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Adaptation in skeletal muscle following

strength training

Article in Journal of applied physiology: respiratory, environmental and exercise physiology · February 1979
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Adaptations in skeletal muscle following
strength training

D. L. COSTILL, E. F. COYLE, W. F. FINK,

G. R. LESMES, AND F. A. WITZMANN
Human Performance Laboratory, Ball State University, Muncie, Indiana 47306

COSTILL, D. L., E. F. COYLE, W. F. FINK, G. R. LESMES, risks and stresses associated with this research before
AND F. A. WITZMANN. Adaptations in skeZetaZ muscle follow- giving their written consent to participate.
ing strength training. J. Appl. Physiol.: Respirat. Environ. Measurements. Testing and training of the knee
Exercise Physiol. 46(l): 96-99, 1979. -Five men were studied extensor muscles were conducted with the aid of an
before and after 7 wk of isokinetic strength training to
determine its effects on muscle enzyme activities and fiber
isokinetic dynamometer (Cybex II, Lumex, Inc.) as
composition. One of the subject’s legs was trained using 10 previously described by Thorstensson (17). Before and
repeated 6-s maximal work bouts, while the other leg per- after training, each of the subject’s legs was tested for
formed repeated 30-s maximal knee extension exercise. The peak torque at knee extension velocities ranging from
total work accomplished by each leg was constant. Training 4 1.05 to 5.23 rad/s. In addition, an anaerobic performance
times/wk achieved similar gains in peak torque for both legs test was done with each leg. This test consisted of
at the training velocity (3.14 rad/s) and at slower speeds. maximal knee flexions and extensions at 3.14 rad/s for
Fatigability of the knee extensor muscles, as measured by a 60 s. Work output was summed every 10 s during this
60-s exercise test, was similar in both legs after training. test.
Biopsy specimens showed significant changes in the % of the Four biopsies were obtained from the vastus lateralis
muscle area composed of type I and IIa fibers as a result of
muscle of each leg before and after training. One portion
both strength training programs. In terms of muscle enzymes,
only the 30 s exercise program resulted in elevated glycolytic,
of the specimen was positioned in a mounting medium
ATP-CP and mitochondrial activities. Despite these changes, and frozen in isopentane cooled to the temperature of
none of the parameters measured were found to be related to liquid nitrogen for histochemical analysis. The remain-
the gains in either muscle strength or fatigability during ing biopsy material was weighed, frozen in liquid nitro-
maximal isokinetic contractions. gen and later assayed for muscle enzyme activities.
The myofibrillar ATPase method (4, 16) was used for
muscle enzymes; muscle histochemistry; muscle fatigue muscle fiber classification. Tissue slices (10 pm thick)
were preincubated at a pH 4.3 and 4.6, and the staining
reaction carried out at a pH 9.4. Muscle fibers were
ADAPTATIONS IN SKELETAL MUSCLE following endurance subsequently classified as types I (slow twitch oxida-
training are well documented (6, 10) and demonstrate tive), IIa (fast twitch, oxidative), and IIb (fast twitch,
an enhanced capacity for oxidative metabolism. Adjust- glycolytic). Fiber areas were determined from serial
ments to strength training, on the other hand, are not cross sections of each muscle sample after staining for
so well defined. The intent of the present investigation NADH-diaphorase (15). The mean muscle fiber area for
is to assess the effects of two modes of maximal isoki- each sample was determined by averaging the cross-
netic training on muscle enzyme activities and fiber sectional areas of 20 fibers that had been photographi-
composition. A comparison has been made between cally reproduced and measured by planimetry.
training programs that required 6- and 30-s bouts of Enzyme anaZyses. Muscle samples analyzed for succi-
maximal isokinetic contractions of the knee extensor nate dehydrogenase (SDH), total (cytoplasmic plus mi-
muscles. The muscle enzymes selected for study are tochondrial) malate dehydrogenase (MDH), lactate de-
representative of the metabolic systems responsible for hydrogenase (LDH), and total phosphorylase were first
energy derivation during anaerobic (i.e., creatine phos- homogenized at 4°C in an 0.1 M triethanolamine (TEA)
phokinase, myokinase, phosphorylase, phosphofructo- buffer (pH 7.6; 0.5% bovine serum albumin (BSA) 5 mM
kinase, and lactate dehydrogenase) and aerobic (i.e., 2-mercaptoethanol). We have noted that the use of this
succinate dehydrogenase and malate dehydrogenase) buffer results in SDH activity that is 0.5 times that
muscular effort. obtained with a PO, homogenizing buffer. The propor-
tionality of the SDH activity produced with the TEA
METHODS
and PO, buffers is constant and does not alter the
interpretation of the findings in the present study. The
Five healthy males served as subjects in this investi- reaction media and fluorometric methods for these en-
gation. The age, height and weight for the men aver- zyme assays have been detailed earlier (3, 11).
aged (tSE)23.6 t 1.3 yr, 177.2 t 2.6 cm, and77.3 t 4.7 Homogenates for phosphofructokinase (PFK) were
kg, respectively. All subjects were fully informed of the prepared in 100 mM potassium phosphate buffer (pH
96 0161-7567/79/0000-0000$01.25 Copyright 0 1979 the American Physiological Society
MUSCLE ENZYME ACTIVITIES FOLLOWING STRENGTH TRAINING 97

8.2), containing 10 mM glutathione, 0.5 mM ATP, 5 mM 300

MgSOd, and 30 mM NaF (1). The fluorometric determi-
nation of NADH disappearance was performed at 25°C
using a reaction cocktail described by Mansour et al. 250
(12)
Creatine phosphokinase (CPK) and myokinase (MK)
activities were determined fluorometrically on whole
muscle homogenized in a TEA-BSA buffer (see SDH
method above), containing 10 mM cysteine or 1.0 mM
glutathione. The MK reaction was performed in a
cocktail containing ADP (0.2 mM), MgCl, (5 mM),
glucose (2 mM), NADP + (0.1 mM), 5 pg/ml hexoki-
nase, and 1 pg/ml glucose-6-phosphate dehydrogenase.
After determining the MK reaction rate, creatine phos-
phate (CP) was added to the mixture to measure the
activity of CPK (11).
Training. The subjects trained each leg 4 times/wk
for a period of 7 wk. One leg (6 s) was trained using 10
repeated 6-s maximal knee extensions, while the other
leg (30 s) performed repeated 30-s maximal knee exten-
sion exercise. The rest intervals between the 6- and 30-s
bouts was 114 s and 20 min, respectively. The 6-s leg TIME (sec.)
was exercised first during each training session, and FIG.1. Mean power values for each 10 s of maximal anaerobic
the work bouts for the 30-s leg were repeated until the performance test.
total work performed was equal to that produced by the
6-s leg. All training bouts were executed at a velocity of TABLE 1. Muscle fiber composition be fore
3.14 rad/s (18O”/s). The rationale for selecting training and after training
bouts of 6 and 30 s was based on our efforts to stress
6-s Leg 30-s Leg
both systems of anaerobic ATP generation (ATP-CP
and glycolytic systems). In preliminary studies we noted Pre Post Pre Post

little or no muscle lactate increase following 6 s of %Fiber type

maximal isokinetic exercise (unpublished observations). I 44.8 41.8 48.2 46.8
+5.3 k4.7 k5.3 +4.2
The 30-s maximal work, however, increased muscle IIa 30.0 34.8 28.4 32.0
lactate from a resting level of 0.9 to 19.4 mmol/kg wet t5.1 t3.3 k4.1 23.5
wt. These data suggest that the 6 s of maximal exercise IIb 25.2 23.4 23.4 21.2
was achieved principally at the expense of the ATP-CP +2.3 22.4 k3.3 +2.4
systems, while the 30 s bout stressed both the ATP-CP Fiber areas, pm2
I 6,106 5,887 4,865 4,959
and glycolytic systems. +541 -+527 1~381 +283
Differences between means were tested for signifi- IIa 7,370 7,318 6,233 7,592
cance with a t test for paired observations. + 834 t700 + 563 *645
IIb 6,766 7,116 5,773 5,628
+614 2650 ?419 t715
RESULTS %Fiber area
41.6 36.6* 42.6 34.8*
As a result of training, the subjects showed a signifi- t7.1 26.3 k4.5 k4.9
cant (P < 0.05) increase in peak torque for both legs (6 IIa 32.8 37.2* 32.6 44.6*
and 30 s) at the velocity used during training (3.14 rad/ +6.5 +1.3 t5.0 k4.6
IIb 25.6 26.0 24.8 20.2
s) and at slower speeds. Improvements in peak torque k3.3 +2.7 k3.0 k1.5
ranged from a high of 14% (0 rad/s) to a low of 4% at %Fiber area ratio
3.14 rad/s. No differences, however, were found between IIa/I 0.79 1.02* 0.77 1.28*
the strength gains of the 6-s and 30-s legs. IIb/I 0.62 0.71 0.58 0.58
Figure 1 illustrates that during the 60-s maximal IIa/IIb 1.28 1.43* 1.31 2.21*
exercise test, both the 6-s and 30-s legs increased (P < Values are means + SE for legs exercised with repeated bouts of
0.05) their mean power output as a result of training. 6- and 30-s maximal isokinetic contractions. %Fiber area represents
the fraction of the total area of the muscle section that was composed
This apparent training advantage was noted only dur- of each fiber type. * Significant (P < 0.05) differences between
ing the first 30 s of the test. Thereafter, the slope of this means of pre- and posttraining.
“fatigue” curve and the mean power values were the
same in both legs before and after training. tional area represented by each fiber type, however, the
Mean (t SE) muscle fiber characteristics measured type I fibers showed a decrease (P < 0.05) of 5.0 and
before and after training are presented in Table 1. 7.8% in the 6-s and 30-s legs, respectively. At the same
Statistically, the percentage of type I, Ha, and IIb fibers time, the type IIa fibers in both legs increased signifi-
did not change with either form of training. When cantly (P < 0.05). The type IIb fibers remained un-
computed as the nercentage of the muscle’s cross-sec- changed with training. Neither the 6-s nor 30-s training
98 COSTILL ET AL.

TABLE 2. Muscle enzyme activities result of the incre ased en .ergy requirements imposed bY
before and after training the hi .gher power output in the trained muscles duri %
the first half of the performance test. Recent studies
(13), however, have demonstrated an increase in muscle
ATP and CP concentrations with strength training,
Phosphorylase 18.3 17.4 18.1 19.6* which could compensate for the greater energy demands
k2.0 +1.6 22.0 a.9 at these higher power outputs.
Phosphofructokinase 64.5 69.1* 61.2 74.6* Another possible explanation for the more rapid de-
+3.2 +2.8 +2.4 k2.8
Lactate 321 329 295 318
cline in me-an power by the trained muscles might be
dehydrogenase +32 +28 +26 +22 attributed to the influence of pH on maximal muscular
Creatine 611 603 609 702* force. Hill (9) in 1940 demonstrated that the formation
phosphokinase +44 +47 k46 AZ53 of lactic acid in response to stimulation stopped when
Myokinase 309 308 309 350*
+18 *14 +14 +5
muscle pH dropped to roughly 6.3. More recently Her-
Malate 44.0 46.0 47.1 53.7* mansen and Osnes (8) have measured the pH in exercis-
dehydrogenase +2.3 22.5 k1.4 22.6 ing human skeletal muscle and have reported values as
Succinate 4.0 4.1 4.5 5.0* low as 6.35 at exhaustion. Because lowering cellular pH
dehydrogenase kO.7 +0.6 +0.6 +0.6 is known to slow the rate of glycolysis, it might be
Values are means + SE, in pmollg min, for legs exercised with
l
argued that the decrease in muscle pH which accompa-
repeated 6-and 30-s maximal isokinetic contractions. * Significant nied the anaerobic performance test could have limited
(P < 0.05) difference between means of pre- and posttraining.
ATP synthesis by reducing the effectiveness of the
glycolytic enzymes. If this were the case, then one
programs had any effect on the cross sectional areas of might expect to see a lesser rate of fatigue in the 30-s-
any of the fiber types (I, IIa, IIb). trained leg, which shows the greatest enzymatic poten-
Muscles from the 6-s-trained leg showed little change tial for glycolysis. The fact that both the 30- and 6-s
in enzyme activities (Table 2). Only muscle PFK activ- trained legs showed similar rates of fatigue suggests
ity increased significantly (P < 0.05). The 30 s exercise that the factor responsible for muscular exhaustion may
program, on the other hand, resulted in elevated (P < be independent of ATP resynthesis.
0.05) glycolytic, ATP-CP, and Krebs cycle enzyme activ- Fuchs et al. (5) have suggested that increased hydro-
ities (Table 2). Of the muscle enzymes measured, only gen ion concentration in muscle reduces the binding
LDH activity failed to increase with the 30-s training capacity for Ca2+ through an inactivation of the fibrillar
program. protein, troponin. Recent unpublished studies by Her-
mansen (personal communication) have demonstrated
that in skinned rabbit muscle fibers, a decrease in
DISCUSSION
muscle pH results in a marked loss of contractile
There are 3 major findings of this research. The first tension that persists despite the availability of ATP.
is that two 30-s maximal exercise bouts/day (4 days/wk) Thus, the loss of mean power illustrated in Fig. 1 may
are sufficient stimulus to increase the activities of be due, in Pad 9to the effects of increasing hydrogen ion
muscle phosphorylase, PFK, CPK, MK, MDH, and concentration on the muscle’s contractile mechanism,
SDH. When the same quantity of work, however, was rather than on the glycolytic ATP resynthesis, per se.
divided into repeated 6-s exercise bouts, only PFK It is interesting to note that during the final 30 s of
activity increased. Thus, with the exception of PFK the anaerobic performance test bo th the trained and
activity, the stimulus responsible for increasing muscle untrained muscles produced the same mean power
enzyme activities seems to be related to the duration of values. If we adhere to the concept that a decrease in
each maximal exercise bout rather than the quantity of pH was responsible for the decline in mean power, then
work performed by the muscle. we might speculate that its influence was greatest in
The second major observation in this investigation the pH sensitive fast twitch (type II) muscle fibers (2).
was that, while the muscle enzyme activities increased Thus, the rapid fatigue noted in the first 30 s of the test
in the 30-s leg, the muscle’s resistance to fatigue was after training may be due to a decline in tension
the same as the 6-s-trained leg which showed no in- generated by the type II fibers. The mean power pro-
crease in muscle enzymes (Fig. 1 and Table 2). Although duced in the final 30 s of the test both before and after
an increase in glycolytic and ATP-CP enzymes is gen- training may simply reflect the tension and lesser
erally interpreted to reflect an enhanced anaerobic fatigability of the slow twitch (type I) fibers. This
potential, the present data demonstrate that fatigue concept is supported by fatigue and muscle glycogen
during repeated maximal contractions is independent of depletion studies conducted during repeated fast volun-
the muscle’s capacity to generate ATP via anaerobic tary contractions in man (14, 19). These studies demon-
metabolism. Despite the greater strength exhibited in strated that the decline in peak torque which accompa-
the early seconds of the 60 s anaerobic performance test, nied repeated maximal contractions was positively cor-
mean power declined so rapidly that the trained legs related (r = 0.86) with the percentage of type II fibers
exhibited the same mean power as the untrained legs in the contracting muscle.
after 30-40 s of effort (Fig. 1). One possible explanation The third principal finding of this research was that
for this greater rate of decline in the trained muscles is the biopsy specimens showed a significant (P < 0.05)
a more rapid depletion of muscle ATP and CP as a change in the fiber composition of the vastus lateralis
MUSCLE ENZYME ACTIVITIES FOLLOWING STRENGTH TRAINING 99

muscle after 7 wk of strength training (Table 1). There These studies of strength training demonstrate signif-
was an increase in the IIa to I and IIa to IIb fiber area icant enzymatic changes and modifications in the com-
ratios of both the 30- and 6-s-trained muscles. Since position (fiber area ratios) of skeletal muscle. Despite
neither the percentage nor cross sectional areas of the these adaptations, none of the parameters measured
type I, IIa, and IIb fibers show statistical changes with was found to be related to either muscle strength or
training, caution should be used in speculating in the fatigability during maximal isokinetic contractions.
significance of the changes in fiber area ratios. It These data suggest that fatigue in maximal muscular
should, however, be noted that Thorstensson (18) also effort is not dependent on the muscle’s anaerobic poten-
observed a selective hypertrophy of the fast twitch (type tial as measured by glycolytic and ATP-CP enzyme
II) fibers after 8 wk of maximal isokinetic training. The activities.
changes seen in our muscle fiber composition (fiber area
ratios) with strength training may be due to an increase This research was supported by National Institutes of Health
Grant HL-20408; Lumex Inc.; and the Ball State University Research
in type IIa fibers, a shift in type I and IIb fibers to type Committee Grant Res. 79-1976.
IIa fibers, or merely chance error of the measurement. Current address: E. F. Coyle, Dept. of Physical Education,
It is, however, interesting to note a recent study by University of Arizona, Tucson, AZ 85724; G. R. Lesmes, Dept. of
Gonyea et al. (7) which clearly demonstrated muscle Physical Education, Northeastern Illinois State University, Chi-
cago, IL 60625
fiber splitting in the forelimb of the cat after strength
training. Received 4 April 1978; accepted in final form 8 August 1978.

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