Chapter 6. Summarizing discussion
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1 Chapter 6 Summarizing discussion
2 Muscle activation during isometric and dynamic exercise The general aim of this thesis was to investigate the activation of the quadriceps muscle during dynamic exercise and to compare this with the activation during isometric exercise. Muscle activation was investigated, using muscle biopsy samples from the vastus lateralis, with the glycogen depletion method and the PCr/Cr ratio method in Chapter 2 and with the use of intramuscular EMG of the vastus lateralis and surface EMG of all quadriceps muscles in Chapters 3, 4 and 5. Using the combination of these methods insight was obtained in the recruitment of the different muscle fibre types and motor units and the discharge rates at which the fibres are activated. A summary of the main results will be given and discussed below. Furthermore, limitations and recommendations for future research will be presented. Muscle activation during dynamic exercise From studies in which isometric contractions were performed, it is known that the order of recruitment is rather fixed and follows the size principle. This means that at low levels of force the type I fibres are recruited and with higher forces type IIA and subsequently IIAX fibres are activated (Beltman et al, 2004a; Gollnick et al, 1973; Gollnick et al, 1974; Vøllestad et al, 1984). It is however not entirely clear whether the force during dynamic contractions is regulated by the same fixed order of fibre recruitment. In literature an inconsistency exists in the submaximal exercise intensity at which type II fibres are recruited. According to Beltman et al (2004a), using PCr/Cr ratios, during repeated isometric contractions, type II fibres were only activated at high exercise intensities, i.e. at force levels of ~70 % MVC and higher. In contrast, Vøllestad et al (1984) found, using glycogen depletion, that type II fibres were already activated during a cycling exercise in which ~40 % of the maximal dynamic force was exerted on the pedals. In Chapter 2 of this thesis it was shown that, in line with the findings of Vøllestad et al (1984), the type II fibres of the vastus lateralis muscle were already recruited within 1 min of exercise at ~40 % of the maximal dynamic force exerted on the pedals, and remained active during the remainder of the 45-min cycling exercise. Thus, at the same (~40 %) relative muscle force (power) a greater proportion of type II fibres is recruited during cycling than previously reported for isometric contractions, probably because of the dynamic character of the exercise. Since type II fibres are the fast fatigable muscle fibres, the consequence of the recruitment of type II fibres during cycling at lower intensities is that the dynamic exercise is more fatiguing than isometric exercise. For the subjects in the present thesis, 55 % of the fibres were classified as type I and 45 % of the fibres as type II. It can be expected that in subjects with a 128
3 Chapter 6 different fibre type distribution, for example 80 % type I and 20 % type II fibres as in endurance athletes, the finding of an earlier recruitment of type II fibres would not have been found. By determining fibre activation with the use of both the PCr/Cr ratio method and the glycogen depletion method in Chapter 2, we additionally investigated which method was more sensitive in quantifying fibre activation. The PCr/Cr ratio method already proved to be a useful method for the detection of muscle fibre activation, even after only 7 maximal isometric contractions (Beltman et al, 2004b). In line with the results of Beltman et al (2004b), in the present thesis fibre activation was detected already after 1 min of exercise at ~40 % of the maximal available force during cycling. Although fibre activation was also detected after 1 min of cycling with the use of the glycogen depletion method, even after 45 min of exercise fewer fibres were activated according to the glycogen depletion method compared to the PCr/Cr ratio method. Since, in contrast to glycogen depletion, a decrease in PCr is directly linked to ATP resynthesis during exercise (Infante et al, 1965), we suggested that probably other substrates than glycogen were used to provide energy and that glycogen depletion was not a reliable indication for fibre activation. We therefore concluded that the PCr/Cr ratio method was more sensitive in determining fibre activation. Since during the cycling exercise only shortening contractions were exerted by the quadriceps muscle, whereas in daily life lengthening contractions are also performed, we investigated muscle activation during shortening and isometric contractions as well as during lengthening contractions. In Chapter 3 we showed that the intrinsic muscle strength of the quadriceps muscle at the slow speed (10 s -1 ) used during shortening and lengthening was respectively 4 % lower and 16 % higher than the maximal isometric strength, due to the force velocity relationship. Differences in muscle activation between shortening, lengthening and isometric contractions, when the same absolute force had to be generated, could thus at least partly be the result of these mode dependent differences in intrinsic muscle strength. Therefore we studied quadriceps muscle activation during shortening and isometric contractions and lengthening and isometric contractions at the same relative contraction intensity, i.e. at the same percentage of the intrinsic muscle strength at the different contraction modes. The present thesis demonstrated that, when mode dependent differences in intrinsic muscle strength were taken into account, quadriceps muscle activation was similar between lengthening and isometric contractions, but activation remained higher during shortening compared to isometric contractions (Chapter 3). When mode dependent strength differences were taken into account, surface EMG was ~30 % 129
4 higher and discharge rates were ~20 % higher during shortening compared to isometric contractions, indicating that motor units of the vastus lateralis muscle were activated at a higher rate and that probably additional motor units are recruited (Figure 3.3). The higher muscle activation during shortening compared to isometric contractions at the same relative contraction intensity is in line with the suggestion of de Haan (1998) that higher calcium concentrations are required to obtain maximal torque during shortening compared to isometric contractions. Moreover, the enhanced muscle activation could at least partly be due to the depression of force during shortening (de Ruiter et al, 1998), for instance caused by a stress-induced inhibition of cross bridge attachment (Marechal and Plaghki, 1979). In Chapter 4 we have shown that muscle activation of the vastus lateralis muscle, discharge rate and probably also recruitment, remained enhanced during isometric contractions 1 5 s following shortening compared to isometric reference contractions at the same torque and knee angle, probably to compensate for the lower intrinsic muscle strength following shortening. It can be concluded that it is more difficult to produce a certain amount of force during and following shortening than during isometric contractions. This is not just because muscles are intrinsically weaker during shortening since, even after correction for these differences in intrinsic strength, shortening required higher muscle activation. The extra muscle activation required during and following shortening was reflected by the higher discharge rates of already activated motor units and also by the recruitment of additional motor units, probably containing the fast fatigable type II fibres (Chapter 2). An unexpected finding in Chapter 4 was that the higher muscle activation to produce a certain isometric force following shortening was not dependent on the torque output during shortening. Although these findings were in line with the findings of Rousanoglou et al (2007) and Lee & Herzog (2003), according to the theory of stressdependent inhibition of cross bridge attachment, muscle activation following shortening should increase with the force produced during shortening (Herzog and Leonard, 2007; Marechal and Plaghki, 1979). Since the torque dependency of shortening induced force depression was previously demonstrated during electrically stimulated contractions, we suggested that the different way in which motor units are activated could somehow play a role: during electrically evoked contractions motor units are activated in a synchronous way whereas during voluntary contractions motor units are activated asynchronously. During lengthening contractions similar vastus lateralis discharge rates were found compared to isometric contractions when corrected for mode dependent differences in intrinsic muscle strength, indicating that the higher muscle strength can 130
5 Chapter 6 fully explain why it is easier to produce a certain absolute force during lengthening compared to isometric contractions (Chapter 3). Surface EMG was, however, found to be higher during lengthening compared to isometric contractions, which could indicate that additional motor units were recruited, but the increased surface EMG during lengthening could also be a consequence of an increased synchronisation of motor unit discharging (Semmler et al, 2002). In contrast, surface EMG was found to be lower during isometric contractions 1 5 s following lengthening compared to values during isometric reference contractions, whereas, similar to what was found during lengthening, motor unit discharge rates remained unchanged (Chapter 4). These findings would indicate that motor units of the vastus lateralis muscle were derecruited to compensate for the enhanced force following lengthening (de Ruiter et al, 2000) and as a consequence, maintaining a force level is easier during isometric contractions following lengthening compared to isometric reference contractions. The decrease in surface EMG following lengthening (indicative for greater force enhancement) was not larger at higher torques (Chapter 4), which is in contrast to the findings of Oskouei & Herzog (2005; 2006), but in line with the results de Ruiter et al (2000), and indicate that force enhancement has characteristics that seem unrelated to cross bridge properties. In previous studies, muscle activation was often found to be lower during lengthening compared to shortening contractions, which was mainly attributed to a different motor unit behaviour during lengthening contractions to compensate for the higher intrinsic muscle strength (Del Valle and Thomas, 2005; Howell et al, 1995; Kossev and Christova, 1998; Søgaard et al, 1996). However, the present thesis showed that the larger adaptations in muscle activation occur during shortening contractions. Muscle activation during isometric contractions at different knee angles Since during dynamic contractions force is produced over a range of knee angles, we were interested in the effect of knee angle on quadriceps muscle activation during isometric contractions (Chapter 5). According to the force length (knee angle) relationship muscles are intrinsically weaker at more flexed and more extended knee angles compared to the optimum knee angle for force production. We therefore expected that, when the same force had to be produced at the different knee angles, activation would be higher at the more flexed and the more extended knee angles compared to the optimum knee angle. We demonstrated that, as expected, recruitment and derecruitment thresholds of the vastus lateralis muscle were lower at more flexed knee angles compared to the optimum angle, indicating that more motor units were 131
6 activated at the more flexed knee angles. However, in contrast to our expectations, vastus lateralis recruitment and derecruitment thresholds were not lower at the more extended knee angles compared to the optimum angle. Moreover, vastus lateralis motor unit discharge rate was unaffected by the knee angle. These joint angle independent discharge rates were in line with the findings of Pasquet et al (2005), but in contrast to the higher discharge rates at short muscle lengths found in the study of Christova et al (1998). Moreover, the present lack of decrease in recruitment threshold at the more extended knee angles was in contrast to the findings of Pasquet et al (2005). Thus despite the fact that the intrinsic muscle strength was (~40 %) lower at the more extended compared to the optimum knee angle, there was no evidence for additional recruitment of motor units in the vastus lateralis muscle and moreover, discharge rates were unchanged. However, surface EMG was increased at the more extended and the more flexed knee angles compared to the optimum angle. Therefore, recruitment of additional motor units in different parts of the vastus lateralis muscle and/or in other quadriceps muscles can not be excluded and this may explain the discrepancy between the behaviour of single motor unit EMG and surface EMG at the extended knee angles. Although the lack of changes in (de)recruitment and discharge rate at the more extended knee angles are unexpected and inexplicable, these findings are in line with the lower oxygen consumption (de Ruiter et al, 2005) and the higher resistance to fatigue (Kooistra et al, 2006; Place et al, 2005) found during isometric force production at the more extended knee angles. We conclude that, in contrast to our expectations based on the force length relationship, it is easier to produce a certain absolute force at the more extended knee angles than the optimum angle. Limitations and recommendations In the present thesis different methodologies were used to measure muscle activation. All these methods have their advantages but also their limitations and the latter may restrict the extrapolation to real life movement. In Chapter 2 muscle fibre activation of the vastus lateralis muscle was determined using the PCr/Cr ratio method and the glycogen depletion method. With these methods information of fibre activation is obtained from muscle biopsies, which are only small samples of the vastus lateralis muscle, which is one muscle of the quadriceps muscle group. Although the vastus lateralis muscle is thought to be representative for the quadriceps muscle, extrapolation of the results from the small biopsies to the whole quadriceps muscle may not be completely correct. Furthermore, the activation pattern by which a muscle fibre is driven could not be investigated at 132
7 Chapter 6 different points in time and therefore different populations of muscle fibres were investigated in time (Chapter 2). As a consequence, the measured muscle fibres may have belonged to the different motor units with different properties, introducing some variation in the results. The great advantage of both the PCr/Cr ratio method and the glycogen depletion method is that fibre activation can be measured for dynamic contractions up to maximal intensity. Moreover, since a decrease in PCr is directly linked to ATP resynthesis during exercise (Infante et al, 1965), an acute measurement of the energy state of the muscle fibre is obtained. In contrast to the biopsy method, with the use of single motor unit EMG, the activation pattern of one motor unit can be studied repeatedly in time and the discharge behaviour of the same single motor unit of the vastus lateralis muscle could therefore be studied in Chapters 3, 4 and 5. While measuring the discharge behaviour of the same single motor unit in different conditions has the advantage that activation at different modes and intensities of exercise can be investigated very accurately at the motor unit level, with this method the small sample size (as with the biopsy method) may limit extrapolation of single motor unit EMG to the whole muscle activation. Moreover, identification of the same motor unit is more difficult when higher forces are exerted by the muscle, because of simultaneous discharging of many motor units in the area of the electrode. Therefore, motor unit discharge behaviour is often obtained during low force contractions during which, according to the size principle, only the slow motor units are recruited. Although we have been able to measure discharge rates of a single motor unit at relatively high torques (up to 70 % MVC), the majority of results are probably derived from slow motor units. Thus, in contrast to the biopsy method, in which high intensity exercise can be studied including activity of fast motor units, the experiments measuring motor unit EMG only studied activation of slow motor units. It is unclear whether and to what extent the behaviour of the fast motor units during movement is different from the slow units. In Chapter 2 a dynamic cycling exercise was performed at 90 rpm (corresponding to ~270 s -1 ), which is representative for cycling in daily life. The speed at which the shortening and lengthening contractions in Chapters 3 and 4 were performed were, however, limited to 10 s -1 since it was not possible for the subjects to maintain the required constant torque at higher velocities. Furthermore, the slow movement performed was, in contrast to daily life, a simple isolated movement of the lower leg. Since the differences in muscle activation may have been greater during movements which are more complex and performed at higher velocities, the mode 133
8 dependent differences in muscle activation described in this thesis may be an underestimation of the mode dependent differences in daily life movement. From this thesis it can be concluded that, when taking mode dependent differences in maximal intrinsic muscle strength into account, higher muscle activation is required for shortening contractions compared to lengthening and isometric contractions. Moreover, muscle activation during isometric contractions at different knee angles (muscle lengths) is different than expected from the force length relationship. The next interesting step would be studying single motor unit discharge behaviour during more complex contractions and at higher velocities, thereby approaching muscle actions during daily life movement. Furthermore, it would be interesting to study motor unit EMG in muscles containing a relatively high percentage of fast fibres, to investigate differences in the discharge behaviour between slow and fast fibres in several movement conditions. 134
9 Chapter 6 References Beltman JG, de Haan A, Haan H, Gerrits HL, van Mechelen W, Sargeant AJ (2004a). Metabolically assessed muscle fibre recruitment in brief isometric contractions at different intensities. Eur J Appl Physiol 92: Beltman JG, Sargeant AJ, Haan H, van Mechelen W, de Haan A (2004b). Changes in PCr/Cr ratio in single characterized muscle fibre fragments after only a few maximal voluntary contractions in humans. Acta Physiol Scand 180: Christova P, Kossev A, Radicheva N (1998). Discharge rate of selected motor units in human biceps brachii at different muscle lengths. J Electromyogr Kinesiol 8: de Haan A (1998). The influence of stimulation frequency on force-velocity characteristics of in situ rat medial gastrocnemius muscle. Exp Physiol 83: de Ruiter CJ, de Boer MD, Spanjaard M, de Haan A (2005). Knee angle-dependent oxygen consumption during isometric contractions of the knee extensors determined with near-infrared spectroscopy. J Appl Physiol 99: de Ruiter CJ, de Haan A, Jones DA, Sargeant AJ (1998). Shortening-induced force depression in human adductor pollicis muscle. J Physiol 507: de Ruiter CJ, Didden WJ, Jones DA, de Haan A (2000). The force-velocity relationship of human adductor pollicis muscle during stretch and the effects of fatigue. J Physiol 526: Del Valle A, Thomas CK (2005). Firing rates of motor units during strong dynamic contractions. Muscle Nerve 32: Gollnick PD, Armstrong RB, Saubert CW, IVth, Sembrowich WL, Shepherd RE, Saltin B (1973). Glycogen depletion patterns in human skeletal muscle fibers during prolonged work. Pflügers Arch - Eur J Physiol 344: Gollnick PD, Piehl K, Saltin B (1974). Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J Physiol 241: Herzog W, Leonard TR (2007). Residual force depression is not abolished following a quick shortening step. J Biomech 40: Howell JN, Fuglevand AJ, Walsh ML, Bigland-Ritchie B (1995). Motor unit activity during isometric and concentric-eccentric contractions of the human first dorsal interosseus muscle. J Neurophysiol 74: Infante AA, Klaupiks D, Davies RE (1965). Phosphorylcreatine consumption during 135
10 single working contractions of isolated muscle. Biochim Biophys Acta 94: Kooistra RD, Blaauboer ME, Born JR, de Ruiter CJ, de Haan A (2006). Knee extensor muscle oxygen consumption in relation to muscle activation. Eur J Appl Physiol 98: Kossev A, Christova P (1998). Discharge pattern of human motor units during dynamic concentric and eccentric contractions. Electromyogr Clin Neurophysiol 109: Lee HD, Herzog W (2003). Force depression following muscle shortening of voluntarily activated and electrically stimulated human adductor pollicis. J Physiol 551: Marechal G, Plaghki L (1979). The deficit of the isometric tetanic tension redeveloped after a release of frog muscle at a constant velocity. J Gen Physiol 73: Oskouei AE, Herzog W (2005). Observations on force enhancement in submaximal voluntary contractions of human adductor pollicis muscle. J Appl Physiol 98: Oskouei AE, Herzog W (2006). Force enhancement at different levels of voluntary contraction in human adductor pollicis. Eur J Appl Physiol 97: Pasquet B, Carpentier A, Duchateau J (2005). Change in muscle fascicle length influences the recruitment and discharge rate of motor units during isometric contractions. J Neurophysiol 94: Place N, Maffiuletti NA, Ballay Y, Lepers R (2005). Twitch potentiation is greater after a fatiguing submaximal isometric contraction performed at short vs. long quadriceps muscle length. J Appl Physiol 98: Rousanoglou EN, Oskouei AE, Herzog W (2007). Force depression following muscle shortening in sub-maximal voluntary contractions of human adductor pollicis. J Biomech 40: 1-8. Semmler JG, Kornatz KW, Dinenno DV, Zhou S, Enoka RM (2002). Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle. J Physiol 545: Søgaard K, Christensen H, Jensen BR, Finsen L, Sjøgaard G (1996). Motor control and kinetics during low level concentric and eccentric contractions in man. Electromyogr Clin Neurophysiol 101: Vøllestad NK, Vaage O, Hermansen L (1984). Muscle glycogen depletion patterns in type I and subgroups of type II fibres during prolonged severe exercise in man. Acta Physiol Scand 122:
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