DP occurred in the elbow joint, adapting to higher velocities through faster elbow flexion and a decreasing delay (more immediate transition) between flexion and extension phase; (2) Peak pole force, occurring around the elbow angle minimum, and the rate of

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force production increased two- and seven-fold, respectively, although the poling time decreased; (3) Muscle preactivation times and EMG levels in the triceps brachii, pectoralis major, latissimus dorsi and teres major increased across velocities; (4) Muscular activation during the flexion phase showed the greatest increases, even exceeding MVC activity in shoulder muscles at the higher velocities. (5) During the extension phase muscle activity showed only


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Fig. 7 Changes in TMa (teres major) pre-activation (PRE), and activation during flexion (FLEX) and extension phases (EXT) across double poling velocities (9 km h-1, vmax). The data are mean ? SE. *P \ 0.05. The solid arrows indicate significant changes and the dashed arrows nonsignificant changes (P \ 0.05) from the FLEX to EXT phases separately for each velocity

Fig. 8 Changes in TRI (triceps brachii) activation during RIA (reflex induced muscle activation) and LER (late EMG response) phases across double poling velocities (9 km h-1, vmax) and differences between RIA and LER phase activation at each velocity. The data are mean ? SE. *P \ 0.05

minor increases in the latissimus dorsi and teres major at the lower velocities, but a cumulative decrease of EMG level from flexion to extension phase at the three highest velocities could be observed in all muscles. The role of muscle pre-activity A well-timed pre-activation of the muscular system prior to an expected load during ground contact has been described as an important prerequisite for an effective SSC action (Komi 2000). Our results demonstrated earlier muscle onsets before pole plant (Fig. 3a–d) and increases in preactivity (Figs. 4, 5, 6, 7) in the recorded arm and shoulder muscles with increasing DP velocities. This is in line with studies of running (Boyer and Nigg 2004; Ishikawa and Komi 2007; Komi et al. 1987; Kyro¨laïnen et al. 2005) and jumping (Ishikawa et al. 2005; Mrdakovic et al. 2008; Sousa et al. 2007) showing the occurrence of increased preactivity in leg muscles with increased loads. Similarly to our results (Fig. 3a–d), Nilsson et al. (1985) demonstrated

an earlier onset of extensor activity with increasing loads when changing from walking to running. So the question arises: what are possible reasons for and functions of higher and earlier muscle pre-activity with increasing loads during DP? Increased muscle pre-activity is generally accepted as a preparatory muscle action in order to accommodate increasing impact loads during different types of locomotion (for refs see Komi 2000). From a functional point of view, the increased pre-activity in the measured arm and shoulder extensors (Figs. 4, 5, 6, 7) may be interpreted as a reaction of the neuromuscular system, providing enhanced stiffness of the muscle–tendon complex in order to support the toleration of increasing impact forces, peak pole forces and rates of force development across increasing DP velocities (Fig. 2b). It may not be taken to be a safety mechanism, such as in sprint running or hopping on hard surfaces with *8–9 times higher peak ground reaction forces at the highest intensities (Kyro¨laïnen et al. 2005; Moritz and Farley 2005; Nicol et al. 2006) compared to DP and the inhibitory role of I-b afferents. Secondly, increased muscle–tendon and joint stiffness may provide an efficient transfer of high forces through the poles down to the ground at the beginning of poling phase. The positive influence of pre-activity on muscle–tendon or joint stiffness has been demonstrated in several studies on running and jumping (Gollhofer et al. 1984; Kuitunen et al. 2002; Kyro¨laïnen et al. 1999, 2003). In addition to the abovementioned aspects, a well pre-activated system has been shown to increase the capacity for storing elastic energy in the muscle–tendon complex during eccentric loading in dynamic movements (Bosco et al. 1982; Cavagna 1977; Gollhofer et al. 1992). Several previous studies on force–velocity characteristics regarding contraction velocity of single fibers in vivo showed that type I fibers need *100–140 ms and type IIA *55–85 ms to create maximal tension and thereby force (Buchthal and Schmalbruch 1970; Eberstein and Goodgold

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1968; Garnett et al. 1978). It could be argued that the decreases in time to peak pole force, as well as elbow flexion time in our study, which are well below 100 ms at the highest DP velocities represent critical limits for the full recruitment of both type I and II fibers for sufficient force generation. If slow-twitch fibers are to be fully recruited and thereby contribute to the necessary high muscular performance at high DP velocities, this fiber type must be activated prior to pole ground contact. Similar to leg muscles in walking (Nilsson et al. 1985), at the lowest velocity we found extensor muscle onsets to be very short before (TRI, LD, TMa) or, interestingly, even after pole plant (PMa) (Fig. 3a–d), which can be interpreted as a low need for early and high pre-activity due to the lower forces (Fig. 2b) and longer durations to create muscle fiber tension at this velocity. According to the size principle of motor unit recruitment (Henneman and Olson 1965; Henneman et al. 1965), small slow-twitch motor units must be recruited before larger fast-twitch motor units. This principle has been recently demonstrated to be operational during lengthening contractions in sport (for refs see Beltman et al. 2004; Chalmers 2008). Consequently, in order to activate all the available muscle units for a fast, pronounced pole force production at high velocities, slow-twitch fibers must be activated well before pole plant. Fast-twitch fibers can then be activated later so that the highest activation rate is achieved during the highest loading situation (peak pole force). The coordinated activation between slow and fasttwitch fibers enables the maximal amount of muscle fibers to be recruited; and consequently, a higher force output to be generated. As cross-country skiers have been described has having a predominance of slow-twitch fibers (*70– 75%) in their arm and shoulder muscles (Saltin 1997), it could be suggested that increased pre-activation may be a crucial strategy to enable the fast and pronounced pole force production required during limited poling times at high DP velocities. As a further important aspect, muscle pre-activity is assumed to increase the sensitivity of muscle spindles (Matthews and Stein 1969) by enhancing the alpha–gamma co-activation, causing a potentiation of stretch-reflexes in the subsequent joint flexion phase (Gottlieb et al. 1981). The higher sensitivity of muscle spindles leads to an increase in the excitation of type Ia afferents (Matthews 1984) and consequently to a facilitation of a-motoneurones, finally producing increased EMG activation in the involved extensor muscles. The additionally increased activation in the measured extensor muscles during DP directly after pole plant (Figs. 4, 5, 6, 7) can be interpreted as an effect of enhanced muscle spindle sensitivity. This has also recently been shown in running at high speeds (Kyro¨laïnen et al. 2005), where higher pre-activity was

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strongly related to higher muscle activity during the subsequent lengthening of muscle–tendon units during ground contact. This is in line with our results on DP. Muscle activity during poling phase The poling phase was characterized by a flexion–extension pattern in the elbow joint which became more pronounced across velocities (Fig. 2a). Requirements for an effective SSC (Komi 2000) in the elbow joint during DP can be interpreted as fulfilled, especially at high velocities with (1) an increased angular elbow flexion (muscle–tendon stretch) velocity up to *8.5 rad s-1, (2) a more immediate transition from flexion to extension phase at the highest velocities (Fig. 2a), (3) the increased forces during the flexion phase (Fig. 2b) and consequently, (4) a threefold increase of TRI activity during flexion phase together with a cumulative decrease in EMG activity from the flexion to the extension phase with increasing velocities (Fig. 4). High EMG activity in the flexion phase and the stretching velocity of the muscle–tendon complex have been proven to create high stiffness in leg muscles resulting from stretch reflexes (Dietz et al. 1979; Gollhofer et al. 1984; Kuitunen et al. 2002) and, consequently, to provide a beneficial condition for the storage of elastic strain energy in the tendo-muscular unit (Bosco et al. 1981; Ishikawa and Komi 2004; Komi and Gollhofer 1997). During high speed DP, this elastic energy might also be utilized in the subsequent arm-extension (shortening) phase to economize performance (Cavagna et al. 1964) by maintaining high muscle output, even if the neural input is decreasing (Fig. 4). In running and jumping (Bosco et al. 1981; Ito et al. 1983) and diagonal skiing (Komi and Norman 1987) the lower muscle activity during the concentric compared to the pre-stretch phase, has been interpreted as increased mechanical efficiency of positive work due to the storage and release of elastic energy. Similar to SSC actions in legs (Aura and Komi 1986; Bosco et al. 1981; Gollhofer et al. 1992), the increasing stretch velocity in the TRI during DP may have increased the mechanical efficiency of the elbow-extension phase at higher velocities. This can partly explain the fact that pole force during extension phase can be produced with lower EMG activity. Additionally, it has been suggested that the lower motor unit activity in the leg muscles during diagonal skiing (Komi and Norman 1987) implies lower expenditure of metabolic energy in the muscle, increasing the efficiency of the positive work phase (Norman and Komi 1985). Recent studies on SSC in jumping and running using real-time ultrasonography demonstrated decreased fascicle and increased tendinous tissue lengthening during the eccentric phase due to higher pre-stretch intensity by increased jumping height or running speed (for refs see Ishikawa and Komi 2008;


Magnusson et al. 2008). The observation that stiffer fascicles may help reuse of elastic recoil for the tendinous tissues in higher pre-stretch conditions (Ishikawa and Komi 2004) can support the concept of improved efficiency of positive work during SSC (Aura and Komi 1986), as well as for DP, indicated by decreases in muscle activity from the flexion to extension phase, especially at high velocities (Fig. 4). In SSC, the integration of reflex mechanisms seems to play an important role in enhancing power output (Dietz et al. 1979; Kyro¨laïnen et al. 2005; Nicol and Komi 1998). According to Gollhofer et al. (1990), the eccentric phase in a movement cycle is influenced by mono- and poly-synaptic reflex mechanisms. In our study, an elbow flexion occurred after pole plant with increasing angular flexion velocities across speeds. The elbow flexion time gradually shortened from 229 ± 16 ms at 9 km h-1 down to 93 ± 4 ms at vmax. This corresponds rather well with the reflex time periods of the RIA phase from 21 km h-1 with flexion times of 131 ± 28 ms. From the timing, as well from the increasing EMG activity in the RIA phase (Fig. 8), it may be concluded that at higher DP velocities stretch-reflexes might play an important role in stiffness regulation in the TRI muscle in order to enhance force production during the extension phase, although no clear evidence of a reflex response can be seen in every single EMG signal. However, the relevance of reflex activation is underlined by the fact that at the faster velocities the decrease in aEMG from RIA to LER phase increases (Fig. 8) and therefore neuromuscular activation to improve motor performance is only provided in this reflex-mediated phase. Additionally, as at faster velocities EMG values in some muscles were above the MVC level, this can be interpreted as an indication of the reflex contribution to EMG. Similar to TRI, the measured shoulder muscles also showed a further but even greater increase in EMG activity (Figs. 5, 6, 7) across velocities during the first part of the poling phase up to peak pole force. However, due to the fact that no kinematic data were measured for the shoulder joint in the present study, it is somewhat speculative to decide whether the analyzed shoulder muscles work in a SSC mode or not, even if the neuromuscular patterns give some evidence for this. Support for a flexion–extension pattern in the shoulder joint during DP could be found in kinematic data by Smith et al. (1996), showing an initial short shoulder flexion directly after pole plant in elite skiers at racing speed, before they extended their shoulder. Based on that, the increased pre-activity before pole plant in our study as well as the multifold increase in EMG activity during the rising part of the force curve may be interpreted as the measured shoulder muscles using a stretch-shortening mechanism at higher velocities. The significant role of the LD, TMa and PMa muscles in DP has been described in

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an earlier study by our group (Holmberg et al. 2005) as being highly active shoulder extensors during the initial part of poling phase. It is notable that the EMG of the shoulder muscles even exceeded the MVC level at higher velocities (Figs. 5, 6, 7). The high muscle activity shows the importance of the analyzed shoulder muscles for a fast and pronounced pole force production (Fig. 2b) during DP at high velocities. In addition, DP represents a functional and dynamic motion with higher activation levels, compared to an isometric situation. This is in line with findings in Kyro¨laïnen et al. (2005), who found higher leg muscle EMG activity compared to the MVC level during the braking and even the pre-contact phase in running. This was interpreted as representing an additional recruitment of muscle fibers during the more functional situation in running. In summary, this study demonstrates that the neuromuscular pattern of arm and shoulder muscles across increasing velocities during DP on a treadmill is characterized by an increase in muscle onset times and pre-activity. Both aspects are described as important prerequisites for an effective stretch-shortening cycle. In addition, the substantial increase in EMG activity during the initial flexion phase in the elbow joint, the immediate transition from flexion to extension at higher velocities and the decrease in EMG activity from the flexion to the extension phase further support an occurrence of SSC contraction during DP. This pattern is evident in the triceps brachii. However, even though the shoulder muscles show a similar neuromuscular pattern further kinematic analyses have to be performed to fully confirm that the stretchshortening cycle is also apparent in the shoulder muscles. Finally, DP may serve as a useful exercise mode for investigating the biomechanical and neurophysiological aspects of the stretch-shortening cycle in upper limb extensor muscles. Future studies are recommended to combine kinematic, kinetic and EMG methods in order to analyze the stretch-shortening cycle in cross-country skiing, including 3D analysis on snow. Acknowledgments We thank Dr. Vojko Strojnik at University of Ljubljana, Slovenia for his valuable comments on the manuscript, and the Swedish Winter Sports Research Centre for providing us the facility for this study. The authors also thank the athletes and coaches for their participation, enthusiasm, and cooperation in this study. This study was supported by the Swedish Olympic Committee.

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