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Force depression following muscle shortening in sub-maximal voluntary contractions of human adductor pollicis
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Journal of Biomechanics 40 (2007) 1–8 www.elsevier.com/locate/jbiomech www.JBiomech.com
Force depression following muscle shortening in sub-maximal voluntary contractions of human adductor pollicis Elissavet N. Rousanogloua, Ali E. Oskoueib, Walter Herzogb, a
Faculty of Physical Education & Sport Science, National & Kapodistrian University of Athens, Ethnikis Antistasis 41, Daphne, 172-37, Greece Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, 2500 University Drive NW, Calgary, AB, Canada T2N 1N4
b
Accepted 6 December 2005
Abstract Mechanical properties of skeletal muscles are often studied for controlled, electrically induced, maximal, or supra-maximal contractions. However, many mechanical properties, such as the force–length relationship and force enhancement following active muscle stretching, are quite different for maximal and sub-maximal, or electrically induced and voluntary contractions. Force depression, the loss of force observed following active muscle shortening, has been observed and is well documented for electrically induced and maximal voluntary contractions. Since sub-maximal voluntary contractions are arguably the most important for everyday movement analysis and for biomechanical models of skeletal muscle function, it is important to study force depression properties under these conditions. Therefore, the purpose of this study was to examine force depression following sub-maximal, voluntary contractions. Sets of isometric reference and isometric-shortening-isometric test contractions at 30% of maximal voluntary effort were performed with the adductor pollicis muscle. All reference and test contractions were executed by controlling force or activation using a feedback system. Test contractions included adductor pollicis shortening over 101, 201, and 301 of thumb adduction. Force depression was assessed by comparing the steady-state isometric forces (activation control) or average electromyograms (EMGs) (force control) following active muscle shortening with those obtained in the corresponding isometric reference contractions. Force was decreased by 20% and average EMG was increased by 18% in the shortening test contractions compared to the isometric reference contractions. Furthermore, force depression was increased with increasing shortening amplitudes, and the relative magnitudes of force depression were similar to those found in electrically stimulated and maximal contractions. We conclude from these results that force depression occurs in sub-maximal voluntary contractions, and that force depression may play a role in the mechanics of everyday movements, and therefore may have to be considered in biomechanical models of human movement. r 2006 Elsevier Ltd. All rights reserved. Keywords: Muscle properties; Force–length relationship; Force enhancement; Muscle activation
1. Introduction It has been known for a long time (Abbott and Aubert, 1952) that the steady-state isometric force following shortening of an activated muscle is smaller than the corresponding force obtained in a purely isometric contraction (Edman et al., 1993). This so Corresponding author. Tel.: +1 403 220 8525; fax: +1 403 220 2414. E-mail address: [email protected] (W. Herzog).
0021-9290/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2005.12.002
called ‘‘force depression’’ (Herzog, 1998) increases with increasing shortening magnitude (Mare´chal and Plaghki, 1979), increasing shortening force (Herzog and Leonard, 1997), decreasing shortening speed (Abbott and Aubert, 1952), and increasing mechanical work (Herzog et al., 2000). Furthermore, force depression is associated with a decrease in muscle stiffness (Sugi and Tsuchiya, 1988; Lee and Herzog, 2003), thereby suggesting that the loss of force following shortening is associated with a decrease in the number of attached cross-bridges (Mare´chal and Plaghki, 1979; Herzog,
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1998). Despite an abundance of descriptive literature on the topic, two basic problems have eluded satisfactory explanation. First, the detailed mechanisms underlying this phenomenon remain unknown (Rassier and Herzog, 2004) and second, it is not known whether force depression plays a functional role during normal, everyday, voluntary contractions. Until recently, all work on force depression had been conducted in isolated muscle or fibre preparations that were activated artificially through electrical stimulation (Herzog and Leonard, 1997; Morgan et al., 2000; Abbott and Aubert, 1952; Mare´chal and Plaghki, 1979; Edman et al., 1993). Few results are now available on force depression in human skeletal muscles that were either activated through electrical stimulation (De Ruiter et al., 1998; Lee and Herzog, 2003) or maximal voluntary contraction (MVC) (Lee et al., 1999; Lee and Herzog, 2003; De Ruiter and de Haan, 2003). These studies confirmed that under these experimental conditions, force depression following shortening of the activated muscles exists very much in the same way as it does in isolated, artificially stimulated preparations (De Ruiter and de Haan, 2003; Lee and Herzog, 2002). However, normal, everyday movements occur at submaximal force levels, with a continuously changing activation. Under sub-maximal conditions, mechanical properties may be quite different from those observed in maximally contracting muscles. For example, the shape of the force–length relationship is greatly affected by the level of activation, and there is a shift of the peak force to greater lengths with decreasing levels of activation (e.g., Rack and Westbury, 1969; Close, 1972; Rassier et al., 1998). Therefore, if force depression only occurs on the descending, but not the ascending limb of the force–length relationship, as proposed by supporters of the so-called ‘‘sarcomere length non-uniformity theory’’, a change in the shape of the force–length relationship would also affect the region of muscle lengths where force depression would be observed (Morgan et al., 2000). Therefore, it is perceivable that force depression may differ from that observed in maximally or electrically elicited muscle contractions. The purpose of this study was to test if there is force depression following sub-maximal, voluntary contractions in human skeletal muscle. In order to achieve this goal, force or activation were kept constant while the uncontrolled variable was observed for purely isometric reference contractions and for contractions involving sub-maximal active shortening. We chose the human adductor pollicis group for this investigation, as it is the best studied human muscle in this area of research (Lee and Herzog, 2003; De Ruiter et al., 1998; De Ruiter and de Haan, 2003; De Ruiter et al., 2000; Lee and Herzog, 2002; Oskouei and Herzog, 2005). It shows force depression for artificially stimulated and MVC (De Ruiter et al., 1998; Lee and Herzog, 2003; De Ruiter and de Haan, 2003), and
its force and activation can be quantified easily (De Ruiter and de Haan, 2003; De Ruiter et al., 1998; Lee and Herzog, 2003; Cafarelli and Bigland-Ritchie, 1979). Based on previous work (De Ruiter et al., 1998; Edman et al., 1993; Herzog and Leonard, 1997; Herzog et al., 2000; Lee and Herzog, 2003; Mare´chal and Plaghki, 1979), we hypothesized that force depression is caused by a stress-induced inhibition of cross-bridge attachments in the actin–myosin overlap zone that is newly formed during shortening. If so, we would expect force depression to occur during all sub-maximal voluntary contractions, and also expect that force depression would increase with increasing magnitudes of shortening, and the absolute magnitude of force depression would be smaller for sub-maximal compared to maximal contractions.
2. Methods 2.1. Subjects A total of 45 subjects (28 males and 17 females, 22–48 years) with no history of neuromuscular disorder and injury to the left hand gave free written informed consent to participate in one of the four test protocols comprising this study. The first test (n ¼ 10 male subjects) was aimed at determining the variability in steady-state isometric force (activation) for a given, constant level of sub-maximal activation (force). The remaining three tests were all aimed at establishing if there was force depression following sub-maximal voluntary shortening contractions of the adductor pollicis group. In the second test (n ¼ 8, 4 males and 4 females), activation was kept constant while force was measured for isometric reference contractions and for experimental shortening contractions over a 301 thumb adduction angle. The third test (n ¼ 11, 6 males and 5 females) was identical to the second one, except that force was controlled at a sub-maximal level while activation was measured. Finally, the fourth test (n ¼ 16, 8 males and 8 females) was identical to the second one, except that shortening was produced over 101, 201, and 301 thumb adduction. All experimental procedures were approved by the Conjoint Ethics Committee of the University of Calgary. 2.2. Apparatus A custom-designed dynamometer, which measures thumb adduction force via a set of calibrated strain gauges arranged in a full Whealstone bridge configuration, was used for all testings. It measures the thumb angle at the carpometacarpal joint using an analogue encoder and a goniometer. This apparatus has been described in detail elsewhere (Lee and Herzog, 2002).
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2.3. Experimental settings The left hand was used for testing and was immobilized with a reusable clinical cast (Ezeform, Rehabilitation Division, Smith & Nephew Inc., Germantown, WI, USA) in a neutral position. Immobilization restricted the movement of the wrist and fingers, except for the thumb. After immobilization, subjects sat on an adjustable chair with the shoulder slightly abducted and the elbow flexed 901. The forearm was placed in a V-shaped metal plate, and was secured with velcro straps. The centre of rotation of the motor was aligned with the carpometacarpal joint. An aluminium rod was placed horizontally between thumb and index fingers. By placing the distal end of the thumb on the auxiliary piece attached to the aluminium rod, thumb movement was restricted to the frontal plane (Lee and Herzog, 2002, 2003). Before testing, the range of motion during thumb abduction – adduction was tested carefully for each subject. The lowest adducted angle was defined as 01. The thumb was then abducted to 301 (tests 1–3) and the desired starting angle (301, 201, 101) in test 4. Thumb angles were defined to increase with abduction. 2.4. Muscle activation measurements Adductor pollicis activation was measured using surface electromyography (EMG). The medial aspect of the palmar side of the hand and the posterior side of the thumb were cleaned with alcohol. A pair of surface electrodes (Ag/AgCl, Ref. 01-7545 ConMed Corporation, UTICA, NY, USA) was placed on the palmar side of the hand over the adductor pollicis. One electrode was placed close to the base of the proximal phalanx, the other one over the middle of the third metacarpal bone. The inter-electrode distance was 2.370.1 cm.The reference electrode was placed on the posterior bony side of the thumb and the inter-electrode impedance was measured and confirmed to be less than 5 kO in all measurements. EMG signals were amplified ( 1000) no further than 10 cm from the recording site and they were band-pass filtered (10 and 1000 Hz). EMG signals were collected at a sampling frequency of 3000 Hz. A linear envelope of the EMG signal was obtained by fullwave rectifying and smoothing the EMG using a time window of 400 ms sliding average of the rectified signal (Medical Engineering Systems and Ergonomics, Aachen, Germany).
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which consisted of two sub-protocols, A and B, comprising ten sub-maximal, voluntary, isometric trials (5 s) each. Subjects were asked to perform three maximal voluntary thumb adductor contractions at a thumb abduction angle of 01 with a 2-min (minimum) interval between contractions. The average of three maximal voluntary efforts was taken as the MVC and used to calculate 30% of MVC. In sub-protocol A (activation control), subjects were asked to match an average EMG trace on an oscilloscope that corresponded to 30% of the average EMG measured during maximum voluntary contraction. While doing so, the corresponding isometric force was measured. In sub-protocol B (force control), subjects were asked to match a force trace on an oscilloscope that corresponded to 30% of the maximum voluntary contraction force. While doing so, the corresponding average EMG was measured. 2.5.2. Tests 2– 4 Force depression for sub-maximal voluntary contractions was measured using three separate tests. In all the tests, subjects (n ¼ 8, n ¼ 11 and n ¼ 16 for tests 2, 3, and 4, respectively) were asked to perform a number of trial sets. Each set consisted of an isometric reference contraction and a corresponding isometric-shorteningisometric test contraction. Reference contractions were performed at a thumb angle of 01 (fully adducted thumb) and subjects were asked to match a reference line corresponding to an EMG trace of 30% of MVC (tests 2 and 4, Fig. 1) or a 30% MVC force trace (test 3, Fig. 2). Test contractions consisted of an isometric contraction at 301 of thumb abduction (tests 2 and 3) and at 101, 201, 301 of thumb abduction randomized across subjects (test 4), followed by a shortening contraction to 01, and a subsequent isometric contraction at the 01 angle while matching the corresponding sub-maximal force or average EMG traces (Figs. 1 and 2). The shortening speed for all test contractions was 101/s. Isometric reference contractions were held for a minimum of 12 s, so as to have the same duration of contraction as the isometric-shortening-isometric test contractions. In the experimental tests, contractions were maintained for a minimum of 4 s following the shortening phase, to ensure that all transient force and EMG responses had subsided and a steady-state force and EMG response had been reached when force/EMG measurements were made. 2.6. Data collection and analysis
2.5. Experimental tests 2.5.1. Test 1 The first step of this study was to determine whether sub-maximal voluntary contractions of human adductor pollicis could be performed with minimum variability in EMG and force. Ten male subjects completed a protocol
Thumb adduction forces, thumb angles, and EMG signals were recorded simultaneously at a sampling frequency of 3000 Hz. Mean isometric force and muscle activation were determined for a 2 s period after steadystate force or EMG had been reached in the test contractions (Figs. 1 and 2). Then, the corresponding
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Fig. 1. Example of average (full-wave rectified and smoothed) EMG (AEMG (A), raw EMG (B), thumb adduction force (C), and metacarpophalangeal joint angle (D) as a function of time during 30% of maximal voluntary contractions (MVC) of human adductor pollicis for an isometric reference and an isometric-301 shorteningisometric test contraction. Subjects were asked to control activation (activation control) at 30% MVC (see Methods). Isometric reference force (F Iso ref) was measured for a 2-s period in the final, steady-state part (labelled by the horizontal dotted arrow in C) for comparison with the corresponding values obtained from the isometric contractions following active shortening (F Iso short). Contractions were maintained for a minimum of 4 s following the shortening phase, to ensure that all transient force had subsided and a steady-state force had been reached. The difference between the isometric reference and shortening test force was defined as force depression. AEMG Iso ref, isometric reference average EMG; AEMG Iso short, isometric shortening average EMG; Raw EMG ref, reference raw EMG; Raw EMG short, isometric shortening raw EMG.
phase in the isometric reference contraction was located and the mean isometric force and muscle activation were determined. Force depression following muscle shortening (tests 2 and 4) was determined by subtracting the mean steadystate force of the shortening test contraction from the corresponding force of the isometric reference contraction. Possible increases in muscle activation following muscle shortening (test 3) were determined by subtract-
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Fig. 2. Example of thumb adduction force (A), raw (B), AEMG (C), and metacarpophalangeal joint angle (D) as a function of time during 30% of maximal voluntary contractions of human adductor pollicis for an isometric reference and an isometric-301 shortening-isometric test contraction. Muscle force was kept constant (force control) throughout the contractions (see Methods). Isometric reference EMG (AEMG Iso ref) was measured for a 2-s period in the final, steady-state part (labelled by the horizontal dotted arrow in C) for comparison with the corresponding values obtained from the isometric contractions following active shortening (AEMG Iso short). Contractions were maintained for a minimum of 4 s following the shortening phase, to ensure that all transient EMG responses had subsided and a steadystate EMG response had been reached. The difference in activation between the isometric reference and shortening test force was defined as EMG increase. F Iso ref, isometric reference force; F Iso short, isometric force after shortening; Raw EMG ref, reference raw EMG; Raw EMG short, isometric shortening raw EMG.
ing the steady-state average EMG of the shortening test contractions from the corresponding values of the isometric reference contractions. 2.7. Statistical analysis Differences in steady-state isometric force and average EMG were compared for the isometric reference contractions and the shortening test contractions, three
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45 40 35 Force (N)
shortening amplitudes (101, 201, and 301; test 4), and the interaction between shortening amplitude and contraction type (test 4 only). Repeated measures ANOVA and Bonferroni post hoc comparisons were used for statistical analysis. Values are presented as means71SE. All tests were performed at a level of significance of a ¼ 0:05.
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3.2. Test 2 (force depression, 301 shortening, activation control) We found a significant 2173% steady-state force depression (po0:05) following 301 of shortening of the adductor pollicis during activation-controlled, sub-maximal voluntary contractions (Fig. 4A). This result was observed consistently for all eight subjects. The mean average EMG did not differ significantly between the isometric reference and the shortening test contractions. 3.3. Test 3 (force depression, 301 shortening, force control) There was a significant increase (po0:05) in steadystate average EMG (1873%) in the force-controlled 301
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Fig. 3. Mean (SE) coefficients of variation of average EMG (white bars) and force (grey bars) in the activation control and the force control protocols of test 1 ðn ¼ 10Þ. Note that the variability of force and average EMG are similar (10%) for the activation and force control tests, respectively, while force can be controlled tighter than average EMG in the force control compared to the activation control protocol.
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When asked to perform isometric contractions with the adductor pollicis and control activation at 30% of that observed during MVC, force values across subjects varied by 972% (Fig. 3). Similarly, when asked to perform sub-maximal isometric contractions and match force at 30% of MVC, average EMG values across subjects varied by 1071% (Fig. 3).
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Fig. 4. Mean (SE) isometric sub-maximal thumb adduction force (A) in the isometric reference and the 301 shortening test contractions ðn ¼ 8Þ, and mean (SE) average EMG (B) for isometric reference and 301 shortening test contractions ðn ¼ 11Þ. Force is significantly smaller in the shortening test contractions compared to the isometric reference contractions when activation is controlled, indicating that there is a force depression during sub-maximal voluntary contractions (*po0.05). Conversely, average EMG is significantly greater for the test compared to the isometric reference contractions (*po0.05) in the tests with force control.
shortening contractions compared to the isometric reference contractions (Fig. 4B). The controlled mean force was the same for the shortening tests (3978 N) and the isometric reference contractions (3878 N). This result was observed consistently for all 11 subjects participating in test 3. 3.4. Test 4 (force depression; 101, 201, and 301 shortening; activation control) There was a significant effect (po0:05) of shortening amplitude on force depression during 30% of MVC submaximal, voluntary shortening of the adductor pollicis (Fig. 5). Mean force depression was significantly increased (po0:05) as shortening amplitude increased from 101 to 301 and from 201 to 301 (Fig. 5). Although there was a trend of increasing force depression from 101 to 201 of shortening, the difference was not statistically significant (Fig. 5). This result was observed consistently for all 16 subjects participating in test 4. The mean average EMG did not differ significantly between the isometric reference and the shortening test contractions for all three shortening amplitudes.
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Fig. 5. Mean (SE) force depression for 101 (white bar), 201 (grey bar), and 301 (black bar) shortening amplitudes, for activation controlled testing ðn ¼ 16Þ. Force depression was significantly increased when shortening amplitude increased from 101 to 301 and from 201 to 301 (*po0.05). The difference between 101 and 201 was not statistically significant.
4. Discussion We found steady-state isometric force depression for sub-maximal voluntary contractions for every subject. This is the first study to show that force depression exists not only for artificially elicited electrical contractions in isolated muscle and fibre preparations (Herzog and Leonard, 1997; Morgan et al., 2000; Abbott and Aubert, 1952; Mare´chal and Plaghki, 1979; Edman et al., 1993) and for human voluntary contractions at maximal effort (Lee et al., 1999; De Ruiter and de Haan, 2003; Lee and Herzog, 2003), but also for sub-maximal voluntary contractions. For controlled activation (at 30% of MVC), force depression was about 21%, 15%, and 11% for thumb adduction movements over a range of 301, 201, and 101, respectively (Fig. 5). These values are consistent with those observed for the adductor pollicis group at maximal voluntary (22%, 17%, and 12%, respectively) and electrically stimulated contractions (24%, 14%, and 8%, respectively) under otherwise identical conditions (Lee and Herzog, 2003). For controlled force (at 30% of MVC), average EMG following the shortening contractions was increased by 18% (Fig. 4B). This result is a further evidence of force depression for sub-maximal voluntary contractions and indicates that force depression in sub-maximal efforts may not be apparent, as it can be offset by an increase in muscle activation to compensate for the reduced force capabilities. It has been shown that force depression is directly related to the amount of muscle or fibre shortening (Mare´chal and Plaghki, 1979; Herzog and Leonard, 1997), the force during the shortening phase (Herzog and Leonard, 1997), and the mechanical work performed during the shortening phase (Herzog et al., 2000; De Ruiter et al., 1998). Based on these observations, a
possible mechanism for force depression is a stressinduced inhibition of cross-bridges in the actin–myosin overlap zone that is formed during shortening (Mare´chal and Plaghki, 1979). According to this mechanism, if a muscle is activated, the compliant thick and thin filaments are stretched (Goldman and Huxley, 1994; Higuchi et al., 1995; Huxley et al., 1994; Kojima et al., 1994; Nishizaka et al., 1995; Wakabayashi et al., 1994) and the angular alignment of cross-bridge to actin attachment site may be distorted (Daniel et al., 1998). The greater the stress during shortening, the greater the angular distortion, which causes the proposed inhibition of cross-bridge attachments in the newly formed overlap zone. If so, force depression would be expected following sub-maximal shortening contractions. However, since the force during shortening is decreased, one would expect the absolute amount of force depression to be decreased for sub-maximal compared to maximal effort contractions. This result is consistent with observations in cat soleus in which decreases in force during shortening caused a decrease in force depression (Herzog and Leonard, 1997). Force decrease was found here to be approximately 20% of the isometric reference force for sub-maximal contractions, and the average EMG was found to increase approximately 18% of the corresponding isometric reference EMG. The shortening tests were well within the range of thumb adduction movement and force, and we made no attempt at maximizing the magnitude of force depression. De Ruiter et al. (1998) found force depression values of 37% in the adductor pollicis when adducting the thumb by 381 at a speed of 61/s. We found isolated force depression values exceeding 50% in adductor pollicis (Lee and Herzog, 2003). Therefore, given the right conditions, force depression may be substantial. Nevertheless, we are not aware of functional muscle models that incorporate force depression in the analysis of human or animal movements. Many mechanical properties of muscles depend on the level of activation. For example, the force–length relationship changes shape, and peak forces are shifted to increased muscle length with decreasing levels of activation (e.g., Rack and Westbury, 1969; Close, 1972; Rassier et al., 1998). Also, force enhancement, following active muscle stretch, is often absent in subjects at submaximal levels of contraction, even though it is always present in maximal voluntary and electrically induced contractions (Oskouei and Herzog, 2005; Lee and Herzog, 2002). However, force depression was observed here in all subjects and for all test conditions. Although the detailed mechanisms underlying force depression are still debated, this study adds the result that, whatever the mechanism, the relative amount of force depression does not appear to be affected by the level of activation or force, and seems to occur to the same extent during voluntary and electrically induced contractions.
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There are several limitations that should be considered when interpreting the results of this study. First and foremost, forces and activations were associated with a variability of the uncontrolled parameter of about 10% (Fig. 3), i.e., when subjects were asked to match activation at 30% of MVC, the coefficient of variation in force was approximately 10%, and vice versa when subjects were asked to control force at 30% of MVC. Another limitation of this study was that activation of antagonistic muscles was not measured. The inherent assumption underlying our results is that antagonistic activity was the same for the isometric reference and the shortening test contractions. Also, the idea of using surface EMG as a measure of muscle activation may easily be criticized. However, we felt it was an adequate approach for a non-invasive human study, but the implicit assumptions are by no means trivial. Finally, the control of activation and force during the shortening phase was virtually impossible for any of the subjects. All we can say with certainty is that the effort during shortening was sub-maximal, but it could have deviated considerably from a 30% of MVC effort. However, despite these limitations, we feel confident that the general results reported here are valid and correct.
5. Conclusion We conclude that sub-maximal voluntary shortening causes a loss of isometric steady-state force compared to the force observed in a purely isometric reference contraction. Force depression is substantial, it exceeds the uncertainty associated with the experimental procedures, and it was observed consistently in all subjects participating in this study. Therefore, we think it is likely that force depression plays a role in normal everyday movements.
Acknowledgements The Natural Sciences and Engineering Research Council of Canada, the Canada Research Chair Programme, and Iran’s Ministry of Health are acknowledged for their assistance in this study.
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in frog skeletal muscle fibres. Journal of Physiology 407, 215–229. Wakabayashi, K., Sugimoto, Y., Tanaka, H., Ueno, Y., Takezawa, Y., Amemiya, Y., 1994. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophysical Journal 67, 2422–2435.
Journal of Biomechanics 40 (2007) 1–8 www.elsevier.com/locate/jbiomech www.JBiomech.com
Force depression following muscle shortening in sub-maximal voluntary contractions of human adductor pollicis Elissavet N. Rousanogloua, Ali E. Oskoueib, Walter Herzogb, a
Faculty of Physical Education & Sport Science, National & Kapodistrian University of Athens, Ethnikis Antistasis 41, Daphne, 172-37, Greece Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, 2500 University Drive NW, Calgary, AB, Canada T2N 1N4
b
Accepted 6 December 2005
Abstract Mechanical properties of skeletal muscles are often studied for controlled, electrically induced, maximal, or supra-maximal contractions. However, many mechanical properties, such as the force–length relationship and force enhancement following active muscle stretching, are quite different for maximal and sub-maximal, or electrically induced and voluntary contractions. Force depression, the loss of force observed following active muscle shortening, has been observed and is well documented for electrically induced and maximal voluntary contractions. Since sub-maximal voluntary contractions are arguably the most important for everyday movement analysis and for biomechanical models of skeletal muscle function, it is important to study force depression properties under these conditions. Therefore, the purpose of this study was to examine force depression following sub-maximal, voluntary contractions. Sets of isometric reference and isometric-shortening-isometric test contractions at 30% of maximal voluntary effort were performed with the adductor pollicis muscle. All reference and test contractions were executed by controlling force or activation using a feedback system. Test contractions included adductor pollicis shortening over 101, 201, and 301 of thumb adduction. Force depression was assessed by comparing the steady-state isometric forces (activation control) or average electromyograms (EMGs) (force control) following active muscle shortening with those obtained in the corresponding isometric reference contractions. Force was decreased by 20% and average EMG was increased by 18% in the shortening test contractions compared to the isometric reference contractions. Furthermore, force depression was increased with increasing shortening amplitudes, and the relative magnitudes of force depression were similar to those found in electrically stimulated and maximal contractions. We conclude from these results that force depression occurs in sub-maximal voluntary contractions, and that force depression may play a role in the mechanics of everyday movements, and therefore may have to be considered in biomechanical models of human movement. r 2006 Elsevier Ltd. All rights reserved. Keywords: Muscle properties; Force–length relationship; Force enhancement; Muscle activation
1. Introduction It has been known for a long time (Abbott and Aubert, 1952) that the steady-state isometric force following shortening of an activated muscle is smaller than the corresponding force obtained in a purely isometric contraction (Edman et al., 1993). This so Corresponding author. Tel.: +1 403 220 8525; fax: +1 403 220 2414. E-mail address: [email protected] (W. Herzog).
0021-9290/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2005.12.002
called ‘‘force depression’’ (Herzog, 1998) increases with increasing shortening magnitude (Mare´chal and Plaghki, 1979), increasing shortening force (Herzog and Leonard, 1997), decreasing shortening speed (Abbott and Aubert, 1952), and increasing mechanical work (Herzog et al., 2000). Furthermore, force depression is associated with a decrease in muscle stiffness (Sugi and Tsuchiya, 1988; Lee and Herzog, 2003), thereby suggesting that the loss of force following shortening is associated with a decrease in the number of attached cross-bridges (Mare´chal and Plaghki, 1979; Herzog,
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1998). Despite an abundance of descriptive literature on the topic, two basic problems have eluded satisfactory explanation. First, the detailed mechanisms underlying this phenomenon remain unknown (Rassier and Herzog, 2004) and second, it is not known whether force depression plays a functional role during normal, everyday, voluntary contractions. Until recently, all work on force depression had been conducted in isolated muscle or fibre preparations that were activated artificially through electrical stimulation (Herzog and Leonard, 1997; Morgan et al., 2000; Abbott and Aubert, 1952; Mare´chal and Plaghki, 1979; Edman et al., 1993). Few results are now available on force depression in human skeletal muscles that were either activated through electrical stimulation (De Ruiter et al., 1998; Lee and Herzog, 2003) or maximal voluntary contraction (MVC) (Lee et al., 1999; Lee and Herzog, 2003; De Ruiter and de Haan, 2003). These studies confirmed that under these experimental conditions, force depression following shortening of the activated muscles exists very much in the same way as it does in isolated, artificially stimulated preparations (De Ruiter and de Haan, 2003; Lee and Herzog, 2002). However, normal, everyday movements occur at submaximal force levels, with a continuously changing activation. Under sub-maximal conditions, mechanical properties may be quite different from those observed in maximally contracting muscles. For example, the shape of the force–length relationship is greatly affected by the level of activation, and there is a shift of the peak force to greater lengths with decreasing levels of activation (e.g., Rack and Westbury, 1969; Close, 1972; Rassier et al., 1998). Therefore, if force depression only occurs on the descending, but not the ascending limb of the force–length relationship, as proposed by supporters of the so-called ‘‘sarcomere length non-uniformity theory’’, a change in the shape of the force–length relationship would also affect the region of muscle lengths where force depression would be observed (Morgan et al., 2000). Therefore, it is perceivable that force depression may differ from that observed in maximally or electrically elicited muscle contractions. The purpose of this study was to test if there is force depression following sub-maximal, voluntary contractions in human skeletal muscle. In order to achieve this goal, force or activation were kept constant while the uncontrolled variable was observed for purely isometric reference contractions and for contractions involving sub-maximal active shortening. We chose the human adductor pollicis group for this investigation, as it is the best studied human muscle in this area of research (Lee and Herzog, 2003; De Ruiter et al., 1998; De Ruiter and de Haan, 2003; De Ruiter et al., 2000; Lee and Herzog, 2002; Oskouei and Herzog, 2005). It shows force depression for artificially stimulated and MVC (De Ruiter et al., 1998; Lee and Herzog, 2003; De Ruiter and de Haan, 2003), and
its force and activation can be quantified easily (De Ruiter and de Haan, 2003; De Ruiter et al., 1998; Lee and Herzog, 2003; Cafarelli and Bigland-Ritchie, 1979). Based on previous work (De Ruiter et al., 1998; Edman et al., 1993; Herzog and Leonard, 1997; Herzog et al., 2000; Lee and Herzog, 2003; Mare´chal and Plaghki, 1979), we hypothesized that force depression is caused by a stress-induced inhibition of cross-bridge attachments in the actin–myosin overlap zone that is newly formed during shortening. If so, we would expect force depression to occur during all sub-maximal voluntary contractions, and also expect that force depression would increase with increasing magnitudes of shortening, and the absolute magnitude of force depression would be smaller for sub-maximal compared to maximal contractions.
2. Methods 2.1. Subjects A total of 45 subjects (28 males and 17 females, 22–48 years) with no history of neuromuscular disorder and injury to the left hand gave free written informed consent to participate in one of the four test protocols comprising this study. The first test (n ¼ 10 male subjects) was aimed at determining the variability in steady-state isometric force (activation) for a given, constant level of sub-maximal activation (force). The remaining three tests were all aimed at establishing if there was force depression following sub-maximal voluntary shortening contractions of the adductor pollicis group. In the second test (n ¼ 8, 4 males and 4 females), activation was kept constant while force was measured for isometric reference contractions and for experimental shortening contractions over a 301 thumb adduction angle. The third test (n ¼ 11, 6 males and 5 females) was identical to the second one, except that force was controlled at a sub-maximal level while activation was measured. Finally, the fourth test (n ¼ 16, 8 males and 8 females) was identical to the second one, except that shortening was produced over 101, 201, and 301 thumb adduction. All experimental procedures were approved by the Conjoint Ethics Committee of the University of Calgary. 2.2. Apparatus A custom-designed dynamometer, which measures thumb adduction force via a set of calibrated strain gauges arranged in a full Whealstone bridge configuration, was used for all testings. It measures the thumb angle at the carpometacarpal joint using an analogue encoder and a goniometer. This apparatus has been described in detail elsewhere (Lee and Herzog, 2002).
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2.3. Experimental settings The left hand was used for testing and was immobilized with a reusable clinical cast (Ezeform, Rehabilitation Division, Smith & Nephew Inc., Germantown, WI, USA) in a neutral position. Immobilization restricted the movement of the wrist and fingers, except for the thumb. After immobilization, subjects sat on an adjustable chair with the shoulder slightly abducted and the elbow flexed 901. The forearm was placed in a V-shaped metal plate, and was secured with velcro straps. The centre of rotation of the motor was aligned with the carpometacarpal joint. An aluminium rod was placed horizontally between thumb and index fingers. By placing the distal end of the thumb on the auxiliary piece attached to the aluminium rod, thumb movement was restricted to the frontal plane (Lee and Herzog, 2002, 2003). Before testing, the range of motion during thumb abduction – adduction was tested carefully for each subject. The lowest adducted angle was defined as 01. The thumb was then abducted to 301 (tests 1–3) and the desired starting angle (301, 201, 101) in test 4. Thumb angles were defined to increase with abduction. 2.4. Muscle activation measurements Adductor pollicis activation was measured using surface electromyography (EMG). The medial aspect of the palmar side of the hand and the posterior side of the thumb were cleaned with alcohol. A pair of surface electrodes (Ag/AgCl, Ref. 01-7545 ConMed Corporation, UTICA, NY, USA) was placed on the palmar side of the hand over the adductor pollicis. One electrode was placed close to the base of the proximal phalanx, the other one over the middle of the third metacarpal bone. The inter-electrode distance was 2.370.1 cm.The reference electrode was placed on the posterior bony side of the thumb and the inter-electrode impedance was measured and confirmed to be less than 5 kO in all measurements. EMG signals were amplified ( 1000) no further than 10 cm from the recording site and they were band-pass filtered (10 and 1000 Hz). EMG signals were collected at a sampling frequency of 3000 Hz. A linear envelope of the EMG signal was obtained by fullwave rectifying and smoothing the EMG using a time window of 400 ms sliding average of the rectified signal (Medical Engineering Systems and Ergonomics, Aachen, Germany).
3
which consisted of two sub-protocols, A and B, comprising ten sub-maximal, voluntary, isometric trials (5 s) each. Subjects were asked to perform three maximal voluntary thumb adductor contractions at a thumb abduction angle of 01 with a 2-min (minimum) interval between contractions. The average of three maximal voluntary efforts was taken as the MVC and used to calculate 30% of MVC. In sub-protocol A (activation control), subjects were asked to match an average EMG trace on an oscilloscope that corresponded to 30% of the average EMG measured during maximum voluntary contraction. While doing so, the corresponding isometric force was measured. In sub-protocol B (force control), subjects were asked to match a force trace on an oscilloscope that corresponded to 30% of the maximum voluntary contraction force. While doing so, the corresponding average EMG was measured. 2.5.2. Tests 2– 4 Force depression for sub-maximal voluntary contractions was measured using three separate tests. In all the tests, subjects (n ¼ 8, n ¼ 11 and n ¼ 16 for tests 2, 3, and 4, respectively) were asked to perform a number of trial sets. Each set consisted of an isometric reference contraction and a corresponding isometric-shorteningisometric test contraction. Reference contractions were performed at a thumb angle of 01 (fully adducted thumb) and subjects were asked to match a reference line corresponding to an EMG trace of 30% of MVC (tests 2 and 4, Fig. 1) or a 30% MVC force trace (test 3, Fig. 2). Test contractions consisted of an isometric contraction at 301 of thumb abduction (tests 2 and 3) and at 101, 201, 301 of thumb abduction randomized across subjects (test 4), followed by a shortening contraction to 01, and a subsequent isometric contraction at the 01 angle while matching the corresponding sub-maximal force or average EMG traces (Figs. 1 and 2). The shortening speed for all test contractions was 101/s. Isometric reference contractions were held for a minimum of 12 s, so as to have the same duration of contraction as the isometric-shortening-isometric test contractions. In the experimental tests, contractions were maintained for a minimum of 4 s following the shortening phase, to ensure that all transient force and EMG responses had subsided and a steady-state force and EMG response had been reached when force/EMG measurements were made. 2.6. Data collection and analysis
2.5. Experimental tests 2.5.1. Test 1 The first step of this study was to determine whether sub-maximal voluntary contractions of human adductor pollicis could be performed with minimum variability in EMG and force. Ten male subjects completed a protocol
Thumb adduction forces, thumb angles, and EMG signals were recorded simultaneously at a sampling frequency of 3000 Hz. Mean isometric force and muscle activation were determined for a 2 s period after steadystate force or EMG had been reached in the test contractions (Figs. 1 and 2). Then, the corresponding
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Fig. 1. Example of average (full-wave rectified and smoothed) EMG (AEMG (A), raw EMG (B), thumb adduction force (C), and metacarpophalangeal joint angle (D) as a function of time during 30% of maximal voluntary contractions (MVC) of human adductor pollicis for an isometric reference and an isometric-301 shorteningisometric test contraction. Subjects were asked to control activation (activation control) at 30% MVC (see Methods). Isometric reference force (F Iso ref) was measured for a 2-s period in the final, steady-state part (labelled by the horizontal dotted arrow in C) for comparison with the corresponding values obtained from the isometric contractions following active shortening (F Iso short). Contractions were maintained for a minimum of 4 s following the shortening phase, to ensure that all transient force had subsided and a steady-state force had been reached. The difference between the isometric reference and shortening test force was defined as force depression. AEMG Iso ref, isometric reference average EMG; AEMG Iso short, isometric shortening average EMG; Raw EMG ref, reference raw EMG; Raw EMG short, isometric shortening raw EMG.
phase in the isometric reference contraction was located and the mean isometric force and muscle activation were determined. Force depression following muscle shortening (tests 2 and 4) was determined by subtracting the mean steadystate force of the shortening test contraction from the corresponding force of the isometric reference contraction. Possible increases in muscle activation following muscle shortening (test 3) were determined by subtract-
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Fig. 2. Example of thumb adduction force (A), raw (B), AEMG (C), and metacarpophalangeal joint angle (D) as a function of time during 30% of maximal voluntary contractions of human adductor pollicis for an isometric reference and an isometric-301 shortening-isometric test contraction. Muscle force was kept constant (force control) throughout the contractions (see Methods). Isometric reference EMG (AEMG Iso ref) was measured for a 2-s period in the final, steady-state part (labelled by the horizontal dotted arrow in C) for comparison with the corresponding values obtained from the isometric contractions following active shortening (AEMG Iso short). Contractions were maintained for a minimum of 4 s following the shortening phase, to ensure that all transient EMG responses had subsided and a steadystate EMG response had been reached. The difference in activation between the isometric reference and shortening test force was defined as EMG increase. F Iso ref, isometric reference force; F Iso short, isometric force after shortening; Raw EMG ref, reference raw EMG; Raw EMG short, isometric shortening raw EMG.
ing the steady-state average EMG of the shortening test contractions from the corresponding values of the isometric reference contractions. 2.7. Statistical analysis Differences in steady-state isometric force and average EMG were compared for the isometric reference contractions and the shortening test contractions, three
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45 40 35 Force (N)
shortening amplitudes (101, 201, and 301; test 4), and the interaction between shortening amplitude and contraction type (test 4 only). Repeated measures ANOVA and Bonferroni post hoc comparisons were used for statistical analysis. Values are presented as means71SE. All tests were performed at a level of significance of a ¼ 0:05.
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3.2. Test 2 (force depression, 301 shortening, activation control) We found a significant 2173% steady-state force depression (po0:05) following 301 of shortening of the adductor pollicis during activation-controlled, sub-maximal voluntary contractions (Fig. 4A). This result was observed consistently for all eight subjects. The mean average EMG did not differ significantly between the isometric reference and the shortening test contractions. 3.3. Test 3 (force depression, 301 shortening, force control) There was a significant increase (po0:05) in steadystate average EMG (1873%) in the force-controlled 301
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Fig. 3. Mean (SE) coefficients of variation of average EMG (white bars) and force (grey bars) in the activation control and the force control protocols of test 1 ðn ¼ 10Þ. Note that the variability of force and average EMG are similar (10%) for the activation and force control tests, respectively, while force can be controlled tighter than average EMG in the force control compared to the activation control protocol.
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When asked to perform isometric contractions with the adductor pollicis and control activation at 30% of that observed during MVC, force values across subjects varied by 972% (Fig. 3). Similarly, when asked to perform sub-maximal isometric contractions and match force at 30% of MVC, average EMG values across subjects varied by 1071% (Fig. 3).
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Fig. 4. Mean (SE) isometric sub-maximal thumb adduction force (A) in the isometric reference and the 301 shortening test contractions ðn ¼ 8Þ, and mean (SE) average EMG (B) for isometric reference and 301 shortening test contractions ðn ¼ 11Þ. Force is significantly smaller in the shortening test contractions compared to the isometric reference contractions when activation is controlled, indicating that there is a force depression during sub-maximal voluntary contractions (*po0.05). Conversely, average EMG is significantly greater for the test compared to the isometric reference contractions (*po0.05) in the tests with force control.
shortening contractions compared to the isometric reference contractions (Fig. 4B). The controlled mean force was the same for the shortening tests (3978 N) and the isometric reference contractions (3878 N). This result was observed consistently for all 11 subjects participating in test 3. 3.4. Test 4 (force depression; 101, 201, and 301 shortening; activation control) There was a significant effect (po0:05) of shortening amplitude on force depression during 30% of MVC submaximal, voluntary shortening of the adductor pollicis (Fig. 5). Mean force depression was significantly increased (po0:05) as shortening amplitude increased from 101 to 301 and from 201 to 301 (Fig. 5). Although there was a trend of increasing force depression from 101 to 201 of shortening, the difference was not statistically significant (Fig. 5). This result was observed consistently for all 16 subjects participating in test 4. The mean average EMG did not differ significantly between the isometric reference and the shortening test contractions for all three shortening amplitudes.
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Fig. 5. Mean (SE) force depression for 101 (white bar), 201 (grey bar), and 301 (black bar) shortening amplitudes, for activation controlled testing ðn ¼ 16Þ. Force depression was significantly increased when shortening amplitude increased from 101 to 301 and from 201 to 301 (*po0.05). The difference between 101 and 201 was not statistically significant.
4. Discussion We found steady-state isometric force depression for sub-maximal voluntary contractions for every subject. This is the first study to show that force depression exists not only for artificially elicited electrical contractions in isolated muscle and fibre preparations (Herzog and Leonard, 1997; Morgan et al., 2000; Abbott and Aubert, 1952; Mare´chal and Plaghki, 1979; Edman et al., 1993) and for human voluntary contractions at maximal effort (Lee et al., 1999; De Ruiter and de Haan, 2003; Lee and Herzog, 2003), but also for sub-maximal voluntary contractions. For controlled activation (at 30% of MVC), force depression was about 21%, 15%, and 11% for thumb adduction movements over a range of 301, 201, and 101, respectively (Fig. 5). These values are consistent with those observed for the adductor pollicis group at maximal voluntary (22%, 17%, and 12%, respectively) and electrically stimulated contractions (24%, 14%, and 8%, respectively) under otherwise identical conditions (Lee and Herzog, 2003). For controlled force (at 30% of MVC), average EMG following the shortening contractions was increased by 18% (Fig. 4B). This result is a further evidence of force depression for sub-maximal voluntary contractions and indicates that force depression in sub-maximal efforts may not be apparent, as it can be offset by an increase in muscle activation to compensate for the reduced force capabilities. It has been shown that force depression is directly related to the amount of muscle or fibre shortening (Mare´chal and Plaghki, 1979; Herzog and Leonard, 1997), the force during the shortening phase (Herzog and Leonard, 1997), and the mechanical work performed during the shortening phase (Herzog et al., 2000; De Ruiter et al., 1998). Based on these observations, a
possible mechanism for force depression is a stressinduced inhibition of cross-bridges in the actin–myosin overlap zone that is formed during shortening (Mare´chal and Plaghki, 1979). According to this mechanism, if a muscle is activated, the compliant thick and thin filaments are stretched (Goldman and Huxley, 1994; Higuchi et al., 1995; Huxley et al., 1994; Kojima et al., 1994; Nishizaka et al., 1995; Wakabayashi et al., 1994) and the angular alignment of cross-bridge to actin attachment site may be distorted (Daniel et al., 1998). The greater the stress during shortening, the greater the angular distortion, which causes the proposed inhibition of cross-bridge attachments in the newly formed overlap zone. If so, force depression would be expected following sub-maximal shortening contractions. However, since the force during shortening is decreased, one would expect the absolute amount of force depression to be decreased for sub-maximal compared to maximal effort contractions. This result is consistent with observations in cat soleus in which decreases in force during shortening caused a decrease in force depression (Herzog and Leonard, 1997). Force decrease was found here to be approximately 20% of the isometric reference force for sub-maximal contractions, and the average EMG was found to increase approximately 18% of the corresponding isometric reference EMG. The shortening tests were well within the range of thumb adduction movement and force, and we made no attempt at maximizing the magnitude of force depression. De Ruiter et al. (1998) found force depression values of 37% in the adductor pollicis when adducting the thumb by 381 at a speed of 61/s. We found isolated force depression values exceeding 50% in adductor pollicis (Lee and Herzog, 2003). Therefore, given the right conditions, force depression may be substantial. Nevertheless, we are not aware of functional muscle models that incorporate force depression in the analysis of human or animal movements. Many mechanical properties of muscles depend on the level of activation. For example, the force–length relationship changes shape, and peak forces are shifted to increased muscle length with decreasing levels of activation (e.g., Rack and Westbury, 1969; Close, 1972; Rassier et al., 1998). Also, force enhancement, following active muscle stretch, is often absent in subjects at submaximal levels of contraction, even though it is always present in maximal voluntary and electrically induced contractions (Oskouei and Herzog, 2005; Lee and Herzog, 2002). However, force depression was observed here in all subjects and for all test conditions. Although the detailed mechanisms underlying force depression are still debated, this study adds the result that, whatever the mechanism, the relative amount of force depression does not appear to be affected by the level of activation or force, and seems to occur to the same extent during voluntary and electrically induced contractions.
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There are several limitations that should be considered when interpreting the results of this study. First and foremost, forces and activations were associated with a variability of the uncontrolled parameter of about 10% (Fig. 3), i.e., when subjects were asked to match activation at 30% of MVC, the coefficient of variation in force was approximately 10%, and vice versa when subjects were asked to control force at 30% of MVC. Another limitation of this study was that activation of antagonistic muscles was not measured. The inherent assumption underlying our results is that antagonistic activity was the same for the isometric reference and the shortening test contractions. Also, the idea of using surface EMG as a measure of muscle activation may easily be criticized. However, we felt it was an adequate approach for a non-invasive human study, but the implicit assumptions are by no means trivial. Finally, the control of activation and force during the shortening phase was virtually impossible for any of the subjects. All we can say with certainty is that the effort during shortening was sub-maximal, but it could have deviated considerably from a 30% of MVC effort. However, despite these limitations, we feel confident that the general results reported here are valid and correct.
5. Conclusion We conclude that sub-maximal voluntary shortening causes a loss of isometric steady-state force compared to the force observed in a purely isometric reference contraction. Force depression is substantial, it exceeds the uncertainty associated with the experimental procedures, and it was observed consistently in all subjects participating in this study. Therefore, we think it is likely that force depression plays a role in normal everyday movements.
Acknowledgements The Natural Sciences and Engineering Research Council of Canada, the Canada Research Chair Programme, and Iran’s Ministry of Health are acknowledged for their assistance in this study.
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