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In vivo moment generation and architecture of the human plantar flexors after different shortening–stretch cycles velocities
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Journal of Electromyography and Kinesiology 19 (2009) 322–330 www.elsevier.com/locate/jelekin
In vivo moment generation and architecture of the human plantar flexors after different shortening–stretch cycles velocities Gianpiero De Monte, Adamantios Arampatzis
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Institute of Biomechanics and Orthopaedics, German Sport University of Cologne, Carl-Diem-Weg 6, 50933 Cologne, Germany Received 5 June 2007; received in revised form 10 August 2007; accepted 14 August 2007
Abstract The purpose of this study was to examine the moment generation of the human plantar flexors and the architecture of the gastrocnemius medialis muscle during and after shortening–stretch cycles in vivo. Fourteen male subjects (30 ± 7 years, 177 ± 7 cm, 80 ± 9 kg) performed a series of electro-stimulated shortening–stretch plantar flexion contractions. The shortening–stretch cycles were performed at three constant angular velocities (25/s, 50/s, 100/s), two amplitudes (15 and 25 ankle angle changes) and at two different stimulation frequencies (30 Hz and 85 Hz). The resultant ankle joint moments were calculated through inverse dynamics. Pennation angle and fascicle length of the m. gastrocnemius medialis at rest and during contractions were measured using ultrasonography. The corresponding ankle moments, kinematics and changes in muscle architecture were analysed at seven time intervals. A three-way analysis of variance (amplitude · velocity · stimulation frequency) and post-hoc test with Bonferroni correction were used to check the amplitude, velocity and stimulation level related effects on moment enhancement (a = 0.05). The results show an ankle joint moment enhancement after shortening–stretch cycles influenced by muscle architectural changes. We found 2–3% isometric ankle joint moment enhancement at steady state, 1.5–2.0 s after the shortening–stretch cycle. However, the observed alteration in muscle architecture after the imposed perturbation, could lead to an underestimation (1–3%) of joint moment enhancement due to the force–length relationship of the triceps surae. Furthermore, the enhancement observed was independent of the shortening–stretch amplitude, velocity and stimulation frequency. 2007 Elsevier Ltd. All rights reserved. Keywords: Force enhancement; Force depression; Muscle architecture; Muscle mechanics; Triceps surae
1. Introduction It is accepted that following active muscle stretching or shortening, phenomena known as force enhancement and force depression can be present (Abbott and Aubert, 1952; Edman, 1978a,b; Edman et al., 1982; Marechal and Plaghki, 1979). These phenomena are present in voluntary contractions (Lee and Herzog, 2002) during both, maximal and submaximal activation level conditions (Oskouei and Herzog, 2006). Force depression has been shown to increase with increasing shortening magnitude (Marechal
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Corresponding author. Fax: +49 221 4971598. E-mail address: [email protected] (A. Arampatzis).
1050-6411/$ - see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2007.08.005
and Plaghki, 1979), with decreasing shortening velocities (Abbott and Aubert, 1952; De Ruiter et al., 1998), and with increasing activation levels (De Ruiter et al., 1998). Force enhancement becomes greater with increasing stretch amplitudes (Edman, 1978a,b; Edman et al., 1982), has been shown to be stretch velocity dependent in the whole muscle (Abbott and Aubert, 1952), and activation level dependent for voluntary contractions (Oskouei and Herzog, 2006). However, during daily activities muscles very rarely undergo simple stretches or shortenings but rather stretch–shortening or shortening–stretch cycles. To the best of our knowledge there have been no studies reported in the literature to date investigating history dependent phenomena of force production such as force depression or force enhancement after stretch–shortening or shorten-
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ing–stretch cycles in human muscles in vivo. The existing reports on force depression or force enhancement after stretch–shortening or shortening–stretch cycles all were obtained from animal models (Herzog and Leonard, 2000; Lee et al., 2001; Rassier and Herzog, 2004b). Herzog and Leonard (2000) reported that in cat soleus muscle the isometric forces following shortening–stretch cycles of equal magnitude were the same as those obtained for purely isometric contractions. They concluded that when the amounts of shortening and stretch are equal, the net result is no force enhancement. On the other hand, Lee et al. (2001) found force enhancement greater than 1% of the reference isometric force after shortening–stretch cycles of equal magnitude. Additionally Rassier and Herzog (2004b) reported force enhancements between 5% and 10% in single skeletal muscle fibres after different shortening–stretch cycles. Generally it is believed that the magnitude of shortening preceding stretch affects the force enhancement in a dose dependent manner, i.e. when the amount of shortening increased, the force enhancement decreases (Herzog and Leonard, 2000; Herzog et al., 2003). The architectural complexity of the muscles analysed during human studies (m. adductor pollicis, m. quadriceps femoris) create essential difficulties to translate the generated joint angular displacement into accurate muscle lengths (De Ruiter et al., 2000). Furthermore, it is well known that during voluntary contractions in vivo despite careful external fixations it is not possible to completely prevent any motion of the joint relative to the dynamometer (Magnusson et al., 2001; Muramatsu et al., 2001). More recently it has been reported that even for a single isometric plantar flexion (Arampatzis et al., 2005) or knee extension (Arampatzis et al., 2004) contraction trial, at identical joint moments the joint angles could differ causing significant changes in muscle architecture (Karamanidis et al., 2005). Differences in muscle architecture after shortening or stretching in relation to the reference contraction can affect the moment generation independently of force depression or force enhancement phenomena (due to the force–length relationship of the muscle). In general, for a proper interpretation of history effects on muscle contraction, information about the actual fascicle length is necessary. The purpose of this study was to examine the moment generation of the human plantar flexors and the architecture of the m. gastrocnemius medialis (GM) during and after shortening–stretch cycles in vivo. Based on the current literature (Arampatzis et al., 2004, 2005; Herzog and Leonard, 2000; Lee et al., 2001; Rassier and Herzog, 2004b) we expected a moment enhancement after shortening–stretch cycles in the triceps surae muscles and an influence on moment enhancement by the muscle architecture. We further expected an amplitude, velocity and activation effect on moment enhancement after the shortening–stretch cycle. Therefore, we investigated shortening–stretch contractions of equal magnitudes in the human plantar flexor muscles by manipulating the shortening–stretch amplitude, velocity and electrical muscle stimulation intensity.
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2. Methods 2.1. Participants Fourteen male volunteers participated in the study (age: 30 ± 7 years, height: 177 ± 7 cm, body mass: 80 ± 9 kg). The participants were all recruited from students of the German Sport University Cologne and gave their informed consent to participate in the experiment. 2.2. Experimental protocol The participants performed a series of electro-stimulated shortening–stretch plantar flexion contractions in three different measuring sessions. The subjects were seated on a custom-made dynamometer with the right ankle dorsiflexed at 80 (tibia perpendicular to the sole, ankle angle 90) and the knee flexed at 120 (knee fully extended 180). Inextensible Velcro straps were used to fix the right leg and the foot to the dynamometer. In addition, the thigh and the trunk of the subjects were fixed on the dynamometer chair with inextensible belts (Fig. 1). After a warm up period, consisting of 5 min of submaximal electro-stimulation and 2–3 submaximal voluntary plantar flexions, the subjects performed one maximal voluntary contraction (MVC). After this, the maximal tolerated electro-stimulation intensity (mA) was determined at the subjective limit of each subject. The operator manually increased the stimulation intensity of the electro-stimulator with continuous subject feedback. The right triceps surae muscle of each participant was activated by means of a constant-voltage adjustable intensity electrical stimulator (Compex 2, Compex Me´dical SA, Switzerland) using monopolar biphasic compensated square wave pulses (85 Hz). The 85 Hz stimulation yielded a maximal isometric force response in the gastrocnemius medialis. Two carbon–rubber stimulation electrodes (4.5 · 7.5 cm) thinly coated with conductive gel, were secured onto the shaved and cleaned skin. The cathode was positioned midway across the medial and lateral heads of the gastrocnemius approximately 5 cm distal to the crease in the popliteal fossa. The anode was positioned at the soleus motor point, along the medial line directly below the belly of the medial and lateral gastrocnemius muscles. The motor point was identified by moving the electrode (anode) over the soleus muscle to find the position where the lowest stimulation intensity produced the largest response (muscle contraction). The duration of the electrical stimulation was 6 s. During this time the dynamometer first remained static, followed by a 25 or 15 plantar flexion (shortening), a 25 or 15 dorsiflexion (stretch) and finally static again. The ankle rotations (shortening–stretch cycles) were performed at three constant angular velocities (25/s: slow velocity; 50/s: medium velocity; 100/s: high velocity). The final isometric contraction induced by the electrical stimulation persisted for at least two seconds; between successive contractions there was a resting period of at least 2 min. The room temperature was monitored in all experiments: range 22–26.7 C, mean ± SD 24.4 ± 1.3 C. In the first session the participants performed the shortening– stretch cycles in all three angular velocities (25/s, 50/s and 100/ s) at constant shortening–stretch amplitude of 25 and by a stimulation frequency of 85 Hz, in a randomised order (Fig. 2). In the second session the experimental design was the same regarding the three angular velocities and stimulation frequencies as the first and only the constant shortening–stretch amplitude changed to
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15. In the third session we examined shortening–stretch cycles at all three angular velocities (25/s, 50/s and 100/s) with a stimulation frequency of 30 Hz (in contrast to the 85 Hz, a 30 Hz stimulation frequency resulted in a submaximal isometric force response of the triceps surae muscle). The shortening–stretch amplitude in the third session was 15. Between the three experimental sessions there was a break for at least three weeks. In addition at these three measuring sessions, in a later experiment, 10 of the participants performed a series of isometric electrostimulated contractions at four different ankle joint positions (80, 90, 100, 110) in order to determine the plantar flexors torque–angle relationship at both stimulation frequencies (submaximal: 30 Hz and maximal: 85 Hz) used during the main experiments. 2.3. Measurement of the ankle joint moment
Fig. 1. Experimental setup. A custom-made dynamometer was built for measuring the plantar flexion moment. The subjects were seated with the ankle dorsiflexed at 80 (tibia perpendicular to the sole = 90 ankle angle) and the knee flexed at 120 (knee fully extended = 180). Inextensible Velcro straps were used to fix the foot to the dynamometer’s footplate. In addition the thigh and the trunk of the subjects were fixed to the dynamometer chair with inextensible belts.
For measuring the plantar flexion moment, a custom-made dynamometer was built. It consisted of a Global Drive 9325 servo inverter (Lenze Drive Systems GmbH, Hameln Germany) coupled with a synchronous servo-motor MDSKS 017-13, 185 (Lenze Drive Systems GmbH, Hameln Germany) accessorised with a torque sensor type 8628 (Burster gmbh Co. KG, Gernsbach Germany, measuring range 0 ± 500 Nm). At the beginning of each experiment, the axis of rotation of the ankle was carefully aligned with the axis of rotation of the dynamometer. The axis of rotation of the ankle joint was defined to be parallel to the axis of the dynamometer passing through the midpoint of the line connecting both malleoli. During the contraction, the axes clearly shifted away from each other. This shift significantly influences the resultant joint moments (Arampatzis et al., 2005, 2006, 2007). In order to correct for this influence, the kinematics was recorded using the Vicon 624 system (Vicon Motion Systems, United Kingdom) with eight cameras operating at 250 Hz. During the plantar flexion the co-ordinates of 10 retro-reflective markers (radius 5 mm) fixed on the following positions were captured: tuber calcanei, lateral and medial malleolus, the most prominent points of the lateral and medial femoral condyles, trochanter major, forefoot on the pressure insole between the second and the third metatarsals, axis of the dynamometer and two markers on the footplate to define the line of force application (Fig. 1). The moments measured by the dynamometer were registered synchronously by the Vicon system at a sampling rate of 3750 Hz. To determine the centre of pressure under the foot a flexible pressure distribution insole (Pedar-system, Novel GmbH, Germany) operating at 99 Hz was used. The Pedar-system emitted an additional signal switching between 0 and 5 V every 10 frames, which was also registered by the Vicon unit to synchronise both measuring systems. To achieve a common frequency (3750 Hz) with the moment data, the kinematic and centre of pressure data were interpolated using quintic splines. The resultant moments at the ankle joint were calculated through inverse dynamics as described in detail in a previous publication (Arampatzis et al., 2007). 2.4. Measurement of muscle architecture
Fig. 2. Example comparison of the ankle joint moment obtained from one subject during the three shortening–stretch cycle velocities (low: 25/s, medium: 50/s, and high: 100/s) at 85 Hz stimulation frequency and 25 shortening–stretch amplitude.
A 7.5 MHz linear array ultrasound probe (Aloka SSD4000; 43 Hz) was used to visualise the muscle belly of the GM at rest and during the contractions. The ultrasound probe was placed above the GM muscle belly at about 50% of its length. The
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Fig. 3. Ultrasound image of the muscle gastrocnemius medialis with an overlaid graphical representation of a fascicle, the deep aponeurosis and the pennation angle a.
ultrasound images were digitally recorded via firewire on a notebook for further analysis. The video data (ultrasound sequences) were synchronised with the remaining data using a synchronisation box (Peak Performance Technologies, USA). The experiment leader manually triggered a TTL signal (0–5 V), which was overlaid on the video images and simultaneously captured by the Vicon system. The video data were analysed frame-by-frame using the Simi video analysis system (Simi Motion 6.1, SIMI Reality Motion Systems GmbH, Unterschleißheim Germany). The pennation angle of the GM was measured as the angle of insertion of one muscle fascicle into the deep aponeurosis. The fascicle length was defined as the length of the fascicular path between the insertions of the fascicle into the upper and deeper aponeuroses (Fig. 3). When the fascicle extended out of the acquired ultrasound image the length of the missing portion of the fascicle was estimated by linear extrapolation of both, the fascicular path and the aponeurosis (Arampatzis et al., 2006). 2.5. Data analysis Previous studies on history dependence of force production (Brown and Loeb, 2000; Cook and McDonagh, 1995; Edman, 1978a,b; Ettema et al., 1992; Herzog and Leonard, 2002; Lee and Herzog, 2002; Lee et al., 2000; Linari et al., 2000; Peterson et al., 2004; Ruiter et al., 2000) analysed force parameters at intervals located between 50 ms and 4.5 s after stretching or shortening movements. We quantify the plantar flexion moment at the plateau before the onset of the shortening–stretch cycle (I0) and at six time intervals (I1, I2, I3, I4, I5, I6) beginning at the end of the stretch and ending two minutes later (Fig. 4). At these same intervals ankle-, knee-, pennation-angles and fascicle lengths were determined (Fig. 5) and compared to each other. A three-way analysis of variance (amplitude · velocity · stimulation frequency) and post-hoc test with Bonferroni correction were used to check the amplitude, velocity and stimulation level related effects on moment enhancement after the shortening–stretch cycle. The level of significance was set at a = 0.05.
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Fig. 4. Analysed intervals of the ankle joint moment–time (I0–I6). Initial interval 0: average moment value during the 500 ms before starting the shortening. Interval I1 average value in the first 125 ms after stretch end. Interval I2: average value between 125 and 250 ms after stretch end. Interval I3: average value between 250 and 500 ms after stretch end. Interval I4: average value between 500 ms and 1.0 s after stretch end. Interval I5: average value between 1.0 and 1.5 s after stretch end. Interval 6: average value between 1.5 and 2.0 s after stretch end.
3. Results 3.1. Maximal electrical stimulation frequency (85 Hz) At the plateau of the electro-stimulated contractions prior to the beginning of the shortening–stretch cycles (I0) the ankle joint moment was about 43% of the moment reached during the maximal voluntary contraction. The corresponding actual ankle angle at this time was 100.7 ± 3.0 (mean ± SD, Table 1). At I0 fascicle length and pennation angle of the GM muscle were 21.4 ± 3.4 mm and 55.8 ± 4.5, respectively (mean ± SD, Table 1). The architecture of the GM muscle after the shortening– stretch cycle differed significantly (p < 0.05) from that observed at the initial isometric contraction. For all examined intervals after the shortening–stretch cycle, the ratio of the pennation angle to the I0 was higher than 1.0 (Fig. 6), and below 1.0 for the fascicle length (Fig. 6) indicating that after the shortening–stretch cycle the pennation angles where greater and the fascicle lengths shorter than at I0. However, within the intervals I3–I6 the fascicle length values showed no significant differences (p > 0.05) indicating a steady state in the GM architecture (Fig. 6). In a similar manner to the GM architecture, the ankle angle was greater at the examined intervals after the shortening– stretch cycle than at the initial isometric contraction (Fig. 6). At all studied shortening–stretch cycle velocity combinations and at all intervals (I1–I6) the ankle joint moment ratios were statistically significant greater than at I0 (p < 0.01) (Fig. 6). At I1 (0–0.125 s after stretch) the mean ± SD of the moment ratio was 1.144 ± 0.057. This value decreased to 1.026 ± 0.046 at I6 (1.5–2 s after stretch).
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Fig. 5. Footplate angle-, ankle joint moment-, gastrocnemius medialis pennation angle- and gastrocnemius medialis fascicle length–time histories during the shortening–stretch cycle at 30 Hz electrical stimulation and 25 footplate amplitude. Data from one trial.
3.2. Submaximal electrical stimulation frequency (30 Hz) Under submaximal electrical stimulation frequency conditions the mean ± SD torque was more than 10% lower than at the maximal (85 Hz) condition (p < 0.05). The torque at I0 was 43.5 ± 8.9 Nm. Similarly, the ankle angle, the fibre length and the pennation angle at I0 were significantly different (p < 0.05) from the 85 Hz stimulation frequency condition (Table 1). Nevertheless after the shortening– stretch cycle the overall behaviour was similar to that observed at the 85 Hz stimulation condition. For the 30 Hz stimulation frequency the architecture of the GM muscle and the ankle angle following shortening–stretching cycles were again significantly different than those at the I0. At all examined intervals (I1–I6) the fascicle lengths were shorter than at the beginning (see ratios in Fig. 7), whereas the pennation and the ankle angles were greater (Fig. 7). The fascicle length of the GM showed no significant differences within the intervals I3–I6 (p > 0.05), indicating a steady state in the GM architecture (Fig. 7). As we Table 1 Ankle joint moment (interval I0) and corresponding actual ankle angle, for the 85 Hz electro-stimulation frequency compared to the values reached during 30 Hz Parameter
85 Hz
30 Hz
Joint moment (Nm) Ankle angle () Fascicle length (mm) Pennation angle ()
48.5 ± 9.0 100.7 ± 3.0 21.4 ± 3.4 55.8 ± 4.5
43.5 ± 8.9* 99.6 ± 3.9* 23.7 ± 3.9* 52.1 ± 5.4*
The same comparison is made for the architectural characteristics (fascicle length, pennation angle) of the m. gastrocnemius medialis during the maximal isometric force production (means ± SD). * Statistically significant differences between 85 and 30 Hz electro-stimulation frequency (p < 0.05).
observed at the stimulation frequency of 85 Hz, also at 30 Hz the ankle joint moment ratios were significantly higher after the shortening–stretch cycle (I1–I6) than before (I0) (p < 0.01) (Fig. 7). We found a stimulation frequency dependent behaviour for the first 500 ms after the shortening–stretch cycle (intervals I1–I3) where the joint moment ratios were lower for the 30 Hz than for the 85 Hz stimulation. 4. Discussion The purpose of this study was to examine the moment generation of the human plantar flexors and the architecture of the m. gastrocnemius medialis before and after shortening–stretch cycles in vivo. To our knowledge this was the first study showing that after shortening–stretch cycles an ankle joint moment enhancement could be present, and that in vivo this enhancement may be influenced by muscle architectural changes. We found 2–3% isometric ankle joint moment enhancement at steady state, 1.5–2.0 s after the shortening–stretch cycle. However, the observed alteration of the architectural characteristics of the muscle after the imposed perturbation, could lead to an underestimation of the ankle joint moment enhancement due to the force–length relationship of the triceps surae. Furthermore, for the first time it was found that the ankle joint moment enhancement observed after the shortening–stretch cycle was independent of the shortening–stretch amplitude, velocity and stimulation frequency. Although force enhancement after stretch and force depression after shortening have been intensively studied, the literature reports concerning history dependent phenomena such as force depression or force enhancement after stretch–shortening or shortening–stretch cycles are
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Fig. 6. Mean ± SD of several ratios during the 85 Hz electrical stimulation frequency at 15 and 25 footplate motion amplitude at the seven different analysed intervals (n = 10). Left column: values at 15 footplate motion amplitude (pennation angle, fascicle length, ankle angle, joint moment). Right column: values at 25 footplate motion amplitude. (*) Statistically significant differences to interval I0 (p < 0.05).
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Fig. 7. Mean ± SD of several ratios during the 30 Hz electrical stimulation frequency and 15 footplate motion amplitude at the seven different analysed intervals (n = 10). Top: pennation angle (left) and fascicle length (right). Bottom: ankle angle (left) and ankle joint moment (right). (*) Statistically significant differences to interval I0 (p < 0.05).
limited (Herzog and Leonard, 2000; Lee et al., 2001; Rassier and Herzog, 2004b). We found that after shortening– stretch cycles (1.5–2.0 s, interval I6) the isometric plantar flexion moments were enhanced by 2–3% in relation to the initial isometric moment. The results of the present study also show that after the shortening–stretch cycle ankle angle, fascicle length and pennation angle are significantly different from the initial isometric condition (p < 0.05). At all examined intervals after the shortening– stretch cycle the ankle angles as well as the pennation angles showed higher values, whereas the fascicle lengths were lower than at the initial interval I0. Consequently, the differences in leg geometry (higher ankle angle) after the shortening–stretch cycle influence the architecture of the GM muscle–tendon unit and possibly also the architecture of the soleus and gastrocnemius lateralis muscles (the length of all these three muscles is ankle angle dependent). We examined the moment generation of the plantar flexor muscles before and after the shortening–stretch cycle at an actual ankle joint angle of 100 ± 3 and a knee joint angle of 118 ± 5 (real ankle and knee joint angles determined by the kinematic analysis). It has been reported that at this position the muscles of the triceps surae muscle–tendon unit operate on the ascending limb of the force–length relationship (Herzog et al., 1991). Thus shorter fascicle lengths
of the GM after the shortening–stretch cycle would reduce the force potential of the muscle as compared to the initial condition. This in turn would mean that the moment enhancement found in our experiment was underestimated. In order to estimate the effect of these differences in ankle angle between the initial condition and time interval I6 we examined the moment–ankle angle relationship using both electro-stimulation frequencies (Fig. 8). The data plotted in Fig. 8 indicate that the moment enhancement 1.5–2.0 s after the shortening–stretch cycle is underestimated by 1–3%. Although the exact underlying mechanisms of force depression after shortening or force enhancement after stretch in skeletal muscles are at the moment in debate (Granzier and Pollack, 1989; Herzog et al., 2003; Sugi and Tsuchiya, 1988), experimental data indicate that mechanisms related to cross-bridge kinetics contribute to force depression as well as to force enhancement phenomena (Herzog et al., 2006, Herzog and Leonard, 1997, 2002, 2005; Rassier and Herzog, 2004a). In addition a ‘‘passive’’ force enhancement component, especially for stretches performed on the descending limb of the force–length relationship, has also been proposed (Herzog and Leonard, 2002). However, independent of the mechanisms underlying history dependent phenomena in muscle contraction, it is
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accepted that force depression increases with increasing shortening magnitude (Bullimore et al., 2007; Herzog and Leonard, 1997; Marechal and Plaghki, 1979) and decreases with increasing shortening velocity (De Ruiter et al., 1998; Meijer et al., 1997). The latter phenomenon is possibly associated to the decrease in force generation during the contraction at higher shortening velocities (De Ruiter et al., 1998; Leonard and Herzog, 2005). It is also accepted that the steady-state force enhancement after stretch increases with increasing magnitude of stretch being independent of stretch velocity (De Ruiter et al., 2000; Edman, 1978a,b; Lee and Herzog, 2002). Recent studies showed that the stretch magnitude affects primarily the ‘‘passive’’ component of the force enhancement and that the so called ‘‘active’’ component (difference between steady-state force enhancement and ‘‘passive’’ component) (Herzog and Leonard, 2002) is not influenced by the magnitude of the stretch (Bullimore et al., 2007; Schachar et al., 2004). In our study the shortening–stretch contractions were performed on the ascending limb of the force–length relationship of the triceps surae muscles (Fig. 8). Earlier studies reported no evidence of passive force enhancement in the ascending limb of the force–length relationship neither in whole muscle preparations (Herzog and Leonard, 2002) nor in single fibres of skeletal muscles (Peterson et al., 2004). This indicates that the ‘‘passive’’ component of the steady-state force enhancement after the shortening–stretch cycle in our experiments should have a negligible contribution to the observed moment enhancement (Herzog, 2001; Herzog and Leonard, 2002; Peterson et al., 2004). Based on the literature reports stating that (a) the magnitude and velocity of shortening affect the force depression (Herzog and Leonard, 1997; Marechal and Plaghki, 1979), (b) the ‘‘active’’ component of the force enhancement is not affected by the magnitude and velocity of stretching (Bullimore et al., 2007; Schachar et al., 2004) and (c) during shortening–stretch cycles the force depression and force enhancement are additive (Lee et al., 2001) we expected the shortening/stretch magnitude and velocity to influence the moment enhancement after the examined shortening– stretch cycles. Furthermore, the moment values at the end of the shortening showed a velocity effect leading to lower values when increasing the angular velocities of the footplate, indicating an influence of the shortening velocity on the mechanisms of force depression during shortening (De Ruiter et al., 1998; Leonard and Herzog, 2005). Nevertheless we did not find any influence of shortening or stretching amplitude or velocity of equal magnitudes on the moment enhancement after shortening–stretch cycles in physiological force and length ranges of the triceps surae muscles. The results illustrate that the mechanisms responsible for force depression and force enhancement during shortening–stretch cycles at the ascending limb of the force–length relationship of the triceps surae muscles are insensitive to the amplitude or velocity of shortening/stretch of equal magnitudes on moment enhancement after the contraction. In agreement with previous works (De Ruiter et al., 2000),
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Fig. 8. Ankle joint moment–angle relationship for the 85 Hz and the 30 Hz electrical stimulation frequencies (mean ± SD). At both frequencies the muscle was tested in the ascending limb of its force–length relationship. I0: ankle angle at the initial interval; I6: ankle angle 1.5–2 s after the shortening–stretch cycle.
we found that after a shortening–stretch cycle the moment enhancement at the steady state (intervals I4–I6) was not influenced by changes in stimulation frequency. Our results also match those of De Ruiter et al. (2000) in that the reduction of the activation (stimulation frequency) produced significantly lower moment ratios in the first 500 ms (I1–I3) (p < 0.05) (see Fig. 7). In summary, we demonstrated a moment enhancement (2–3%) at the high and low frequency of electro-stimulated human triceps surae muscle in vivo after shortening–stretch cycles. The observed moment enhancement was not affected by the amplitude or velocity of shortening–stretching of equal magnitudes using maximal and submaximal electro-stimulation intensities. Finally, the analysis of the GM architecture during the shortening–stretch cycle, suggest an underestimation (1–3%) of the observed moment enhancement. This strengthens the need to consider the muscle architecture when studying history dependent phenomena of muscle force generation after shortening or stretching contractions in vivo. References Abbott BC, Aubert XM. The force exerted by active striated muscle during and after change of length. J Physiol 1952;117:77–86. Arampatzis A, Karamanidis K, De Monte G, Stafilidis S, Morey-Klapsing G, Bru¨ggemann GP. Differences between measured and resultant joint moments during voluntary and artificially elicited isometric knee extension contractions. Clin Biomech (Bristol, Avon) 2004;19:277–83. Arampatzis A, Morey-Klapsing G, Karamanidis K, De Monte G, Stafilidis S, Bru¨ggemann GP. Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J Biomech 2005;38:885–92. Arampatzis A, Karamanidis K, Stafilidis S, Morey-Klapsing G, De Monte G, Bru¨ggemann GP. Effect of different ankle- and knee-joint positions on gastrocnemius medialis fascicle length and EMG activity during isometric plantar flexion. J Biomech 2006;39:1891–902. Arampatzis A, De Monte G, Morey-Klapsing G. Effect of contraction form and contraction velocity on the differences between resultant and measured ankle joint moments. J Biomech 2007;40:1622–8.
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Brown IE, Loeb GE. Measured and modeled properties of mammalian skeletal muscle: III. The effects of stimulus frequency on stretchinduced force enhancement and shortening-induced force depression. J Muscle Res Cell Motil 2000;21:21–31. Bullimore SR, Leonard TR, Rassier DE, Herzog W. History-dependence of isometric muscle force: effect of prior stretch or shortening amplitude. J Biomech 2007;40:1518–24. Cook CS, McDonagh MJ. Force responses to controlled stretches of electrically stimulated human muscle–tendon complex. Exp Physiol 1995;80:477–90. De Ruiter CJ, De Haan A, Jones DA, Sargeant AJ. Shortening-induced force depression in human adductor pollicis muscle. J Physiol 1998;507(Pt 2):583–91. De Ruiter CJ, Didden WJ, Jones DA, Haan AD. The force–velocity relationship of human adductor pollicis muscle during stretch and the effects of fatigue. J Physiol 2000;526 Pt 3:671–81. Edman KA. Maximum velocity of shortening in relation to sarcomere length and degree of activation of frog muscle fibres [proceedings]. J Physiol 1978a;278:9P–10P. Edman KA, Elzinga G, Noble MI. Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. J Physiol 1978b;281:139–55. Edman KA, Elzinga G, Noble MI. Residual force enhancement after stretch of contracting frog single muscle fibers. J Gen Physiol 1982;80:769–84. Ettema GJ, Huijing PA, de Haan A. The potentiating effect of prestretch on the contractile performance of rat gastrocnemius medialis muscle during subsequent shortening and isometric contractions. J Exp Biol 1992;165:121–36. Granzier HL, Pollack GH. Effect of active pre-shortening on isometric and isotonic performance of single frog muscle fibres. J Physiol 1989;415:299–327. Herzog W. The nature of force depression and force enhancement in skeletal muscle contraction. Eur J Sport Sci 2001;1:1–14. Herzog W, Leonard TR. Depression of cat soleus-forces following isokinetic shortening. J Biomech 1997;30:865–72. Herzog W, Leonard TR. The history dependence of force production in mammalian skeletal muscle following stretch–shortening and shortening–stretch cycles. J Biomech 2000;33:531–42. Herzog W, Leonard TR. Force enhancement following stretching of skeletal muscle: a new mechanism. J Exp Biol 2002;205:1275–83. Herzog W, Leonard TR. The role of passive structures in force enhancement of skeletal muscles following active stretch. J Biomech 2005;38:409–15. Herzog W, Read LJ, ter Keurs HEDJ. Experimental determination of force–length relations of intact human gastrocnemius muscles. Clin Biomech 1991;6:230. Herzog W, Schachar R, Leonard TR. Characterization of the passive component of force enhancement following active stretching of skeletal muscle. J Exp Biol 2003;206:3635–43. Herzog W, Lee EJ, Rassier DE. Residual force enhancement in skeletal muscle. J Physiol 2006;574:635–42. Karamanidis K, Stafilidis S, De Monte G, Morey-Klapsing G, Bruggemann GP, Arampatzis A. Inevitable joint angular rotation affects muscle architecture during isometric contraction. J Electromyogr Kinesiol 2005;15:608–16. Lee HD, Herzog W. Force enhancement following muscle stretch of electrically stimulated and voluntarily activated human adductor pollicis. J Physiol 2002;545:321–30. Lee HD, Suter E, Herzog W. Effects of speed and distance of muscle shortening on force depression during voluntary contractions. J Biomech 2000;33:917–23. Lee HD, Herzog W, Leonard T. Effects of cyclic changes in muscle length on force production in in situ cat soleus. J Biomech 2001;34:979–87.
Leonard TR, Herzog W. Does the speed of shortening affect steady-state force depression in cat soleus muscle?. J Biomech 2005;38:2190–7. Linari M, Lucii L, Reconditi M, Casoni ME, Amenitsch H, Bernstorff S, et al.. A combined mechanical and X-ray diffraction study of stretch potentiation in single frog muscle fibres. J Physiol 2000;526 Pt 3:589–96. Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M. Load–displacement properties of the human triceps surae aponeurosis in vivo. J Physiol 2001;531:277–88. Marechal G, Plaghki L. The deficit of the isometric tetanic tension redeveloped after a release of frog muscle at a constant velocity. J Gen Physiol 1979;73:453–67. Meijer K, Grootenboer HJ, Koopman HF, Huijing PA. Fully isometric length–force curves of rat muscle differ from those during and after concentric contractions. J Appl Biomech 1997;13:164–81. Muramatsu T, Muraoka T, Takeshita D, Kawakami Y, Hirano Y, Fukunaga T. Mechanical properties of tendon and aponeurosis of human gastrocnemius muscle in vivo. J Appl Physiol 2001;90:1671–8. Oskouei AE, Herzog W. The dependence of force enhancement on activation in human adductor pollicis. Eur J Appl Physiol 2006;98: 22–9. Peterson DR, Rassier DE, Herzog W. Force enhancement in single skeletal muscle fibres on the ascending limb of the force–length relationship. J Exp Biol 2004;207:2787–91. Rassier DE, Herzog W. Considerations on the history dependence of muscle contraction. J Appl Physiol 2004a;96:419–27. Rassier DE, Herzog W. Effects of shortening on stretch-induced force enhancement in single skeletal muscle fibers. J Biomech 2004b;37: 1305–12. Ruiter CJ, Didden WJ, Jones DA, Haan AD. The force–velocity relationship of human adductor pollicis muscle during stretch and the effects of fatigue. J Physiol 2000;526 Pt 3:671–81. Schachar R, Herzog W, Leonard TR. The effects of muscle stretching and shortening on isometric forces on the descending limb of the force– length relationship. J Biomech 2004;37:917–26. Sugi H, Tsuchiya T. Stiffness changes during enhancement and deficit of isometric force by slow length changes in frog skeletal muscle fibres. J Physiol 1988;407:215–29. Gianpiero De Monte, graduated in sport sciences in 1997 (Milano), a current doctoral student at the institute for Biomechanics and Orthopaedics of the German Sport University of Cologne. His main research interest is the biomechanics of the muscle–tendon unit.
Adamantios Arampatzis received his PhD at the German Sport University of Cologne in 1995. He is the head of the research group focusing on the neuromechanics of the human muscoloskeletal system at the Institute of Biomechanics and Orthopaedics from the German Sport University Cologne. Among his research interests are the adaptation potential of the human system to physical activity and the influence of the neuromechanical capacity of the muscoloskeletal system on motor task behaviour during daily and sport activities.
Journal of Electromyography and Kinesiology 19 (2009) 322–330 www.elsevier.com/locate/jelekin
In vivo moment generation and architecture of the human plantar flexors after different shortening–stretch cycles velocities Gianpiero De Monte, Adamantios Arampatzis
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Institute of Biomechanics and Orthopaedics, German Sport University of Cologne, Carl-Diem-Weg 6, 50933 Cologne, Germany Received 5 June 2007; received in revised form 10 August 2007; accepted 14 August 2007
Abstract The purpose of this study was to examine the moment generation of the human plantar flexors and the architecture of the gastrocnemius medialis muscle during and after shortening–stretch cycles in vivo. Fourteen male subjects (30 ± 7 years, 177 ± 7 cm, 80 ± 9 kg) performed a series of electro-stimulated shortening–stretch plantar flexion contractions. The shortening–stretch cycles were performed at three constant angular velocities (25/s, 50/s, 100/s), two amplitudes (15 and 25 ankle angle changes) and at two different stimulation frequencies (30 Hz and 85 Hz). The resultant ankle joint moments were calculated through inverse dynamics. Pennation angle and fascicle length of the m. gastrocnemius medialis at rest and during contractions were measured using ultrasonography. The corresponding ankle moments, kinematics and changes in muscle architecture were analysed at seven time intervals. A three-way analysis of variance (amplitude · velocity · stimulation frequency) and post-hoc test with Bonferroni correction were used to check the amplitude, velocity and stimulation level related effects on moment enhancement (a = 0.05). The results show an ankle joint moment enhancement after shortening–stretch cycles influenced by muscle architectural changes. We found 2–3% isometric ankle joint moment enhancement at steady state, 1.5–2.0 s after the shortening–stretch cycle. However, the observed alteration in muscle architecture after the imposed perturbation, could lead to an underestimation (1–3%) of joint moment enhancement due to the force–length relationship of the triceps surae. Furthermore, the enhancement observed was independent of the shortening–stretch amplitude, velocity and stimulation frequency. 2007 Elsevier Ltd. All rights reserved. Keywords: Force enhancement; Force depression; Muscle architecture; Muscle mechanics; Triceps surae
1. Introduction It is accepted that following active muscle stretching or shortening, phenomena known as force enhancement and force depression can be present (Abbott and Aubert, 1952; Edman, 1978a,b; Edman et al., 1982; Marechal and Plaghki, 1979). These phenomena are present in voluntary contractions (Lee and Herzog, 2002) during both, maximal and submaximal activation level conditions (Oskouei and Herzog, 2006). Force depression has been shown to increase with increasing shortening magnitude (Marechal
*
Corresponding author. Fax: +49 221 4971598. E-mail address: [email protected] (A. Arampatzis).
1050-6411/$ - see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2007.08.005
and Plaghki, 1979), with decreasing shortening velocities (Abbott and Aubert, 1952; De Ruiter et al., 1998), and with increasing activation levels (De Ruiter et al., 1998). Force enhancement becomes greater with increasing stretch amplitudes (Edman, 1978a,b; Edman et al., 1982), has been shown to be stretch velocity dependent in the whole muscle (Abbott and Aubert, 1952), and activation level dependent for voluntary contractions (Oskouei and Herzog, 2006). However, during daily activities muscles very rarely undergo simple stretches or shortenings but rather stretch–shortening or shortening–stretch cycles. To the best of our knowledge there have been no studies reported in the literature to date investigating history dependent phenomena of force production such as force depression or force enhancement after stretch–shortening or shorten-
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ing–stretch cycles in human muscles in vivo. The existing reports on force depression or force enhancement after stretch–shortening or shortening–stretch cycles all were obtained from animal models (Herzog and Leonard, 2000; Lee et al., 2001; Rassier and Herzog, 2004b). Herzog and Leonard (2000) reported that in cat soleus muscle the isometric forces following shortening–stretch cycles of equal magnitude were the same as those obtained for purely isometric contractions. They concluded that when the amounts of shortening and stretch are equal, the net result is no force enhancement. On the other hand, Lee et al. (2001) found force enhancement greater than 1% of the reference isometric force after shortening–stretch cycles of equal magnitude. Additionally Rassier and Herzog (2004b) reported force enhancements between 5% and 10% in single skeletal muscle fibres after different shortening–stretch cycles. Generally it is believed that the magnitude of shortening preceding stretch affects the force enhancement in a dose dependent manner, i.e. when the amount of shortening increased, the force enhancement decreases (Herzog and Leonard, 2000; Herzog et al., 2003). The architectural complexity of the muscles analysed during human studies (m. adductor pollicis, m. quadriceps femoris) create essential difficulties to translate the generated joint angular displacement into accurate muscle lengths (De Ruiter et al., 2000). Furthermore, it is well known that during voluntary contractions in vivo despite careful external fixations it is not possible to completely prevent any motion of the joint relative to the dynamometer (Magnusson et al., 2001; Muramatsu et al., 2001). More recently it has been reported that even for a single isometric plantar flexion (Arampatzis et al., 2005) or knee extension (Arampatzis et al., 2004) contraction trial, at identical joint moments the joint angles could differ causing significant changes in muscle architecture (Karamanidis et al., 2005). Differences in muscle architecture after shortening or stretching in relation to the reference contraction can affect the moment generation independently of force depression or force enhancement phenomena (due to the force–length relationship of the muscle). In general, for a proper interpretation of history effects on muscle contraction, information about the actual fascicle length is necessary. The purpose of this study was to examine the moment generation of the human plantar flexors and the architecture of the m. gastrocnemius medialis (GM) during and after shortening–stretch cycles in vivo. Based on the current literature (Arampatzis et al., 2004, 2005; Herzog and Leonard, 2000; Lee et al., 2001; Rassier and Herzog, 2004b) we expected a moment enhancement after shortening–stretch cycles in the triceps surae muscles and an influence on moment enhancement by the muscle architecture. We further expected an amplitude, velocity and activation effect on moment enhancement after the shortening–stretch cycle. Therefore, we investigated shortening–stretch contractions of equal magnitudes in the human plantar flexor muscles by manipulating the shortening–stretch amplitude, velocity and electrical muscle stimulation intensity.
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2. Methods 2.1. Participants Fourteen male volunteers participated in the study (age: 30 ± 7 years, height: 177 ± 7 cm, body mass: 80 ± 9 kg). The participants were all recruited from students of the German Sport University Cologne and gave their informed consent to participate in the experiment. 2.2. Experimental protocol The participants performed a series of electro-stimulated shortening–stretch plantar flexion contractions in three different measuring sessions. The subjects were seated on a custom-made dynamometer with the right ankle dorsiflexed at 80 (tibia perpendicular to the sole, ankle angle 90) and the knee flexed at 120 (knee fully extended 180). Inextensible Velcro straps were used to fix the right leg and the foot to the dynamometer. In addition, the thigh and the trunk of the subjects were fixed on the dynamometer chair with inextensible belts (Fig. 1). After a warm up period, consisting of 5 min of submaximal electro-stimulation and 2–3 submaximal voluntary plantar flexions, the subjects performed one maximal voluntary contraction (MVC). After this, the maximal tolerated electro-stimulation intensity (mA) was determined at the subjective limit of each subject. The operator manually increased the stimulation intensity of the electro-stimulator with continuous subject feedback. The right triceps surae muscle of each participant was activated by means of a constant-voltage adjustable intensity electrical stimulator (Compex 2, Compex Me´dical SA, Switzerland) using monopolar biphasic compensated square wave pulses (85 Hz). The 85 Hz stimulation yielded a maximal isometric force response in the gastrocnemius medialis. Two carbon–rubber stimulation electrodes (4.5 · 7.5 cm) thinly coated with conductive gel, were secured onto the shaved and cleaned skin. The cathode was positioned midway across the medial and lateral heads of the gastrocnemius approximately 5 cm distal to the crease in the popliteal fossa. The anode was positioned at the soleus motor point, along the medial line directly below the belly of the medial and lateral gastrocnemius muscles. The motor point was identified by moving the electrode (anode) over the soleus muscle to find the position where the lowest stimulation intensity produced the largest response (muscle contraction). The duration of the electrical stimulation was 6 s. During this time the dynamometer first remained static, followed by a 25 or 15 plantar flexion (shortening), a 25 or 15 dorsiflexion (stretch) and finally static again. The ankle rotations (shortening–stretch cycles) were performed at three constant angular velocities (25/s: slow velocity; 50/s: medium velocity; 100/s: high velocity). The final isometric contraction induced by the electrical stimulation persisted for at least two seconds; between successive contractions there was a resting period of at least 2 min. The room temperature was monitored in all experiments: range 22–26.7 C, mean ± SD 24.4 ± 1.3 C. In the first session the participants performed the shortening– stretch cycles in all three angular velocities (25/s, 50/s and 100/ s) at constant shortening–stretch amplitude of 25 and by a stimulation frequency of 85 Hz, in a randomised order (Fig. 2). In the second session the experimental design was the same regarding the three angular velocities and stimulation frequencies as the first and only the constant shortening–stretch amplitude changed to
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15. In the third session we examined shortening–stretch cycles at all three angular velocities (25/s, 50/s and 100/s) with a stimulation frequency of 30 Hz (in contrast to the 85 Hz, a 30 Hz stimulation frequency resulted in a submaximal isometric force response of the triceps surae muscle). The shortening–stretch amplitude in the third session was 15. Between the three experimental sessions there was a break for at least three weeks. In addition at these three measuring sessions, in a later experiment, 10 of the participants performed a series of isometric electrostimulated contractions at four different ankle joint positions (80, 90, 100, 110) in order to determine the plantar flexors torque–angle relationship at both stimulation frequencies (submaximal: 30 Hz and maximal: 85 Hz) used during the main experiments. 2.3. Measurement of the ankle joint moment
Fig. 1. Experimental setup. A custom-made dynamometer was built for measuring the plantar flexion moment. The subjects were seated with the ankle dorsiflexed at 80 (tibia perpendicular to the sole = 90 ankle angle) and the knee flexed at 120 (knee fully extended = 180). Inextensible Velcro straps were used to fix the foot to the dynamometer’s footplate. In addition the thigh and the trunk of the subjects were fixed to the dynamometer chair with inextensible belts.
For measuring the plantar flexion moment, a custom-made dynamometer was built. It consisted of a Global Drive 9325 servo inverter (Lenze Drive Systems GmbH, Hameln Germany) coupled with a synchronous servo-motor MDSKS 017-13, 185 (Lenze Drive Systems GmbH, Hameln Germany) accessorised with a torque sensor type 8628 (Burster gmbh Co. KG, Gernsbach Germany, measuring range 0 ± 500 Nm). At the beginning of each experiment, the axis of rotation of the ankle was carefully aligned with the axis of rotation of the dynamometer. The axis of rotation of the ankle joint was defined to be parallel to the axis of the dynamometer passing through the midpoint of the line connecting both malleoli. During the contraction, the axes clearly shifted away from each other. This shift significantly influences the resultant joint moments (Arampatzis et al., 2005, 2006, 2007). In order to correct for this influence, the kinematics was recorded using the Vicon 624 system (Vicon Motion Systems, United Kingdom) with eight cameras operating at 250 Hz. During the plantar flexion the co-ordinates of 10 retro-reflective markers (radius 5 mm) fixed on the following positions were captured: tuber calcanei, lateral and medial malleolus, the most prominent points of the lateral and medial femoral condyles, trochanter major, forefoot on the pressure insole between the second and the third metatarsals, axis of the dynamometer and two markers on the footplate to define the line of force application (Fig. 1). The moments measured by the dynamometer were registered synchronously by the Vicon system at a sampling rate of 3750 Hz. To determine the centre of pressure under the foot a flexible pressure distribution insole (Pedar-system, Novel GmbH, Germany) operating at 99 Hz was used. The Pedar-system emitted an additional signal switching between 0 and 5 V every 10 frames, which was also registered by the Vicon unit to synchronise both measuring systems. To achieve a common frequency (3750 Hz) with the moment data, the kinematic and centre of pressure data were interpolated using quintic splines. The resultant moments at the ankle joint were calculated through inverse dynamics as described in detail in a previous publication (Arampatzis et al., 2007). 2.4. Measurement of muscle architecture
Fig. 2. Example comparison of the ankle joint moment obtained from one subject during the three shortening–stretch cycle velocities (low: 25/s, medium: 50/s, and high: 100/s) at 85 Hz stimulation frequency and 25 shortening–stretch amplitude.
A 7.5 MHz linear array ultrasound probe (Aloka SSD4000; 43 Hz) was used to visualise the muscle belly of the GM at rest and during the contractions. The ultrasound probe was placed above the GM muscle belly at about 50% of its length. The
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Fig. 3. Ultrasound image of the muscle gastrocnemius medialis with an overlaid graphical representation of a fascicle, the deep aponeurosis and the pennation angle a.
ultrasound images were digitally recorded via firewire on a notebook for further analysis. The video data (ultrasound sequences) were synchronised with the remaining data using a synchronisation box (Peak Performance Technologies, USA). The experiment leader manually triggered a TTL signal (0–5 V), which was overlaid on the video images and simultaneously captured by the Vicon system. The video data were analysed frame-by-frame using the Simi video analysis system (Simi Motion 6.1, SIMI Reality Motion Systems GmbH, Unterschleißheim Germany). The pennation angle of the GM was measured as the angle of insertion of one muscle fascicle into the deep aponeurosis. The fascicle length was defined as the length of the fascicular path between the insertions of the fascicle into the upper and deeper aponeuroses (Fig. 3). When the fascicle extended out of the acquired ultrasound image the length of the missing portion of the fascicle was estimated by linear extrapolation of both, the fascicular path and the aponeurosis (Arampatzis et al., 2006). 2.5. Data analysis Previous studies on history dependence of force production (Brown and Loeb, 2000; Cook and McDonagh, 1995; Edman, 1978a,b; Ettema et al., 1992; Herzog and Leonard, 2002; Lee and Herzog, 2002; Lee et al., 2000; Linari et al., 2000; Peterson et al., 2004; Ruiter et al., 2000) analysed force parameters at intervals located between 50 ms and 4.5 s after stretching or shortening movements. We quantify the plantar flexion moment at the plateau before the onset of the shortening–stretch cycle (I0) and at six time intervals (I1, I2, I3, I4, I5, I6) beginning at the end of the stretch and ending two minutes later (Fig. 4). At these same intervals ankle-, knee-, pennation-angles and fascicle lengths were determined (Fig. 5) and compared to each other. A three-way analysis of variance (amplitude · velocity · stimulation frequency) and post-hoc test with Bonferroni correction were used to check the amplitude, velocity and stimulation level related effects on moment enhancement after the shortening–stretch cycle. The level of significance was set at a = 0.05.
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Fig. 4. Analysed intervals of the ankle joint moment–time (I0–I6). Initial interval 0: average moment value during the 500 ms before starting the shortening. Interval I1 average value in the first 125 ms after stretch end. Interval I2: average value between 125 and 250 ms after stretch end. Interval I3: average value between 250 and 500 ms after stretch end. Interval I4: average value between 500 ms and 1.0 s after stretch end. Interval I5: average value between 1.0 and 1.5 s after stretch end. Interval 6: average value between 1.5 and 2.0 s after stretch end.
3. Results 3.1. Maximal electrical stimulation frequency (85 Hz) At the plateau of the electro-stimulated contractions prior to the beginning of the shortening–stretch cycles (I0) the ankle joint moment was about 43% of the moment reached during the maximal voluntary contraction. The corresponding actual ankle angle at this time was 100.7 ± 3.0 (mean ± SD, Table 1). At I0 fascicle length and pennation angle of the GM muscle were 21.4 ± 3.4 mm and 55.8 ± 4.5, respectively (mean ± SD, Table 1). The architecture of the GM muscle after the shortening– stretch cycle differed significantly (p < 0.05) from that observed at the initial isometric contraction. For all examined intervals after the shortening–stretch cycle, the ratio of the pennation angle to the I0 was higher than 1.0 (Fig. 6), and below 1.0 for the fascicle length (Fig. 6) indicating that after the shortening–stretch cycle the pennation angles where greater and the fascicle lengths shorter than at I0. However, within the intervals I3–I6 the fascicle length values showed no significant differences (p > 0.05) indicating a steady state in the GM architecture (Fig. 6). In a similar manner to the GM architecture, the ankle angle was greater at the examined intervals after the shortening– stretch cycle than at the initial isometric contraction (Fig. 6). At all studied shortening–stretch cycle velocity combinations and at all intervals (I1–I6) the ankle joint moment ratios were statistically significant greater than at I0 (p < 0.01) (Fig. 6). At I1 (0–0.125 s after stretch) the mean ± SD of the moment ratio was 1.144 ± 0.057. This value decreased to 1.026 ± 0.046 at I6 (1.5–2 s after stretch).
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Fig. 5. Footplate angle-, ankle joint moment-, gastrocnemius medialis pennation angle- and gastrocnemius medialis fascicle length–time histories during the shortening–stretch cycle at 30 Hz electrical stimulation and 25 footplate amplitude. Data from one trial.
3.2. Submaximal electrical stimulation frequency (30 Hz) Under submaximal electrical stimulation frequency conditions the mean ± SD torque was more than 10% lower than at the maximal (85 Hz) condition (p < 0.05). The torque at I0 was 43.5 ± 8.9 Nm. Similarly, the ankle angle, the fibre length and the pennation angle at I0 were significantly different (p < 0.05) from the 85 Hz stimulation frequency condition (Table 1). Nevertheless after the shortening– stretch cycle the overall behaviour was similar to that observed at the 85 Hz stimulation condition. For the 30 Hz stimulation frequency the architecture of the GM muscle and the ankle angle following shortening–stretching cycles were again significantly different than those at the I0. At all examined intervals (I1–I6) the fascicle lengths were shorter than at the beginning (see ratios in Fig. 7), whereas the pennation and the ankle angles were greater (Fig. 7). The fascicle length of the GM showed no significant differences within the intervals I3–I6 (p > 0.05), indicating a steady state in the GM architecture (Fig. 7). As we Table 1 Ankle joint moment (interval I0) and corresponding actual ankle angle, for the 85 Hz electro-stimulation frequency compared to the values reached during 30 Hz Parameter
85 Hz
30 Hz
Joint moment (Nm) Ankle angle () Fascicle length (mm) Pennation angle ()
48.5 ± 9.0 100.7 ± 3.0 21.4 ± 3.4 55.8 ± 4.5
43.5 ± 8.9* 99.6 ± 3.9* 23.7 ± 3.9* 52.1 ± 5.4*
The same comparison is made for the architectural characteristics (fascicle length, pennation angle) of the m. gastrocnemius medialis during the maximal isometric force production (means ± SD). * Statistically significant differences between 85 and 30 Hz electro-stimulation frequency (p < 0.05).
observed at the stimulation frequency of 85 Hz, also at 30 Hz the ankle joint moment ratios were significantly higher after the shortening–stretch cycle (I1–I6) than before (I0) (p < 0.01) (Fig. 7). We found a stimulation frequency dependent behaviour for the first 500 ms after the shortening–stretch cycle (intervals I1–I3) where the joint moment ratios were lower for the 30 Hz than for the 85 Hz stimulation. 4. Discussion The purpose of this study was to examine the moment generation of the human plantar flexors and the architecture of the m. gastrocnemius medialis before and after shortening–stretch cycles in vivo. To our knowledge this was the first study showing that after shortening–stretch cycles an ankle joint moment enhancement could be present, and that in vivo this enhancement may be influenced by muscle architectural changes. We found 2–3% isometric ankle joint moment enhancement at steady state, 1.5–2.0 s after the shortening–stretch cycle. However, the observed alteration of the architectural characteristics of the muscle after the imposed perturbation, could lead to an underestimation of the ankle joint moment enhancement due to the force–length relationship of the triceps surae. Furthermore, for the first time it was found that the ankle joint moment enhancement observed after the shortening–stretch cycle was independent of the shortening–stretch amplitude, velocity and stimulation frequency. Although force enhancement after stretch and force depression after shortening have been intensively studied, the literature reports concerning history dependent phenomena such as force depression or force enhancement after stretch–shortening or shortening–stretch cycles are
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Fig. 6. Mean ± SD of several ratios during the 85 Hz electrical stimulation frequency at 15 and 25 footplate motion amplitude at the seven different analysed intervals (n = 10). Left column: values at 15 footplate motion amplitude (pennation angle, fascicle length, ankle angle, joint moment). Right column: values at 25 footplate motion amplitude. (*) Statistically significant differences to interval I0 (p < 0.05).
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Fig. 7. Mean ± SD of several ratios during the 30 Hz electrical stimulation frequency and 15 footplate motion amplitude at the seven different analysed intervals (n = 10). Top: pennation angle (left) and fascicle length (right). Bottom: ankle angle (left) and ankle joint moment (right). (*) Statistically significant differences to interval I0 (p < 0.05).
limited (Herzog and Leonard, 2000; Lee et al., 2001; Rassier and Herzog, 2004b). We found that after shortening– stretch cycles (1.5–2.0 s, interval I6) the isometric plantar flexion moments were enhanced by 2–3% in relation to the initial isometric moment. The results of the present study also show that after the shortening–stretch cycle ankle angle, fascicle length and pennation angle are significantly different from the initial isometric condition (p < 0.05). At all examined intervals after the shortening– stretch cycle the ankle angles as well as the pennation angles showed higher values, whereas the fascicle lengths were lower than at the initial interval I0. Consequently, the differences in leg geometry (higher ankle angle) after the shortening–stretch cycle influence the architecture of the GM muscle–tendon unit and possibly also the architecture of the soleus and gastrocnemius lateralis muscles (the length of all these three muscles is ankle angle dependent). We examined the moment generation of the plantar flexor muscles before and after the shortening–stretch cycle at an actual ankle joint angle of 100 ± 3 and a knee joint angle of 118 ± 5 (real ankle and knee joint angles determined by the kinematic analysis). It has been reported that at this position the muscles of the triceps surae muscle–tendon unit operate on the ascending limb of the force–length relationship (Herzog et al., 1991). Thus shorter fascicle lengths
of the GM after the shortening–stretch cycle would reduce the force potential of the muscle as compared to the initial condition. This in turn would mean that the moment enhancement found in our experiment was underestimated. In order to estimate the effect of these differences in ankle angle between the initial condition and time interval I6 we examined the moment–ankle angle relationship using both electro-stimulation frequencies (Fig. 8). The data plotted in Fig. 8 indicate that the moment enhancement 1.5–2.0 s after the shortening–stretch cycle is underestimated by 1–3%. Although the exact underlying mechanisms of force depression after shortening or force enhancement after stretch in skeletal muscles are at the moment in debate (Granzier and Pollack, 1989; Herzog et al., 2003; Sugi and Tsuchiya, 1988), experimental data indicate that mechanisms related to cross-bridge kinetics contribute to force depression as well as to force enhancement phenomena (Herzog et al., 2006, Herzog and Leonard, 1997, 2002, 2005; Rassier and Herzog, 2004a). In addition a ‘‘passive’’ force enhancement component, especially for stretches performed on the descending limb of the force–length relationship, has also been proposed (Herzog and Leonard, 2002). However, independent of the mechanisms underlying history dependent phenomena in muscle contraction, it is
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accepted that force depression increases with increasing shortening magnitude (Bullimore et al., 2007; Herzog and Leonard, 1997; Marechal and Plaghki, 1979) and decreases with increasing shortening velocity (De Ruiter et al., 1998; Meijer et al., 1997). The latter phenomenon is possibly associated to the decrease in force generation during the contraction at higher shortening velocities (De Ruiter et al., 1998; Leonard and Herzog, 2005). It is also accepted that the steady-state force enhancement after stretch increases with increasing magnitude of stretch being independent of stretch velocity (De Ruiter et al., 2000; Edman, 1978a,b; Lee and Herzog, 2002). Recent studies showed that the stretch magnitude affects primarily the ‘‘passive’’ component of the force enhancement and that the so called ‘‘active’’ component (difference between steady-state force enhancement and ‘‘passive’’ component) (Herzog and Leonard, 2002) is not influenced by the magnitude of the stretch (Bullimore et al., 2007; Schachar et al., 2004). In our study the shortening–stretch contractions were performed on the ascending limb of the force–length relationship of the triceps surae muscles (Fig. 8). Earlier studies reported no evidence of passive force enhancement in the ascending limb of the force–length relationship neither in whole muscle preparations (Herzog and Leonard, 2002) nor in single fibres of skeletal muscles (Peterson et al., 2004). This indicates that the ‘‘passive’’ component of the steady-state force enhancement after the shortening–stretch cycle in our experiments should have a negligible contribution to the observed moment enhancement (Herzog, 2001; Herzog and Leonard, 2002; Peterson et al., 2004). Based on the literature reports stating that (a) the magnitude and velocity of shortening affect the force depression (Herzog and Leonard, 1997; Marechal and Plaghki, 1979), (b) the ‘‘active’’ component of the force enhancement is not affected by the magnitude and velocity of stretching (Bullimore et al., 2007; Schachar et al., 2004) and (c) during shortening–stretch cycles the force depression and force enhancement are additive (Lee et al., 2001) we expected the shortening/stretch magnitude and velocity to influence the moment enhancement after the examined shortening– stretch cycles. Furthermore, the moment values at the end of the shortening showed a velocity effect leading to lower values when increasing the angular velocities of the footplate, indicating an influence of the shortening velocity on the mechanisms of force depression during shortening (De Ruiter et al., 1998; Leonard and Herzog, 2005). Nevertheless we did not find any influence of shortening or stretching amplitude or velocity of equal magnitudes on the moment enhancement after shortening–stretch cycles in physiological force and length ranges of the triceps surae muscles. The results illustrate that the mechanisms responsible for force depression and force enhancement during shortening–stretch cycles at the ascending limb of the force–length relationship of the triceps surae muscles are insensitive to the amplitude or velocity of shortening/stretch of equal magnitudes on moment enhancement after the contraction. In agreement with previous works (De Ruiter et al., 2000),
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Fig. 8. Ankle joint moment–angle relationship for the 85 Hz and the 30 Hz electrical stimulation frequencies (mean ± SD). At both frequencies the muscle was tested in the ascending limb of its force–length relationship. I0: ankle angle at the initial interval; I6: ankle angle 1.5–2 s after the shortening–stretch cycle.
we found that after a shortening–stretch cycle the moment enhancement at the steady state (intervals I4–I6) was not influenced by changes in stimulation frequency. Our results also match those of De Ruiter et al. (2000) in that the reduction of the activation (stimulation frequency) produced significantly lower moment ratios in the first 500 ms (I1–I3) (p < 0.05) (see Fig. 7). In summary, we demonstrated a moment enhancement (2–3%) at the high and low frequency of electro-stimulated human triceps surae muscle in vivo after shortening–stretch cycles. The observed moment enhancement was not affected by the amplitude or velocity of shortening–stretching of equal magnitudes using maximal and submaximal electro-stimulation intensities. Finally, the analysis of the GM architecture during the shortening–stretch cycle, suggest an underestimation (1–3%) of the observed moment enhancement. This strengthens the need to consider the muscle architecture when studying history dependent phenomena of muscle force generation after shortening or stretching contractions in vivo. References Abbott BC, Aubert XM. The force exerted by active striated muscle during and after change of length. J Physiol 1952;117:77–86. Arampatzis A, Karamanidis K, De Monte G, Stafilidis S, Morey-Klapsing G, Bru¨ggemann GP. Differences between measured and resultant joint moments during voluntary and artificially elicited isometric knee extension contractions. Clin Biomech (Bristol, Avon) 2004;19:277–83. Arampatzis A, Morey-Klapsing G, Karamanidis K, De Monte G, Stafilidis S, Bru¨ggemann GP. Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J Biomech 2005;38:885–92. Arampatzis A, Karamanidis K, Stafilidis S, Morey-Klapsing G, De Monte G, Bru¨ggemann GP. Effect of different ankle- and knee-joint positions on gastrocnemius medialis fascicle length and EMG activity during isometric plantar flexion. J Biomech 2006;39:1891–902. Arampatzis A, De Monte G, Morey-Klapsing G. Effect of contraction form and contraction velocity on the differences between resultant and measured ankle joint moments. J Biomech 2007;40:1622–8.
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Adamantios Arampatzis received his PhD at the German Sport University of Cologne in 1995. He is the head of the research group focusing on the neuromechanics of the human muscoloskeletal system at the Institute of Biomechanics and Orthopaedics from the German Sport University Cologne. Among his research interests are the adaptation potential of the human system to physical activity and the influence of the neuromechanical capacity of the muscoloskeletal system on motor task behaviour during daily and sport activities.