Content uploaded by Paul DeVita
Author content
All content in this area was uploaded by Paul DeVita
Content may be subject to copyright.
81:1677-1682, 1996. ;J Appl Physiol
Devita, Line Dempsey and Jean Lambert
Tibor Hortobágyi, Jason Barrier, David Beard, John Braspennincx, Peter Koens, Paul
lengthening than maximal shortening
Greater initial adaptations to submaximal muscle
You might find this additional info useful...
26 other HighWire-hosted articles: This article has been cited by
http://jap.physiology.org/content/81/4/1677#cited-by
including high resolution figures, can be found at: Updated information and services
http://jap.physiology.org/content/81/4/1677.full
can be found at: Journal of Applied Physiology about Additional material and information
http://www.the-aps.org/publications/jappl
This information is current as of June 3, 2013.
Physiological Society. ISSN: 8750-7587, ESSN: 1522-1601. Visit our website at http://www.the-aps.org/.
the American Physiological Society, 9650 Rockville Pike, Bethesda MD 20814-3991. Copyright © 1996 the American
especially those papers emphasizing adaptive and integrative mechanisms. It is published 12 times a year (monthly) by
publishes original papers that deal with diverse area of research in applied physiology,Journal of Applied Physiology
by guest on June 3, 2013http://jap.physiology.org/Downloaded from
Greater initial adaptations to submaximal
muscle lengthening than maximal shortening
TIBOR HORTOBA
´
GYI, JASON BARRIER, DAVID BEARD, JOHN BRASPENNINCX,
PETER KOENS, PAUL DEVITA, LINE DEMPSEY, AND JEAN LAMBERT
Biomechanics Laboratory and Physical Therapy Department,
East Carolina University, Greenville, North Carolina 27858
Hortoba´gyi, Tibor, Jason Barrier, David Beard, John
Braspennincx, Peter Koens, Paul Devita, Line Demp-
sey, and Jean Lambert. Greater initial adaptations to
submaximal muscle lengthening than maximal shortening.
J. Appl. Physiol. 81(4): 1677–1682, 1996.—The purpose of
thisstudywasto comparethe short-termstrength andneural
adaptationsto eccentricandconcentric trainingatequal force
levels. Forty-two sedentary women (age 5 21.5 yr) were
ranked based on the initial quadriceps strength score, and
trios of subjects were randomly assigned to either an eccen-
tric (n 5 14), a concentric (n 5 14), or a nonexercising control
group (n 5 14). Training involved a total of 824 eccentric or
concentric quadriceps actions at 1.05 rad·s
21
administered in
four sets of 6–10 repetitions, four times per week for 6 wk.
Before and after training, all subjects were tested for unilat-
eral maximal isometric and eccentric and concentric actions
at 1.05 rad·s
21
and for a 40-repetition eccentric and concen-
tric fatigue series of the left and right quadriceps. Surface
electromyographic activity of the vastus lateralis and media-
lis was monitored during testing. Concentric training in-
creased concentric (36%, P , 0.05), isometric (18%, P , 0.05),
and eccentric strength (13%), and eccentric training in-
creased eccentric (42%, P , 0.05), isometric (30%, P , 0.05),
and concentric (13%) strength. Eccentric training improved
eccentric and isometric strength more (P , 0.05) than did
concentric training. The electromyographic adaptations were
greater with eccentric training. Cross-education was 6%, and
neither training mode modified fatigability. The data suggest
that training of the quadriceps muscle with submaximal
eccentric actions brings about greater strength adaptations
faster than does training with maximal-level concentric ac-
tions in women. This greater adaptation is likely to be
mediated by both mechanical and neural factors.
exercise; muscle; electromyography; fatigue; cross-education
MUSCLE STRENGTH AND SIZE increase due to overload (1).
To maximize the training effect and minimize the time
involvement, researchers (5, 11, 13, 16, 18, 19) have
become interested in taking advantage of the greater
forces (17) associated with muscle lengthening. Yet the
data remain equivocal. While several studies reported
greater gains in muscle strength and size after eccen-
tric (11, 18) compared with concentric training, other
studies found similar changes (5, 16, 19) or actually
greater changes with concentric training (23). One
reason for the inconsistency in the findings could be
that isotonic contractions were used in some studies (6,
13,23),whereasin other studiesisokineticactionswere
used (11, 19). Another and perhaps more important
reason could be that the eccentric and concentric forces
were not equated during the training programs. While
the concentric portion of the movement used for train-
ing in these studies was maximal (16), the eccentric
portion of movement was underloaded as low as ,50%
of maximum (6). Thus one aim of the study was to train
subjects at the sameabsolute force level byusing either
eccentric or concentric contractions. Because neural
inhibition of force production in untrained individuals
causes a greater deviation from the expected eccentric
forces than from the expected concentric forces (14,27),
we hypothesized that a greater neuromuscular adapta-
tion should occurafter eccentric compared withconcen-
tric training, even if the force levels are equated during
training.
Although adaptability of women to resistive exercise
is similar to men’s (25), less attention has been devoted
to the adaptations to exercise with muscle lengthening
in women. Except for one study (19), the initial adap-
tive responses to exercise with muscle lengthening
were studied in men. This isunfortunate,becausesome
researchers suggested that perhaps women, compared
with men, tend to plateau earlier in their responses to
resistive exercise (9). Recent studies also suggest that,
although the rapid initial gains in muscle strength are
associated with neural adaptations (21), intramuscular
changes also occur specifically in female muscles, per-
haps as a precursor for hypertrophy (24). To be able to
directly compare the outcome of the present study with
the results of prior studies that used a 6- to 12-wk
trainingperiod, we also adopted a 6-wk trainingperiod.
Thus the second aim of the present study was to
examine the initial adaptations to muscle lengthening
and shortening in women.
Finally, prior studies have also paidlittleattentionto
the relationship between strength gains with these two
contraction modes and fatigue and failed to use fatigue
to evaluate the nature of neural adaptation to training.
One suggestion was that fatigue is a stimulus for
strength gains (20). Paradoxically, several researchers
observed that very little fatigue occurs during repeated
eccentric compared with concentric actions (8), yet
several studies suggest that eccentric actions are cru-
cial for strength gains and hypertrophy (6). Thus the
thirdaimofthestudywastoexaminetheroleoffatigue
in eliciting strength gains with eccentric andconcentric
actions. The prediction was that fatigue does not need
to occur to induce an increase in muscle strength. In
total, the purpose of the study was to compare the
short-term strength and fatigue adaptations to eccen-
tric and concentric training of the quadriceps muscle at
equal force levels in women.
METHODS
Subjects and design. Forty-two female volunteers were
recruited from the University community. A subject was
0161-7567/96 $5.00 Copyright
r
1996 the American Physiological Society 1677
by guest on June 3, 2013http://jap.physiology.org/Downloaded from
included in the study if she had not participated in resistive
or aerobic exercise training for at least 1 yr before the study
and had no history of knee pathology or injury based on a
physical therapy examination. A written informed consent,
approved bythe university’s Policy and Review Committee on
Human Research, was obtained before testing.
The study was completed in 8 wk and included pre- (week
1) and posttraining testing (week 8) and training of the left
quadriceps muscle four times per week for 6 wk (weeks 2-7).A
6-wk period was used to investigate the early phase of
adaptations. Muscle strength, electromyogram (EMG), and a
40-repetition fatigue series were measured in both quadri-
ceps in all subjects. Left and right quadriceps in each subject
were tested 2–3 days apart, and the limb test order was
counterbalanced across subjects.
During week 1, in two sessions separated by 2–3 days,
subjectswerefamiliarized withthedynamometer by perform-
ing two trials of 50, 75, and 90% of perceived maximal
isometric and concentric and eccentric actions at each speed,
separated by 1 min of rest. The testing followed this familiar-
ization.Afterthe pretraining testing,allsubjectswere ranked
onthe aggregatemaximal isometric, concentric,and eccentric
score. Of the first three subjects, at random, one subject was
assigned to one exercise group, another subject to the other
exercise group, and the third subject to the control group.
This method was used to assign theremaining subjects to one
of three groups, creating strength-matched subject trios in
the three groups.
Subjects in the concentric training group (n5 14)exercised
by using maximal effort concentric actions of the quadriceps
muscle. Each subjectin the eccentric group (n 5 14) exercised
the quadriceps muscle at the same force as did the subject
pair in the concentric group. Practically, the eccentric subject
pairs exercised after the concentric subject pairs finished
their sessions. For the first training session, the eccentric
group’s training intensity was determined based on the
maximal concentric force produced by the concentric subject
pair, measured during the pretraining test.During the subse-
quent training sessions, the average of all repetitions per-
formed by the concentric trainee in one session was computed
and used as a target force by the eccentric subject pair. For
the subjects exercising in the eccentric group, two markers
were set around the target force value creating a 65% band
on the dynamometer’s computer screen. The concentric sub-
ject pairs also had biofeedback: a marker appeared on the
monitor at the maximal force recorded during the previous
session. These subjects were encouraged to exceed the force
level indicated by the marker.
Strength testing and EMG. Unilateral maximal voluntary
isometric and isokinetic eccentric and concentric strength of
the left and right knee extensors was measured on a dyna-
mometer (Kin-Com, 500H, Chattecx, Chattanooga, TN). Sub-
jects sat on the seat of the dynamometer with a knee and hip
joint angle of ,1.57 rads and with arms folded in front of the
chest. The anatomic zero was set at a knee angle of 3.14 rads.
Extraneous movement of the upper body and the involved leg
was limited by two crossover shoulder harnesses, a lap belt, a
thighstrap, andan anklecuff.Thetransverse axisof theknee
joint was aligned with the transverse axis of the dynamom-
eter’s power shaft. The length of the lever arm was individu-
ally determined. Force was measured by a strain gauge
embedded in the ankle cuff. The force values were corrected
by the software for leg mass that was measured in the
horizontalposition. Maximal isometric force was measured at
a knee angle of 2.36 rads. Two maximal-effort 5-s trials were
performed with 1min of rest between trials. Maximalconcen-
tric and eccentric forceof the kneeextensors was measured at
1.05, 2.09, and 3.14 rad·s
21
. Subjects performed two repeti-
tions with a 1-s pause at either end of the range of motion to
avoidthe facilitatingeffectsofthe precedingaction. Theorder
of isometric vs. dynamic actions and eccentric vs. concentric
actions was counterbalanced across subjects, and the order of
speeds was randomized. The higher value of two trials was
used as the criterion measure. Note that strength data are
reported only at 1.06 rad·s
21
.
Surface EMG activity was recorded in the vastus lateralis
and vastus medialis. We recorded from these synergistic
muscles to increase validity of the EMG measures. The skin
surface was cleaned with alcohol. One box electrode with a
built-in preamplifier (Motion Control, Salt Lake City, UT),
powered by 9-V batteries, was placed axially, taped, and
ace-bandaged on each muscle belly. The two electrodes had
similar electronics characteristics: a common mode rejection
ratio of 370 dB, a bandwidth of 8 Hz to 28 kHz, quiescent
current of 0.12 mA, and a direct current input impedance of
1MV.
The force and the goniometer signals from the dynamom-
eter’s analog-to digital board and the two EMG signals were
input to a digital adapter (model 4000A, Vetter, Rebersburg,
PA) that sampled the signals at 80 MHz. The adapter was
connected to a modified videocasette recorder (JVC, HR-
D86OU, model 500C, Vetter, Rebersburg, PA). Data from the
videotape were transferred through a 12-bit analog-to-digital
board (Data Translation, model 2801A, Marlboro, MA). The
Myosoftsoftware package(Noraxon, Scottsdale,AZ) was used
to store and digitize the data.
Before digitization, the direct EMG signals were inspected
and, if movement artifacts (6.5% of alltracings) were present,
anotherrepresentative segmentofthe datawas digitizedthat
was artifact free. Each data file was checked and, if needed,
adjusted for baseline shift. The root mean square (RMS) of
the direct EMG data was obtained by using a 20-ms window.
Across all channels, thefirst marker wasplaced at peak force,
and a second marker was placed 250 ms before the first
marker. Within this 250-ms window, the highest RMS value
was taken as peak EMG (µV) and the average over the
250-ms window as anaverage EMG(µV·s).Peak and average
EMG data were digitized at 2.36-rad knee angle for the
eccentric, concentric, and isometric trials.
Fatigue testing. Seven of fourteen subjects in each group
performed 40 repetitions of quadriceps concentric actions
with the trained and untrained leg, and the remaining seven
subjects did 40 repetitions of eccentric actions with the
trained and untrained leg at 1.05 rad·s
21
. Only the quadri-
ceps muscle was exercised, and the operator returned the
lever arm to the starting position for the next repetition. The
order of eccentric and concentric fatigue bouts was balanced
between subjects.
Training. Subjects trained the left quadriceps four times
per week for 6 wk, except during week 1 when, for a gradual
introduction, there were only three sessions. Each training
session consisted of four sets of 6–10 repetitions of either
concentric or eccentric actions at 1.05 rad·s
21
on the same
isokinetic dynamometer on which the testing was done
(Kin-Com, 500H, Chattecx). Thenumber of repetitions fluctu-
ated: week1,6;week 2,8;week 3,10; week 4,6;week 5,8;week
6, 10 (7). The total number of repetitions was 824. Visual
feedback was provided toboth groups of subjects toencourage
maximal effort in the concentric group and to exercise at the
preset target force for the eccentric group (as described in
Subjects and design).
Statistical analyses. The BMDP PC-90 statistical package
was usedto perform allanalyses.Atest of skeweness(26) was
usedto checkthe force andEMG datafor normal distribution.
1678 ADAPTATIONS TO MUSCLE SHORTENING AND LENGTHENING
by guest on June 3, 2013http://jap.physiology.org/Downloaded from
The data were assumed to be normally distributed if the ratio
of skewness value to its standard error (6/N)
1/2
, where N is
numberof observations, was within 62.58.Reliability offorce
and EMG data was estimated by computing the intraclass
correlation coefficient from the control group’s data (n 5 14).
The force data were analyzed with a group (concentric,
eccentric, control) by speed (21.05, 0, 1.05 rad·s
21
) by time
(pre- and posttraining) analysis of variance with repeated
measures on the last two factors. A similar design was used
for the EMG data. The EMG data were analyzed by taking
thearcsine of theeccentricpeak EMG-to-isometricpeakEMG
and concentric peak EMG-to-isometric peak EMG ratios for
each subject. However, Table 3 shows not the arcsine values
but the actual ratios. The EMG data were analyzed as a ratio
to reduce the error caused by electrode placement before and
after training and by changes in skin properties (28). The
fatigue data were analyzed with a group (concentric, eccen-
tric, control) by contraction mode (concentric, eccentric) by
time (pre- and posttraining) analysis of variance, with the
group and contraction mode being between factors and time
being within factor. This analysis was done on the percent
change in fatigue [average of repetitions 1–3 (initial score) 2
average of repetitions 38–40 (final score) 4 initial score 3
100]. In case of a significant F-ratio, Tukey’s post hoc contrast
was performed to determine the means that were different at
the significance level of P , 0.05.
RESULTS
Skewness analysis revealed that the skewness/SE of
skewness scores ranged from 21.66 (vastus lateralis
peak EMG) to 1.65 (isometric force). Thus the distribu-
tion of the force and EMG variables was assumed to be
normal.Reliability ofthestrengthmeasureswasaccept-
able, and the intraclass correlation coefficients ranged
from r 5 0.82 (peak EMG of the vastus lateralis muscle
during concentric action at 3.14 rad·s
21
)tor50.96
(eccentric force at 1.05 rad·s
21
). There were no signifi-
cant trials or time (pre- and posttest) effects for any of
the strength or EMG variables. The coefficient of
variation ranged from 3.7 to 13.4% for strength and
from 8.7 to 27.5% for the EMG variables.
Table 1 shows that subjects in the three groups were
similar in age, mass, height, and body fat. Percent body
fat was determined based on triceps, suprailiac, and
thigh skinfolds (15).
Figure 1 shows the weekly average forces during
training. The group by time interaction was not signifi-
cant (F 5 0.6, P 5 0.68), suggesting thatthe two groups
improved at the same rate and exercised at the same
force levels. There was a significant time main effect
(F 5 15.8, P 5 0.0001), and the two groups combined
improved 25% from 465to 582 N. The largestdifference
between the two groups in training intensity was 13 N
at week 2.Atweeks 1, 2, 3, 4, 5, and 6, the eccentric
group exercised at 89, 97, 99, 104, 109, and 111%,
respectively, of their maximum pretest eccentric force.
At weeks 1, 2, 3, 4, 5, and 6, the eccentric group
exercised at 111, 120, 123, 127, 135, and 137%, respec-
tively, of their maximum pretest concentric force. At
weeks 1, 2, 3, 4, 5, and 6, the concentric group exercised
at 109, 118, 122, 128, 134, and 138%, respectively, of
their maximum pretest concentric force.
Table 2 shows the changes in muscle strength. There
was a significant (F 5 22.1, P 5 0.000) group by speed
by time three-way interaction. Concentric training
significantly (P , 0.05) improved concentric strength
by 152 N or36% and isometric strength by87 N or 18%.
Concentric training improved eccentric strength by 68
N or 13% (P . 0.05).
Table 1. Subject characteristics
Variable
Concentric
Group
Eccentric
Group
Control
Group
Age, yr 21.26 2.26 21.16 2.38 21.76 3.41
Mass, kg 59.46 8.06 60.36 2.93 58.66 6.47
Height, cm 160.56 6.65 163.86 4.00 161.964.75
Fat, % 23.86 5.19 24.96 6.29 22.86 3.24
Values are means 6 SD for 14 subjects/group.
Fig. 1. Force averages of all repetitions performed during each week
of training to demonstrate similar training intensities in 2 groups.
*Significantly differentcompared with week 1.
Table 2. Changes in muscle strength
Velocity,
rad·s
21
Concentric Group Eccentric Group Control Group
Pre Post
D %D
Pre Post
D %D
Pre Post
D %DMean6SD Mean6SD Mean6SD Mean6SD Mean6SD Mean6SD
21.05 5256 97 5936 83 68 13 5276 104 7496 106 222*† 42 5156 115 5256 100 10 2
0 4956 100 5826 122 87* 18 4716 72 6116 135 140*‡ 30 4886 97 4766 102 212 22
1.05 4236 84 5756 135 152* 36 4266 82 4816 94 13 13 4176 104 4226 89 5 1
Values are in N. Pre and Post, before and after training, respectively. *Significant (P, 0.05) change (D); †significantly more change than
concentric group at 1.05 rad·s
21
; ‡significantly more change than concentric group at 0 rad·s
21
.
1679ADAPTATIONS TO MUSCLE SHORTENING AND LENGTHENING
by guest on June 3, 2013http://jap.physiology.org/Downloaded from
Submaximal-efforteccentrictraining improvedmaxi-
mal eccentric strength by 222 N or 42%. Eccentric
training improved isometric strength (140 N) signifi-
cantly (P , 0.05) more than did concentric training (87
N). Eccentric training improved concentric strength by
94 N or 14% (P . 0.05). Eccentric training increased
eccentric strength (222 N) significantly (P , 0.05) more
than concentric training increased concentric strength
(152 N). The control group did not show significant
changes (P . 0.05).
Because average and peak EMG values correlated
(r 5 0.92; n 5 42), Table 3 shows the changes in the
eccentric-to-isometric and concentric-to-isometric peak
EMG ratios only. For the vastus lateralis, there was a
significant group by speed by time interaction (F 5 8.9,
P5 0.000).Concentric training increased (P, 0.05)the
concentric-to-isometric EMG ratio in the concentric
test, and eccentric training significantly increased (P ,
0.05) EMG eccentric-to-isometric ratio in the eccentric
test. The 92% change was significantly (P , 0.05)
greater in the eccentric test after eccentric training
than the 36% change in the concentric test after
concentric training. No significant changes occurred in
the control group’s vastus lateralis and vastus medialis
activity. In the vastus medialis, the post hoc analysis of
the EMG ratios for the significant group by speed by
time interaction (F 5 13.7, P 5 0.000) revealed a
similar pattern of changes to those observed in the
vastus lateralis.
Figure 2A shows the percent changes in fatigue. The
group by contraction mode by time interaction was not
significant, but there was a significant contraction
(concentric and eccentric fatigue) main effect (F 5
123.3, P 5 0.000, pooled across groups and time):
fatigue was significantly greater during the concentric
(48.2 6 13.6%) than during the eccentric series (5.8 6
18.8%).
Figure 2B shows the fatigue data for the contralat-
eral leg. Except for the significant contraction mode
main effect (F 5 7.6, P 5 0.04), indicating that fatigue
was greater with the concentric (49.2 6 24.2%) than
with the eccentric (7.7 6 12.2%) series (pooled across
groups and time),there were noother significant three-
or two-way interactions or main effects. There were no
significant main or interaction effects for the changes
in strength (6% for all groups and conditions pooled)
and EMG of the contralateral quadriceps.
DISCUSSION
The key findings of the present study were that 1)
submaximal training with eccentric actions improved
maximal eccentric and isometric strength significantly
morethanmaximal-effortconcentrictrainingimproved
Table 3. Changes in peak EMG activity ratios in VL and VM muscles
Velocity,
rad·s
21
Concentric Group Eccentric Group Control Group
Pre Post
D %D
Pre Post
D %D
Pre Post
D %DMean6SD Mean6 SD Mean6SD Mean6 SD Mean6SD Mean6 SD
VL
21.05 1.26 0.15 1.36 0.21 0.1 8 1.36 0.11 2.56 0.33 1.2*† 92 1.26 0.17 1.16 0.26 20.1 28
1.05 1.160.09 1.56 0.21 0.4* 36 1.26 0.10 1.36 0.17 0.1 8 1.16 0.06 1.16 0.12 0 0
VM
21.05 1.36 0.22 1.56 0.34 0.2 15 1.56 0.20 2.76 0.31 1.2*† 80 1.36 0.19 1.46 0.23 20.1 28
1.05 1.260.18 1.76 0.42 0.5* 42 1.26 0.16 1.46 0.20 0.2 17 1.26 0.22 1.36 0.17 0.1 8
Values are eccentric-to-isometric and concentric-to-isometric ratios. VL, vastus lateralis; VM, vastus medialis. *Significant (P, 0.05)
change; †significantly more change than concentric group at 1.05 rad·s
21
.
Fig. 2. Concentric and eccentric fatigue expressed as a percent
(initial 2 final score 4 initial score) in trained (A) and untrained (B)
leg at pre- and posttest in 3 groups. *Significantly greater fatigue
compared with eccentric fatigue bout.
1680 ADAPTATIONS TO MUSCLE SHORTENING AND LENGTHENING
by guest on June 3, 2013http://jap.physiology.org/Downloaded from
maximal concentric and isometric strength; 2) changes
in EMG activity of the vastus lateralis and medialis
paralleled the strength adaptations; and 3) fatigability
was not affected by either training method.
We pursued the hypothesis that muscle lengthening
compared with shortening is superior to cause neuro-
muscular adaptation. Evidence in humans to support
this hypothesis is equivocal. At one extreme is the
report that only ,50% of maximal eccentric force
during a stretch-shortening activity may be sufficient
to cause greater strength (6) and muscle adaptations
(10). At the other extreme is the finding that exercise
training with 80% of maximal eccentric actions results
in less improvement in strength compared with train-
ing with maximal concentric actions (23). In between
these extremes are other studies that report similar
improvements in strength after eccentric and concen-
tric training (16). Training with maximal eccentric
actions brings about the greatest neural adaptations in
the quadriceps (11) and in the forearm flexors (18).
Onereasonfortheinconsistency in the findings could
bethateccentric and concentricforceswerenot equated
duringthe trainingprograms.Thus onecannotdifferen-
tiate the effects due to differences in forces and the
effects caused by the differences in contraction modes.
We addressed this problem by equating the force levels
during training. The inconsistency in the findings can
also be due to the differences between studies in which
isokinetic (11) or isotonic (6) contraction modes were
used, but we did not address this problem in the
present work.
Even when forces were equated in the two training
modalities, eccentric training improved eccentric force
70 N more than concentric training improved concen-
tric force, and eccentric training improved isometric
force 53 N more than did concentric training (all P ,
0.05). During concentric training, the passive elements
are less involved in force production (4). Eccentric
training may increase the stiffness of the passive
elements and could account for the greater increases in
eccentric and isometric forces. This mechanism could
also account in part for the dampened increases in
eccentric force after concentric training and in concen-
tric force after eccentric training.
To isolateintrinsicmuscularadaptations fromsimple
effects of practice, we administered an isometric test
contraction in addition to eccentric and concentric test
contractions. Isometric contraction wasusedby neither
training group, and an increase in isometric force can
be taken as adaptation without the confounding effects
of learning (21). Although both types of training have
brought about strength increases due to some neural
adaptations, submaximal, like maximal (11, 18), eccen-
tric training is associated with a greater intrinsic
muscular adaptation.
There also was a significantly (P , 0.05) greater
neural adaptation associated with submaximal eccen-
tric than with maximal concentric training, as sug-
gested by the changes in surface EMG activity (Table
3). Neural inhibition of force production in untrained
individuals appears to cause a greater deviation from
the expected eccentric forces than from the expected
concentric forces (13, 27). One can thus predict a
greater neural adaptation after eccentric than after
concentric training. The results (Table 3) did confirm
this prediction. Most (21) but not all (7) researchers
hold the viewthat initial strengthgains are largelydue
to nonhypertrophic factors such as increased motor
unit activation, reflected by an increased EMG activity
after training. Perhaps training has also reduced coac-
tivation in the antagonist muscles (7), but we failed to
observe such changes after maximal eccentric and
concentric training for twice the durationofthepresent
study (11).
We also used fatigue to evaluate the nature of neural
adaptation in the trained leg. It is known that motor
unit activation increases with fatigue (3). Because
eccentric actions require fewer active motor units (2)
and a greater involvement of the passive elements (18),
less fatigue is expected to occur with repeated eccentric
compared with concentric actions, as indeed was the
case during training and the fatigue tests. Thus sub-
maximal eccentric training is associated with less
fatigue and greater strength adaptations compared
withconcentrictraining,whichcausesmore fatigue but
less of a strength adaptation. This would suggest that
the neural mechanism may be different between the
two training modes as far as fatigue being a contribut-
ing factor to strength gains (20).
Whetherthis neuraladaptationis peripheral(noncor-
tical) or central (cortical) is unclear. We addressed this
issue by administering an eccentric and concentric
fatigue bout in the nontrained leg before and after
training. The prediction was that if there is central
adaptation, then fatigue is less after training in the
unexercisedmusclesbecausethe nervous systemwould
be able to compensate more effectively for the fatigue
induced by the contraction series. The data suggest
that the magnitude of fatigue was the same before and
after training with both contraction modes (Fig. 2),
suggesting that the nature of neural adaptation in the
trained leg is most likely to be peripheral. Whether
such a peripheral adaptation is linked to the greater
muscle lengthening-related afferent traffic is to be
seen.
After824submaximal eccentricandmaximalconcen-
tric contractions administered over 23 sessions for 6
wk,weobservedonly,6% ofcross-educationinstrength
to the unexercised limb. This is somewhat smaller
cross-education than observed by others for cross-
education with maximal isometric actions (22). It is
also in contrast to our previous observations that
maximal eccentric training resulted in significantly
greater cross-education of strength than did concentric
training (12). However, in that study, we used 1,890
maximal contractions administered over 12 wk. Thus
training intensity (submaximal vs. maximal) as well as
duration (6 vs. 12 wk) may both play a role in the
magnitude of cross-education associated with eccentric
training.
Subjects for this study were women. In agreement
with prior data on women’s adaptations to resistive
1681
ADAPTATIONS TO MUSCLE SHORTENING AND LENGTHENING
by guest on June 3, 2013http://jap.physiology.org/Downloaded from
exercise in general (25), the present study also shows
thatwomen areasresponsive totrainingwith lengthen-
ing as are men (11). Furthermore, the adaptations in
thesewomen’squadricepsmusclewas fasterwitheccen-
tric than with concentric training. In studies that used
up to 12 (11) or 16 wk of training (6), about one-half or
more of the final adaptation occurred at 6–8 wk.
Perhaps, during the second half of the training period
in these studies, the adaptations were less due to
overtraining.
It is unclear whether continued training with sub-
maximaleccentriccontractionsbeyond the 6wkusedin
this study would result in similar rates of gains as
trainingwithmaximal loads. This is important because
some researchers contended that strength gains in
women may plateau at 3 or 4 mo (9). Nonetheless, the
rate of early strength and muscle adaptation seems to
be similar between men and women (24), as also
confirmed by the present study compared with our
previous work in men (11). The submaximal training
effects of muscle lengthening are also important be-
causemaximaleccentricactions, however effectivethey
are, may not be the choice of training in a fitness or a
rehabilitation setting. It is also worth noting the rapid
trainability of the subjects in the present and prior
studies (16). The rapid initial adaptation is most likely
related to the untrained status of these healthy and
active subjects. It should also be noted that the conclu-
sions of this study are confined to the quadriceps
muscle and the results may be different in muscles of
different architecture or fiber composition.
In summary, the results of the present study suggest
that training at ,80% of maximal eccentric contrac-
tions of the quadriceps brings about greater strength
and neural adaptations than does training with maxi-
mal concentric contractions in women. This greater
adaptation is likely to be mediated by both mechanical
and neural factors.
This work was supported in part by an National Institute of Child
Health and Human Development Grant 30422 and by a Research/
Creative Activity grant from East Carolina University’s Faculty
Senate (to T. Hortoba´gyi). J. Braspennincx and P. Koens were on an
internship from the Free University of Amsterdam, Faculty of
Human Movement Sciences, The Netherlands.
Addressforreprintrequests:T.Hortoba´gyi,BiomechanicsLabora-
tory, East Carolina University, Greenville, NC 27858 (E-mail:
hphortob@ecuvm.cis.ecu.edu).
Received 18 October 1995; accepted in final form 6 May 1996.
REFERENCES
1. Atha, J. Strengthening muscle. Exercise Sport Sci. Rev. 9: 1–73,
1981.
2. Bigland, B., and O. C. J. Lippold. Relation between force,
velocity and integrated electrical activity in human muscles. J.
Physiol. Lond. 123: 214–224, 1954.
3. Bigland-Ritchie, B. EMG/force relations and fatigue of human
voluntary contractions. Exercise Sport Sci. Rev. 9: 75–117, 1981.
4. Cavagna, G. A. Storage and utilization of elastic energy in
skeletal muscle. Exercise Sport Sci. Rev.5: 89–129, 1977.
5. Colliander, E. B., and P. A. Tesch. Effects of eccentric and
concentric muscle actions in resistance training. Acta Physiol.
Scand. 140: 31–39, 1990.
6. Dudley, G. A., P. A. Tesch, B. J. Miller, and P. Buchanan.
Importance of eccentric actions in performance adaptations to
resistance training. Aviat. Space Environ. Med. 62: 543–550,
1991.
7. Garfinkel, S., and E. Cafarelli. Relative changes in maximal
force, EMG, and muscle cross-sectional area after isometric
training. Med. Sci. Sports Exercise 24: 1220–1227,1992.
8. Gray, J. C., and J. M. Chandler. Percent decline in peak torque
production during repeated concentric and eccentric contractions
of the quadriceps femoris muscle. J. Orthop. Sports Phys. Ther.
11: 309–314, 1989.
9. Ha¨kkinen, K. Changes in physical fitness profile in female
volleyball players during the competitive season. J. Sports Med.
Phys. Fitness 33: 223–232, 1993.
10. Hather, B. M., P. A. Tesch, P. Buchanan, and G. A. Dudley.
Influence of eccentric actions on skeletal muscle adaptations to
resistance training. Acta Physiol. Scand. 143: 177–185,1991.
11. Hortoba´gyi, T., J. P. Hill, J.A. Houmard, D. D. Fraser, N. J.
Lambert, and R. G. Israel. Adaptive responses to muscle
lengthening and shortening in humans. J. Appl. Physiol. 80:
765–772, 1996.
12. Hortoba´gyi, T., J. P. Hill, N. Lambert, V. Ash, P. Brown,
K. Wells, and R. Israel. Cross-transfer effects with eccentric
training. Soc. Neurosci. Abstr. 19: 156, 1993.
13. Hortoba´gyi, T., and F. I. Katch. Role of concentric force in
limiting improvement in muscular strength. J. Appl. Physiol. 68:
650–658, 1990.
14. Hortoba´gyi, T., and F. I. Katch. Eccentric and concentric
torque-velocity relationships during arm flexion and extension:
influence of strength level. Eur. J. Appl. Physiol. Occup. Physiol.
60: 395–401, 1990.
15. Jackson, A. S., and M. L. Pollock. Generalized equations for
predicting body density of women. Med. Sci. Sports Exercise 12:
175–182, 1980.
16. Johnson, B. L., J. W. Adamczyk, K. O. Tennøe, and S. B.
Strømme. A comparison of concentric and eccentric muscle
training. Med. Sci. Sports Exercise 8: 35–38,1976.
17. Katz, B. The relation between force and speed in muscular
contraction. J. Physiol. Lond. 96: 45–64, 1939.
18. Komi, P. V., and E. R. Buskirk. Effect of eccentric and
concentric muscle conditioning on tension and electrical activity
of human muscle. Ergonomics 15: 417–434, 1972.
19. Pavone, E., and M. Moffat. Isometric torque of the quadriceps
femoris after concentric, eccentric, and isometric training. Arch.
Phys. Med. Rehab. 66: 168–170,1985.
20. Rooney, K. J., R. D. Herbert, and R. Balnave. Fatigue
contributes to the strength training stimulus. Med. Sci. Sports
Exercise 26: 1160–1164, 1994.
21. Sale, D. G. Neural adaptation to resistance training. Med. Sci.
Sports Exercise 20: S135–S145, 1988.
22. Shaver, L. G. Cross transfer effects of conditioning and decondi-
tioning on muscular strength. Ergonomics 18: 9–16,1975.
23. Smith, R. C., and O. M. Rutherford. Acomparison of eccentric
and concentric contractions in strength training in humans
(Abstract). J. Physiol. Lond. 475: 26P, 1994.
24. Staron, R. S., D. L. Karapondo, W. J. Kraemer, A. C. Fry,
S. E. Gordon, J. E. Falkel, F. C. Hagerman, and R. S.
Hikida. Skeletal muscle adaptations during early phase of
heavy-resistance training in men and women. J. Appl. Physiol.
76: 1247–1255, 1994.
25. Staron, R. S., E. S. Malicky, M. J. Leonardi, J. E. Falkel,
F. C. Hagerman, and G. A. Dudley. Muscle hypertrophy and
fast fiber type conversions in heavy resistance-trained women.
Eur. J. Appl. Physiol. Occup. Physiol. 60: 71–79, 1989.
26. Tabachnik, G., and L. S. Fidell. Using Multivariate Statistics.
NewYork: Harper & Row, 1983.
27. Westing, A. H., J. Y. Seger, and A. Thorstensson. Effects of
electrical stimulation on eccentric and concentric torque-velocity
relationshipsduringkneeextension inman.ActaPhysiol. Scand.
140: 17–22, 1990.
28. Winter, D. A., G. Rau, R. Kadefors, H. Broman, and C. J.
deLuca. Units, Terms, and Standards in the Reporting of EMG
Research. The Ad Hoc Committee of the Int. Soc. Electrophysiol.
Kinesiology, 1980, p. 1–9.
1682 ADAPTATIONS TO MUSCLE SHORTENING AND LENGTHENING
by guest on June 3, 2013http://jap.physiology.org/Downloaded from
