European Journal of
Applied Physiology
Eur. J. Appl. Physiol. 41, 73-82 (1979)
and Occupationa~ Physiology 9 Springer-Verlag t979
Serial Isometric Contractions Under Imposed Myotatic Stretch Conditions in High-strength and Low-strength Men Gary Kamen University of Massachusetts, Department of Exercise Science, Amherst, MA 01003, USA
Summary. The immediate effects of an imposed myotatic stretch on knee extensor force were studied in 12 high-strength and 12 low-strength men. Under nonfatigued pre-exercise conditions, significant tension increases of 6.5% for the high-strength group and 11.0% for low-strength subjects were observed as a result of the imposed stretch. An exercise treatment involving 28 serial isometric contractions, each of 5 s duration, with an intertrial rest period of 10 s was administered. This fatiguing exercise resulted in significant decrements in strength on the order of 28.0% and 18.5% for the high-strength and low-strength groups, respectively. A similar treatment which included a 1 s imposed myotatic stretch during each trial resulted in a greater strength decrement for the lowstrength group (26.4%) than for the high-strength subjects (15.0%). A neural factor involving the stretch reflex is tentatively suggested as a plausible explanation accounting for the observation that high-strength subjects fatigue faster than low-strength subjects under conditions of isometric exercise, while lowstrength subjects fatigue faster than high-strength individuals in isometric exercise which is performed with an imposed stretch.
Key words: Fatigue -- Reflex -- Eccentric contraction -- Negative work -- Elastic energy
A muscle is capable of generating greater tension during a lengthening contraction (eccentric contraction) than during either isometric or concentric contraction. Cavagna (1977) has recently reviewed the mechanisms responsible for the greater tension exhibited during eccentric exercise. In a movement requiring both positive and negative work stages, mechanical energy can be absorbed by the muscle during the period of negative work. This energy is either reutilized during the subsequent period of positive work, or is converted to heat if the muscle contraction ceases. One source of the extra elastic energy is believed to be the recoil of the stretched viscoelastic elements which takes place during the period of muscle shortening. It is predominantly chemical processes, however, which account for the greatest portion
0301-5548/79/0041/073/$ 02.00
74
G. Kamen
of the extra mechanical energy observed during the period of positive work (Cavagna, 1977). The idea that the contractile component is at least partially responsible for the added tension observed during eccentric contraction received added impetus when the sliding-filament theory was found to explain much of the experimental evidence in negative work experiments (Joyce et al., 1969). During muscle lengthening, the force exerted by the cross links between the actin and myosin filaments within the myofibrils is believed to increase due to the distortion caused by the movement (Joyce et al., !969). Cavagna and Citterio (1974)further suggested that the probability of these crossbridges breaking would further increase as muscle length increased. When an eccentric contraction is followed by muscle shortening, however, the most strained crossbridges with a high tendency to break, would recoil elastically, resulting in greater force during the interval of muscle shortening than would otherwise be possible (Asmussen, 1976; Cavagna and Citterio, 1974). The efficiency of negative work may be observed through several measurement procedures. Asmussen (1953) reported that eccentric work may be characterized by a smaller energy expenditure than concentric work. The ratio between total electromyographic (EMG) output and tension is lower in eccentric work than in concentric work (Komi, 1973). Furthermore, some preliminary data suggests that crossbridges can develop tension during muscle stretch without the splitting of ATP (Curtin et al., 1970; Infante et al., 1964). From the above evidence, one might question whether indeed, more endurance might be obtained through eccentric work. In an effort to clarify the circumstances surrounding the negative work schema, Komi and Viitasalo (1977) administered 40 maximal eccentric and concentric contractions to each of four individuals. Results showed that quadriceps muscle group EMG parameters were altered similarly for both exercise conditions. Moreover, muscle glycogen and blood lactate changed in a similar manner during both fatiguing exercise treatments. Fenn (1930) showed that resting muscles have very low stiffness, while maximal stiffness may be obtained with muscles lengthened while they are fully contracting. The present study was designed to incorporate this idea of muscle stiffness, by imposing a muscle stretch on a muscle group which is already contracting maximally. A second aim of the present experiment was to further elucidate the relationship between eccentric contraction and fatigue. Since eccentric work is characterized by a general economy of energy expenditure (Cavagna, 1977), it was hypothesized that a fatigue curve resulting from eccentric exercise might differ from that resulting from isometric exercise.
Methods
Subjects Male subjects (N = 24) were dividedinto two groups of 12 subjectseach based on maximalvoluntary contractile strength scores (MVC) of the right knee extensors. The physical characteristics of these subjects are listed in Table 1. Most of the high-strength individualswere weight lifters.
Imposed Stretch and Fatigue
75
Table I. Physical characteristics of the subjects Group
Height (cm)
Weight (kg)
Age (years)
High- strength
174.5
84.1
21.8
Low-strength
169.4
67.3
23.7
Procedures The experiment was designed to compare subject response to two different exercise regimens which were intended to produce local muscular fatigue. One exercise regimen involved only isometric contractions, while the other exercise condition involved the administration of an imposed myotatic stretch upon a muscle group which was already contracting maximally. Each subject reported to the laboratory on two different occasions. During each test session, maximal knee extension strength was measured at 130 and 145 degrees of full knee extension. Following a 5 rnin rest, five imposed stretch trials were given. The individual began an isometric contraction at a knee angle of 145 degrees and, after 2 s, a constant torque motor pulled the leg back to 130 degrees at a rate of 16 deg/s. The stretch lasted approximately 1 s. Each individual was told to resist the pull as strongly as possible. When the motor stopped, the subject maintained the isometric contraction at 130 degrees for 2 s. Since the time necessary to pull the leg back was constant, it was possible to obtain three tension measures on each imposed stretch trial. One measure (pre-streteh) was recorded as the maximum tension prior to the pull. A second measure (peak-stretch) was taken as the maximum tension during the stretch. The last measure (post-stretch) was taken as the maximum tension immediately after the stretch ended. Thus the entire contraction lasted for five seconds.
Exercise After the pre-exercise measures, the subject was given one of two exercise regimens. On one test day, 28 serial isometric contractions were administered. Each contraction was 5 s in duration with an intertrial rest period of 10 s. The subjects performed the exercise at 130 degrees. For the second exercise treatment, 28 maximal 5 s contractions were given with an imposed stretch delivered on each trial. The intertrial rest period remained 10 s between trials. As with the pre-exereise imposed stretch trials, the subject contracted maximally at a pre-stretch angle of 145 degrees for 2 s, then came the onesecond stretch, and finally a post-stretch interval of 2 s at 130 degrees. Thus, three fatigue curves were obtained from this treatment condition as strength measures were obtained just prior to each imposed stretch (pre-stretch), during the stretch (peak-stretch), and immediately following the stretch (poststretch) while the subject held the contraction for 2 s at 130 degrees. A summary of the treatment conditions is given in Figure 1.
Results
Reliability Reliability was assessed by the intraclass correlation analysis of variance procedure. T h e a s s o c i a t e d c o r r e l a t i o n coefficients r a n g e d f r o m 0.85 t o 0.96 f o r t h e five pree x e r c i s e s t r e n g t h m e a s u r e s . P a i r e d t-tests r e v e a l e d n o s i g n i f i c a n t d i f f e r e n c e s a m o n g t h e b a s e l i n e s t r e n g t h m e a s u r e s b e t w e e n d a y s o n e a n d two.
76
G. Kamen TEST
A"
5
5 B"
5
MVC MVC MVC
SCHEDULE TRIALS TRIALS IMPOSED
AT 130 ~ AT 145 ~ STRETCH
TRIALS (145
C"
EXERCISE (5 SECS. WORK / I 0 I) I S O M E T R I C (130 ~ 2) I M P O S E D STRETCH (145
~ 130 ~ )
S E C S, R E S T ) ~
130*)
Fig. 1. A--C. Summary of the measurement schedule. Conditions A and B were administered on both test days. Only one exercise condition was given on each day
Table 2. Pre-exercise strength measuresa Measure
130 degrees 145 degrees Pre-stretch (145 degrees) Peak-stretch Post-stretch (130 degrees)
High-strength
75.7 63.7 52.9 80.6 72.8
Low-strength
sd
X
sd
13.8 11.3 11.8 11.5 11.0
51.8 42.1 39.8 57.5 51.8
12.2 10.6 10.7 13.3 12.5
a All values in kg
Pre-Exercise Conditions The baseline mean strength at a knee angle of 130 degrees was greater than that at 145 degrees, as shown in Table 2. This is in accordance with previous research demonstrating a mechanical advantage at this lower angle (Williams and Lissner, 1963). Mean strength values for both groups are listed in Table 2. In order to assess the effects of the imposed myotatic stretch, the maximal tension recorded during the stretch (the peak stretch measure), was compared to the maximal isometric strength measure recorded previously at a knee angle of 130 degrees. As a result of the imposed myotatic stretch, isometric knee extensor strength was increased significantly during the stretch interval (F (1,22)= 23.29; P < 0.001). When compared with the baseline 130-degree isometric strength measure, this strength increase was on the order of 6.5% for the high-strength subjects, 11.0% for the low-strength group. Lagasse (1974) and Morris (1974) reported increases in strength of 6.9% and 25.2%, respectively, for a group of normal individuals. Although the low-strength group evidenced a greater gain in tension from the imposed stretch than did the high-strength group, this difference was not significant as indicated by the non-significant groups X conditions interaction term (F (1,22) = 0.04; P > 0.05).
Imposed Stretch and Fatigue
77
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Fig. 2. Fatigue curves produced by the exercise conditions. Three curves are shown for the imposed stretch condition. The pre-stretch curve represents tension values which were taken while the leg was contracting at an angle of 145 degrees, while both the post-stretch and the isometric curve represent tension values at 130 degrees. Maximal tension values from the 1 s stretch are plotted in the peakstretch curve
G. Kamen
78 Table
3. Summary of exercise data
Condition
Trials 1 + 2
Trials 27 + 28
%Fatigue
High-strength Low-strength
72.77 i 14.89 49.67 + 10.13
52.37 _+ 11.65 40.50 _+ 12.55
28.0 18.5
Pre-stretch (145~ High-strength Low-strength
51.05 + 10.60 38.84 _+ 12.30
36.08 + 11.55 25.91 + 7.16
29.3 33.3
Peak~stretch High-strength Low-strength
74.77 _+ 10.73 57.76 _+ 15.60
63.52 +_ 12.26 42.52 _+ 9.25
15.0 26.4
Post-stretch (130~) High-strength Low-strength
68.17 + 9.72 48.55 • 13.92
55.22 _+ 10.07 37.29 • 12.00
19.0 23.2
Isometric (130~
All values in kg (X + S.D.)
Exercise Conditions The exercise conditions resulted in significant decrements in knee extensor strength for both groups, as shown in Figure 2. In order to quantify the resultant degree of fatigue, the mean of the first two trials was compared with the mean of the last two trials. Using this comparison, it was observed that the strength of the high-strength group decreased 28.0% during the isometric exercise series, while that of the lows t r e n ~ group decreased 18.5% (see Table 3). An analysis of variance of trends using orthogonal polynomial coefficients (Grant, 1956) was conducted for each of the four fatigue curves (isometric-only, prestretch, peak,stretch, and post~stretch). This analysis revealed a significant overall trend for both groups in the isometric series with significant linear and quadratic components (F (1,22)=41.88; P < 0 . 0 0 1 and F (1,22)= 14.75; P < 0 . 0 1 , respectively). Ninety-one percent o f the overall trend for the high-strength group was accounted for by a linear component, while for the low-strength group, the linear trend component comprised 84% of the variance. These figures are similar to those reported in similar investigations (Kroll, 1967, 1973; Carlson, 1973), and serve to emphasize the importance of the linear overall trend in isometric fatigue curves of this type. The fact that the high-strength group fatigued to a greater extent than did the low-strength group as a result o f the isometric exercise (28.0% vs. 18.5%) is also in accord with earlier studies (Kroll, 1966, 1967). However, the low-strength individuals exhibited less endurance than the high-strength subjects when an imposed myotatic stretch was added m each of the 28 exercise trials. For example, for the peakstretch measure, the low-strength group evidenced a 26.4% strength decrement, while the high-strength group lost only 15.0%. Thus, it seems that the high-strength
Imposed Stretch and Fatigue
79
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Fig. 3. Increase in tension due to the imposed stretch condition9 Each point on the curve represents the difference between the maximal tension exerted during the stretch, and the maximal tension exerted during the corresponding trial of the isometric exercise condition
subjects fatigued less as a result of the isometric exercise performedwith an imposed stretch than did the low-strength group. Recall that the post-stretch strength scores were recorded as the maximal tension value attained during the 2 s interval following each imposed stretch, while the isometric-only fatigue curve resulted from the highest tension valuds recorded during each trial of the isometric exercise series performed on a separate test day. Both measures were taken at a knee angle of 130 degrees. Note that over the last ten trials, the post-stretch strength scores are higher than the isometric-only strength scores for the high-strength group, while the reverse is true for the low-strength group. It would seem that over the latter third of the exercise series, the stretch stimulus augmented the post-stretch tension scores of the hig-strength group, while diminishing the post-stretch tension scores of the low-strength group. The amount of tension gained during the exercise condition with the imposed stretch was computed for both groups over the 28 trials and is presented in Figure 3. Each point represents the value obtained by subtracting the maximum tension value during a trial of the isometric exercise condition from the corresponding tension value obtained during the 1 s imposed stretch (peak-stretch curve). The highstrength group gained significantly more tension from the eccentric exercise as the work task progressed, while the low-strength group seemed to lose some of the increased tension which the imposed stretch offered. Again, this is especially apparent over the last ten trials. In this interval, the peak-stretch strength means for the high-strength group were approximately 20% greater than the corresponding isometric-only strength means. By comparison, the tension increase due to the stretch for
80
G. Kamen
the low-strength subjects seemed to dwindle over the last third of the exercise regimen. Reference to Figure 2A shows that, for the low-strength subjects, the loss of imposed stretch strength seems to be due to a continual decline in the peak-stretch tension scores while the strength decrement in the isometric exercise series shows a plateau effect. A separate trend anaysis conducted over the two curves shown in Figure 3 revealed a significant groups X trials interaction term (F (27,594) -- 1.90; P < 0.01), indicating that while the high-strength group was generally increasing in amount of tension gained from the stretch over the 28 trials, the low-strength group was generally decreasing in imposed stretch strength.
Discussion Few investigations have been conducted in which maximum muscle tension is monitored during eccentric work. Komi and Viitasalo (1977) measured muscle tension before and after eccentric and concentric exercise involving the quadriceps musculature. Using a group of four physical education students, they reported strength decrements of 34.6% and 13.2% for eccentric and concentric work, respectively. Although the present experiment included an isometric exercise task while Komi and Viitasalo (1977) used concentric work exclusively, the trend toward a greater strength decrement due to the eccentric exercise was found to be the case only in the low-strength group. The main question to be answered then, would seem to be: How is it that high-strength individuals can fatigue more than low-strength subjects as a result of a series of isometric contractions, yet manifest less fatigue when an imposed stretch is added to each exercise trial? As mentioned at the beginning, elastic energy is liberated during eccentric exercise to be used for the concentric work which follows (Cavagna, 1977). In the present investigation, however, only an isometric contraction followed each eccentric exercise trial. It is difficult to account for the results of this investigation solely on the basis of the elastic energy schema. Similarly, Cavagna, Dusman and Margada (1968) were unable to account for all of the increased work performed after a period of muscle stretching. Moreover, some preliminary evidence has failed to show any enzymatic adaptation due to eccentric training in human subjects (BondePetersen and Knuttgen, 1970). There exists another area of research with relevance to the present discussion, which has apparently not been considered in previous work concerning eccentric contraction. This mechanism concerns the so-cailed "imposed stretch reflex" (Lagasse, 1974). Lagasse's experiment involved a bilateral contraction of both knee extensors. During the 5 s contraction, an imposed stretch was applied to one leg while the subject attempted to maintain maximum tension in both limbs. Results showed that during the stretch interval, an increase in tension was seen in the stretched leg, while a transient decrease in tension was observed in the contralateral knee extensors which were not stretched. In a related experiment, Morris (1974) reported that if the knee extensors of one leg are stretched while the knee flexors of the contralateral leg are contracting maximally, then there follows an increase in tension of the unstretched knee flexors during the stretch interval.
Imposed Stretch and Fatigue
81
The results obtained by Lagasse (1974) and Morris (1974) cannot be explained on the basis of present knowledge concerning eccentric contraction and elastic energy principles. Strong evidence, however, indicates the presence of an active neural mechanism. The muscle spindle, sensitive to the stretch stimulus, sends a barrage of impulses to the spinal cord. Spindle afferents then synapse directly with motoneurons, resulting in an increased tension output in the muscles of the stretched limb. Crossed-extensor reflex theory would dictate an inhibition of the contralateral hom o n y m o u s muscle, while facilitating the contralateral heteronymous musculature (Carpenter, 1971). This neural explanation would account for the results seen by Lagasse (1974) and Morris (1974). Perhaps an interpretation based upon the imposed stretch reflex would help explain the apparent increased endurance exhibited by the high-strength group during eccentric exercise. The finding that stretch reflexes are modulated by transcortical pathways (Marsden et al., 1972), and that supraspinal connections are potentiated in power-type, high-strength athletes (Milner-Brown et al., 1975; Stepanov and Burlakov, 1961), seems to lend credence to this inference regarding the presence of a neural factor. Whatever the explanation for these results, it is apparent that high-strength individuals, who m a y be at a disadvantage in isometric endurance when compared to a low-strength group, are seen to be superior in endurance when an exercise involving serial isometric contractions with an imposed stretch is administered.
Acknowledgements. The author wishes to thank Professor Walter Kroll for his critical review of the manuscript. Mr. Russell Ostrom assisted in the collection of the data.
References Asmussen, E.: Positive and negative muscular work. Acta Physiol. Scand. 28, 364--381 (1953) Asmussen, E.: Storage of elastic energy and mechanical efficiency of human muscles. Acta Physiol. Scand. Suppl. 440, 13 (1976) Bonde-Petersen, F., Knuttgen, H. G.: Effect of training with eccentric muscle contractions on human skeletal muscle metabolites. Aeta Physiol. Stand. 80, 16A-17A (1970) Carlson, B. R.: Cross transfer during flexor serial isometric trials. Am. Correct Ther. J. 27, 36-40 (1973) Carpenter, M. B.: Upper and lower motor neurons. In: Physiological Basis of Rehabilitation Medicine (J. A. Downey, R. C. Darling, eds.). Philadelphia: Saunders 1971 Cavagna, G. A.: Storage and utilization of dastic energy in skeletal muscle. In: Exercise and Sport Sciences Reviews (R. S. Hutton, ed.), pp. 89--129. Santa Barbara: Journal Publ. 1977 Cavagna, G. A., Citterio, G.: Effect of stretching on the elastic characteristics and the contractile component of frog striated muscle. J. Physiol. (Lond.) 239, 1-14 (1974) Cavagna, G. A., Dusman, B., Margaria, R.: Positive Work Done by a Previously Stretched Muscle. J. Appl. Physiol. 24, 21--32 (1968) Curtin, N. A., Svensson, S. M. M., Davies, R. E.: Force development and the braking mechanism in stretching activated muscle is not limited by the energy from ATP splitting. Fed. Proe. 29, 714 (1970) Fenn, W. O.: Frictional and kinetic factors in the work of sprint running. Am. J+ Physiol. 92, 582-611 (1930) Grant, D. A.: Analysis of variance tests in the analysis and comparison of curves. Psychol. Bull. 53, 141--154 (1956)
82
G. Kamen
Infante, A. A., Klaupiks, D., Davies, R. E.: Adenosine Triphosphate: Changes in Muscles Doing Negative Work. Science 144, 1577-1578 (1964) Joyce, G. C., Rack, P. M. H., Westbury, D. R.: The mechanical properties of cat soleus muscle during controlled lengthening and shortening movements. J. Physiol. (Lond.) 204, 461-474 (1969) Komi, P. V.: Relationship between muscle tension, EMG and velocity of contraction under concentric and eccentric work. In: New Developments in Electromyography and Clinical Neurophysiology (J. E. Desmedt, ed.), pp. 596-606. Basel: Karger 1973 Komi, P. V., and Viitasalo, J. T.: Changes in motor-unit acitvity and metabolism in human skeletal muscle during and after repeated eccentric and concentric contractions. Acta Physiol. Scand. 100, 246-254 (1977) Kroll, W.: Level of isometric strength and isometric endurance in repeated contractions. Res. Q. Am. Assoc. Health Phys. Educ. 37, 375-383 (1966) Kroll, W.: Isometric fatigue curves under varied intertrial recuperation periods. Res. Q. Am. Assoc. Health Phys. Educ. 39, 106--115 (1967) Kroll, W.: Effects of local muscular fatigue due to isotonic and isometric exercise upon fractionated reaction time components. J. Mot. Behav. 5, 81-93 (1973) Lagasse, P. P.: Muscle strength: Ipsilateral and contralateral effects of superimposed stretch. Arch. Phys. Med. Rehabil. 55, 305-310 (1974) Marsden, C. D., Merton, P. A., Morton, H. B.: Servo action in human voluntary movement. Nature 238, 140-143 (1972) Milner-Brown, H. S., Stein, R. B., Lee, R. G.: Synchronization of human motor units: Possible roles of exercise and supraspinal reflexes. Eleetroeneephalogr. Clin. Neurophysiol. 38, 245-254 (1975) Morris, A. F.: Myotatic reflex effects on bilateral reciprocal leg strength. Am. Correct Ther. J. 28, 24-29 (1974) Stepanov, A. S., Burlakov, M. L.: Electrophysiological investigation of fatigue in muscular activity. Sechenov physiol. J. U.S.S.R. 47, 43-47 (1961) Williams, M., Lissner, H. R.: Biomechanieal analysis of knee function. J. Am. Phys. Ther. Assoc. 43, 93--99 (1963) Accepted November 6, 1978
Applied Physiology
Eur. J. Appl. Physiol. 41, 73-82 (1979)
and Occupationa~ Physiology 9 Springer-Verlag t979
Serial Isometric Contractions Under Imposed Myotatic Stretch Conditions in High-strength and Low-strength Men Gary Kamen University of Massachusetts, Department of Exercise Science, Amherst, MA 01003, USA
Summary. The immediate effects of an imposed myotatic stretch on knee extensor force were studied in 12 high-strength and 12 low-strength men. Under nonfatigued pre-exercise conditions, significant tension increases of 6.5% for the high-strength group and 11.0% for low-strength subjects were observed as a result of the imposed stretch. An exercise treatment involving 28 serial isometric contractions, each of 5 s duration, with an intertrial rest period of 10 s was administered. This fatiguing exercise resulted in significant decrements in strength on the order of 28.0% and 18.5% for the high-strength and low-strength groups, respectively. A similar treatment which included a 1 s imposed myotatic stretch during each trial resulted in a greater strength decrement for the lowstrength group (26.4%) than for the high-strength subjects (15.0%). A neural factor involving the stretch reflex is tentatively suggested as a plausible explanation accounting for the observation that high-strength subjects fatigue faster than low-strength subjects under conditions of isometric exercise, while lowstrength subjects fatigue faster than high-strength individuals in isometric exercise which is performed with an imposed stretch.
Key words: Fatigue -- Reflex -- Eccentric contraction -- Negative work -- Elastic energy
A muscle is capable of generating greater tension during a lengthening contraction (eccentric contraction) than during either isometric or concentric contraction. Cavagna (1977) has recently reviewed the mechanisms responsible for the greater tension exhibited during eccentric exercise. In a movement requiring both positive and negative work stages, mechanical energy can be absorbed by the muscle during the period of negative work. This energy is either reutilized during the subsequent period of positive work, or is converted to heat if the muscle contraction ceases. One source of the extra elastic energy is believed to be the recoil of the stretched viscoelastic elements which takes place during the period of muscle shortening. It is predominantly chemical processes, however, which account for the greatest portion
0301-5548/79/0041/073/$ 02.00
74
G. Kamen
of the extra mechanical energy observed during the period of positive work (Cavagna, 1977). The idea that the contractile component is at least partially responsible for the added tension observed during eccentric contraction received added impetus when the sliding-filament theory was found to explain much of the experimental evidence in negative work experiments (Joyce et al., 1969). During muscle lengthening, the force exerted by the cross links between the actin and myosin filaments within the myofibrils is believed to increase due to the distortion caused by the movement (Joyce et al., !969). Cavagna and Citterio (1974)further suggested that the probability of these crossbridges breaking would further increase as muscle length increased. When an eccentric contraction is followed by muscle shortening, however, the most strained crossbridges with a high tendency to break, would recoil elastically, resulting in greater force during the interval of muscle shortening than would otherwise be possible (Asmussen, 1976; Cavagna and Citterio, 1974). The efficiency of negative work may be observed through several measurement procedures. Asmussen (1953) reported that eccentric work may be characterized by a smaller energy expenditure than concentric work. The ratio between total electromyographic (EMG) output and tension is lower in eccentric work than in concentric work (Komi, 1973). Furthermore, some preliminary data suggests that crossbridges can develop tension during muscle stretch without the splitting of ATP (Curtin et al., 1970; Infante et al., 1964). From the above evidence, one might question whether indeed, more endurance might be obtained through eccentric work. In an effort to clarify the circumstances surrounding the negative work schema, Komi and Viitasalo (1977) administered 40 maximal eccentric and concentric contractions to each of four individuals. Results showed that quadriceps muscle group EMG parameters were altered similarly for both exercise conditions. Moreover, muscle glycogen and blood lactate changed in a similar manner during both fatiguing exercise treatments. Fenn (1930) showed that resting muscles have very low stiffness, while maximal stiffness may be obtained with muscles lengthened while they are fully contracting. The present study was designed to incorporate this idea of muscle stiffness, by imposing a muscle stretch on a muscle group which is already contracting maximally. A second aim of the present experiment was to further elucidate the relationship between eccentric contraction and fatigue. Since eccentric work is characterized by a general economy of energy expenditure (Cavagna, 1977), it was hypothesized that a fatigue curve resulting from eccentric exercise might differ from that resulting from isometric exercise.
Methods
Subjects Male subjects (N = 24) were dividedinto two groups of 12 subjectseach based on maximalvoluntary contractile strength scores (MVC) of the right knee extensors. The physical characteristics of these subjects are listed in Table 1. Most of the high-strength individualswere weight lifters.
Imposed Stretch and Fatigue
75
Table I. Physical characteristics of the subjects Group
Height (cm)
Weight (kg)
Age (years)
High- strength
174.5
84.1
21.8
Low-strength
169.4
67.3
23.7
Procedures The experiment was designed to compare subject response to two different exercise regimens which were intended to produce local muscular fatigue. One exercise regimen involved only isometric contractions, while the other exercise condition involved the administration of an imposed myotatic stretch upon a muscle group which was already contracting maximally. Each subject reported to the laboratory on two different occasions. During each test session, maximal knee extension strength was measured at 130 and 145 degrees of full knee extension. Following a 5 rnin rest, five imposed stretch trials were given. The individual began an isometric contraction at a knee angle of 145 degrees and, after 2 s, a constant torque motor pulled the leg back to 130 degrees at a rate of 16 deg/s. The stretch lasted approximately 1 s. Each individual was told to resist the pull as strongly as possible. When the motor stopped, the subject maintained the isometric contraction at 130 degrees for 2 s. Since the time necessary to pull the leg back was constant, it was possible to obtain three tension measures on each imposed stretch trial. One measure (pre-streteh) was recorded as the maximum tension prior to the pull. A second measure (peak-stretch) was taken as the maximum tension during the stretch. The last measure (post-stretch) was taken as the maximum tension immediately after the stretch ended. Thus the entire contraction lasted for five seconds.
Exercise After the pre-exercise measures, the subject was given one of two exercise regimens. On one test day, 28 serial isometric contractions were administered. Each contraction was 5 s in duration with an intertrial rest period of 10 s. The subjects performed the exercise at 130 degrees. For the second exercise treatment, 28 maximal 5 s contractions were given with an imposed stretch delivered on each trial. The intertrial rest period remained 10 s between trials. As with the pre-exereise imposed stretch trials, the subject contracted maximally at a pre-stretch angle of 145 degrees for 2 s, then came the onesecond stretch, and finally a post-stretch interval of 2 s at 130 degrees. Thus, three fatigue curves were obtained from this treatment condition as strength measures were obtained just prior to each imposed stretch (pre-stretch), during the stretch (peak-stretch), and immediately following the stretch (poststretch) while the subject held the contraction for 2 s at 130 degrees. A summary of the treatment conditions is given in Figure 1.
Results
Reliability Reliability was assessed by the intraclass correlation analysis of variance procedure. T h e a s s o c i a t e d c o r r e l a t i o n coefficients r a n g e d f r o m 0.85 t o 0.96 f o r t h e five pree x e r c i s e s t r e n g t h m e a s u r e s . P a i r e d t-tests r e v e a l e d n o s i g n i f i c a n t d i f f e r e n c e s a m o n g t h e b a s e l i n e s t r e n g t h m e a s u r e s b e t w e e n d a y s o n e a n d two.
76
G. Kamen TEST
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SCHEDULE TRIALS TRIALS IMPOSED
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Fig. 1. A--C. Summary of the measurement schedule. Conditions A and B were administered on both test days. Only one exercise condition was given on each day
Table 2. Pre-exercise strength measuresa Measure
130 degrees 145 degrees Pre-stretch (145 degrees) Peak-stretch Post-stretch (130 degrees)
High-strength
75.7 63.7 52.9 80.6 72.8
Low-strength
sd
X
sd
13.8 11.3 11.8 11.5 11.0
51.8 42.1 39.8 57.5 51.8
12.2 10.6 10.7 13.3 12.5
a All values in kg
Pre-Exercise Conditions The baseline mean strength at a knee angle of 130 degrees was greater than that at 145 degrees, as shown in Table 2. This is in accordance with previous research demonstrating a mechanical advantage at this lower angle (Williams and Lissner, 1963). Mean strength values for both groups are listed in Table 2. In order to assess the effects of the imposed myotatic stretch, the maximal tension recorded during the stretch (the peak stretch measure), was compared to the maximal isometric strength measure recorded previously at a knee angle of 130 degrees. As a result of the imposed myotatic stretch, isometric knee extensor strength was increased significantly during the stretch interval (F (1,22)= 23.29; P < 0.001). When compared with the baseline 130-degree isometric strength measure, this strength increase was on the order of 6.5% for the high-strength subjects, 11.0% for the low-strength group. Lagasse (1974) and Morris (1974) reported increases in strength of 6.9% and 25.2%, respectively, for a group of normal individuals. Although the low-strength group evidenced a greater gain in tension from the imposed stretch than did the high-strength group, this difference was not significant as indicated by the non-significant groups X conditions interaction term (F (1,22) = 0.04; P > 0.05).
Imposed Stretch and Fatigue
77
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Fig. 2. Fatigue curves produced by the exercise conditions. Three curves are shown for the imposed stretch condition. The pre-stretch curve represents tension values which were taken while the leg was contracting at an angle of 145 degrees, while both the post-stretch and the isometric curve represent tension values at 130 degrees. Maximal tension values from the 1 s stretch are plotted in the peakstretch curve
G. Kamen
78 Table
3. Summary of exercise data
Condition
Trials 1 + 2
Trials 27 + 28
%Fatigue
High-strength Low-strength
72.77 i 14.89 49.67 + 10.13
52.37 _+ 11.65 40.50 _+ 12.55
28.0 18.5
Pre-stretch (145~ High-strength Low-strength
51.05 + 10.60 38.84 _+ 12.30
36.08 + 11.55 25.91 + 7.16
29.3 33.3
Peak~stretch High-strength Low-strength
74.77 _+ 10.73 57.76 _+ 15.60
63.52 +_ 12.26 42.52 _+ 9.25
15.0 26.4
Post-stretch (130~) High-strength Low-strength
68.17 + 9.72 48.55 • 13.92
55.22 _+ 10.07 37.29 • 12.00
19.0 23.2
Isometric (130~
All values in kg (X + S.D.)
Exercise Conditions The exercise conditions resulted in significant decrements in knee extensor strength for both groups, as shown in Figure 2. In order to quantify the resultant degree of fatigue, the mean of the first two trials was compared with the mean of the last two trials. Using this comparison, it was observed that the strength of the high-strength group decreased 28.0% during the isometric exercise series, while that of the lows t r e n ~ group decreased 18.5% (see Table 3). An analysis of variance of trends using orthogonal polynomial coefficients (Grant, 1956) was conducted for each of the four fatigue curves (isometric-only, prestretch, peak,stretch, and post~stretch). This analysis revealed a significant overall trend for both groups in the isometric series with significant linear and quadratic components (F (1,22)=41.88; P < 0 . 0 0 1 and F (1,22)= 14.75; P < 0 . 0 1 , respectively). Ninety-one percent o f the overall trend for the high-strength group was accounted for by a linear component, while for the low-strength group, the linear trend component comprised 84% of the variance. These figures are similar to those reported in similar investigations (Kroll, 1967, 1973; Carlson, 1973), and serve to emphasize the importance of the linear overall trend in isometric fatigue curves of this type. The fact that the high-strength group fatigued to a greater extent than did the low-strength group as a result o f the isometric exercise (28.0% vs. 18.5%) is also in accord with earlier studies (Kroll, 1966, 1967). However, the low-strength individuals exhibited less endurance than the high-strength subjects when an imposed myotatic stretch was added m each of the 28 exercise trials. For example, for the peakstretch measure, the low-strength group evidenced a 26.4% strength decrement, while the high-strength group lost only 15.0%. Thus, it seems that the high-strength
Imposed Stretch and Fatigue
79
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subjects fatigued less as a result of the isometric exercise performedwith an imposed stretch than did the low-strength group. Recall that the post-stretch strength scores were recorded as the maximal tension value attained during the 2 s interval following each imposed stretch, while the isometric-only fatigue curve resulted from the highest tension valuds recorded during each trial of the isometric exercise series performed on a separate test day. Both measures were taken at a knee angle of 130 degrees. Note that over the last ten trials, the post-stretch strength scores are higher than the isometric-only strength scores for the high-strength group, while the reverse is true for the low-strength group. It would seem that over the latter third of the exercise series, the stretch stimulus augmented the post-stretch tension scores of the hig-strength group, while diminishing the post-stretch tension scores of the low-strength group. The amount of tension gained during the exercise condition with the imposed stretch was computed for both groups over the 28 trials and is presented in Figure 3. Each point represents the value obtained by subtracting the maximum tension value during a trial of the isometric exercise condition from the corresponding tension value obtained during the 1 s imposed stretch (peak-stretch curve). The highstrength group gained significantly more tension from the eccentric exercise as the work task progressed, while the low-strength group seemed to lose some of the increased tension which the imposed stretch offered. Again, this is especially apparent over the last ten trials. In this interval, the peak-stretch strength means for the high-strength group were approximately 20% greater than the corresponding isometric-only strength means. By comparison, the tension increase due to the stretch for
80
G. Kamen
the low-strength subjects seemed to dwindle over the last third of the exercise regimen. Reference to Figure 2A shows that, for the low-strength subjects, the loss of imposed stretch strength seems to be due to a continual decline in the peak-stretch tension scores while the strength decrement in the isometric exercise series shows a plateau effect. A separate trend anaysis conducted over the two curves shown in Figure 3 revealed a significant groups X trials interaction term (F (27,594) -- 1.90; P < 0.01), indicating that while the high-strength group was generally increasing in amount of tension gained from the stretch over the 28 trials, the low-strength group was generally decreasing in imposed stretch strength.
Discussion Few investigations have been conducted in which maximum muscle tension is monitored during eccentric work. Komi and Viitasalo (1977) measured muscle tension before and after eccentric and concentric exercise involving the quadriceps musculature. Using a group of four physical education students, they reported strength decrements of 34.6% and 13.2% for eccentric and concentric work, respectively. Although the present experiment included an isometric exercise task while Komi and Viitasalo (1977) used concentric work exclusively, the trend toward a greater strength decrement due to the eccentric exercise was found to be the case only in the low-strength group. The main question to be answered then, would seem to be: How is it that high-strength individuals can fatigue more than low-strength subjects as a result of a series of isometric contractions, yet manifest less fatigue when an imposed stretch is added to each exercise trial? As mentioned at the beginning, elastic energy is liberated during eccentric exercise to be used for the concentric work which follows (Cavagna, 1977). In the present investigation, however, only an isometric contraction followed each eccentric exercise trial. It is difficult to account for the results of this investigation solely on the basis of the elastic energy schema. Similarly, Cavagna, Dusman and Margada (1968) were unable to account for all of the increased work performed after a period of muscle stretching. Moreover, some preliminary evidence has failed to show any enzymatic adaptation due to eccentric training in human subjects (BondePetersen and Knuttgen, 1970). There exists another area of research with relevance to the present discussion, which has apparently not been considered in previous work concerning eccentric contraction. This mechanism concerns the so-cailed "imposed stretch reflex" (Lagasse, 1974). Lagasse's experiment involved a bilateral contraction of both knee extensors. During the 5 s contraction, an imposed stretch was applied to one leg while the subject attempted to maintain maximum tension in both limbs. Results showed that during the stretch interval, an increase in tension was seen in the stretched leg, while a transient decrease in tension was observed in the contralateral knee extensors which were not stretched. In a related experiment, Morris (1974) reported that if the knee extensors of one leg are stretched while the knee flexors of the contralateral leg are contracting maximally, then there follows an increase in tension of the unstretched knee flexors during the stretch interval.
Imposed Stretch and Fatigue
81
The results obtained by Lagasse (1974) and Morris (1974) cannot be explained on the basis of present knowledge concerning eccentric contraction and elastic energy principles. Strong evidence, however, indicates the presence of an active neural mechanism. The muscle spindle, sensitive to the stretch stimulus, sends a barrage of impulses to the spinal cord. Spindle afferents then synapse directly with motoneurons, resulting in an increased tension output in the muscles of the stretched limb. Crossed-extensor reflex theory would dictate an inhibition of the contralateral hom o n y m o u s muscle, while facilitating the contralateral heteronymous musculature (Carpenter, 1971). This neural explanation would account for the results seen by Lagasse (1974) and Morris (1974). Perhaps an interpretation based upon the imposed stretch reflex would help explain the apparent increased endurance exhibited by the high-strength group during eccentric exercise. The finding that stretch reflexes are modulated by transcortical pathways (Marsden et al., 1972), and that supraspinal connections are potentiated in power-type, high-strength athletes (Milner-Brown et al., 1975; Stepanov and Burlakov, 1961), seems to lend credence to this inference regarding the presence of a neural factor. Whatever the explanation for these results, it is apparent that high-strength individuals, who m a y be at a disadvantage in isometric endurance when compared to a low-strength group, are seen to be superior in endurance when an exercise involving serial isometric contractions with an imposed stretch is administered.
Acknowledgements. The author wishes to thank Professor Walter Kroll for his critical review of the manuscript. Mr. Russell Ostrom assisted in the collection of the data.
References Asmussen, E.: Positive and negative muscular work. Acta Physiol. Scand. 28, 364--381 (1953) Asmussen, E.: Storage of elastic energy and mechanical efficiency of human muscles. Acta Physiol. Scand. Suppl. 440, 13 (1976) Bonde-Petersen, F., Knuttgen, H. G.: Effect of training with eccentric muscle contractions on human skeletal muscle metabolites. Aeta Physiol. Stand. 80, 16A-17A (1970) Carlson, B. R.: Cross transfer during flexor serial isometric trials. Am. Correct Ther. J. 27, 36-40 (1973) Carpenter, M. B.: Upper and lower motor neurons. In: Physiological Basis of Rehabilitation Medicine (J. A. Downey, R. C. Darling, eds.). Philadelphia: Saunders 1971 Cavagna, G. A.: Storage and utilization of dastic energy in skeletal muscle. In: Exercise and Sport Sciences Reviews (R. S. Hutton, ed.), pp. 89--129. Santa Barbara: Journal Publ. 1977 Cavagna, G. A., Citterio, G.: Effect of stretching on the elastic characteristics and the contractile component of frog striated muscle. J. Physiol. (Lond.) 239, 1-14 (1974) Cavagna, G. A., Dusman, B., Margaria, R.: Positive Work Done by a Previously Stretched Muscle. J. Appl. Physiol. 24, 21--32 (1968) Curtin, N. A., Svensson, S. M. M., Davies, R. E.: Force development and the braking mechanism in stretching activated muscle is not limited by the energy from ATP splitting. Fed. Proe. 29, 714 (1970) Fenn, W. O.: Frictional and kinetic factors in the work of sprint running. Am. J+ Physiol. 92, 582-611 (1930) Grant, D. A.: Analysis of variance tests in the analysis and comparison of curves. Psychol. Bull. 53, 141--154 (1956)
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Infante, A. A., Klaupiks, D., Davies, R. E.: Adenosine Triphosphate: Changes in Muscles Doing Negative Work. Science 144, 1577-1578 (1964) Joyce, G. C., Rack, P. M. H., Westbury, D. R.: The mechanical properties of cat soleus muscle during controlled lengthening and shortening movements. J. Physiol. (Lond.) 204, 461-474 (1969) Komi, P. V.: Relationship between muscle tension, EMG and velocity of contraction under concentric and eccentric work. In: New Developments in Electromyography and Clinical Neurophysiology (J. E. Desmedt, ed.), pp. 596-606. Basel: Karger 1973 Komi, P. V., and Viitasalo, J. T.: Changes in motor-unit acitvity and metabolism in human skeletal muscle during and after repeated eccentric and concentric contractions. Acta Physiol. Scand. 100, 246-254 (1977) Kroll, W.: Level of isometric strength and isometric endurance in repeated contractions. Res. Q. Am. Assoc. Health Phys. Educ. 37, 375-383 (1966) Kroll, W.: Isometric fatigue curves under varied intertrial recuperation periods. Res. Q. Am. Assoc. Health Phys. Educ. 39, 106--115 (1967) Kroll, W.: Effects of local muscular fatigue due to isotonic and isometric exercise upon fractionated reaction time components. J. Mot. Behav. 5, 81-93 (1973) Lagasse, P. P.: Muscle strength: Ipsilateral and contralateral effects of superimposed stretch. Arch. Phys. Med. Rehabil. 55, 305-310 (1974) Marsden, C. D., Merton, P. A., Morton, H. B.: Servo action in human voluntary movement. Nature 238, 140-143 (1972) Milner-Brown, H. S., Stein, R. B., Lee, R. G.: Synchronization of human motor units: Possible roles of exercise and supraspinal reflexes. Eleetroeneephalogr. Clin. Neurophysiol. 38, 245-254 (1975) Morris, A. F.: Myotatic reflex effects on bilateral reciprocal leg strength. Am. Correct Ther. J. 28, 24-29 (1974) Stepanov, A. S., Burlakov, M. L.: Electrophysiological investigation of fatigue in muscular activity. Sechenov physiol. J. U.S.S.R. 47, 43-47 (1961) Williams, M., Lissner, H. R.: Biomechanieal analysis of knee function. J. Am. Phys. Ther. Assoc. 43, 93--99 (1963) Accepted November 6, 1978
