JOURNALOF NEUROPHYSIOLOGY

Vol. 67. No. 5. May 1992. l’rirltcv’

Strength Increases From the Motor Program: Comparison of Training

With Maximal Voluntary and Imagined Muscle Contractions

GUANG YUE AND KELLY J. COLE

Department of. Exercise Science, The University of Iowa, Iowa City, Iowa 52242

SUMMARY AND CONCLUSIONS 1984; Sale 1986), strength gains achieved during the first
I. This study addressed potential neural mechanisms of the weeks of training reflect an increased ability to activate mo-
strength increase that occur before muscle hypertrophy. In particu- toneurons and therefore appear to be neural in origin.
lar we examined whether such strength increases may result from Abundant evidence demonstrates neural changes that oc-
training-induced changes in voluntary motor programs. We com- cur soon after training begins. Voluntary strength increases
pared the maximal voluntary force production after a training rapidly before the muscles exhibit hypertrophy (Fukunaga
program of repetitive maximal isometric muscle contractions with 1976; Ikai and Fukunaga 1970; Jones and Rutherford
force output after a training program that did not involve repeti- 1987; Liberson and Asa 1959; Moritani and de Vries 1979;
tive activation of muscle; that is, after mental training. Rose et al. 1957; Tesch et al. 1983) and before increases in
2. Subjects trained their left hypothenar muscles for 4 wk, five electrically evoked tension occur (Davies and Young 1983;
sessions per week. One group produced repeated maximal isomet-
ric contractions of the abductor muscles of the fifth digit’s meta- McDonagh et al. 1983 ) . These early voluntary strength in-
carpophalangeal joint. A second group imagined producing these creases are accompanied by increased integrated electro-
same, effortful isometric contractions. A third group did not train myograms (EMG) (Komi 1986; Sale 1986) and increased
their fifth digit. Maximal abduction force, flexion/extension force reflex gains (Milner-Brown et al. 1975; Sale et al. 1982,
and electrically evoked twitch force (abduction) of the fifth digit 1983a,b; Upton and Radford 1975 ). The greatest strength
were measured along with maximal integrated electromyograms gains occur at the trained joint angles (Gardner 1963;
(EMG) of the hypothenar muscles from both hands before and Lindh 1979; Meyers 1967 ). Finally, training of one limb is
after training. associated with increased voluntary strength in the contra-
3. Average abduction force of the left fifth digit increased 22% lateral (untrained) muscles (e.g., Hellebrandt et al. 1947;
for the Imagining group and 30% for the Contraction group. The Houston et al. 1983; Rose et al. 1957; see Enoka 1988; Sale
mean increase for the Control group was 3.7%.
4. The maximal abduction force of the right (untrained) fifth 1986 for a review), even though the contralateral muscles
digit increased significantly in both the Imagining and Contrac- remain virtually quiescent during training (Houston et al.
tion groups after training ( 10 and 14%,respectively), but not in 1983; Panin et al. 196 1; Yasuda and Miyamura 1983).
the Control group (2.3%). Theseresultsare consistentwith pre- The neural mechanisms of these strength gains are poorly
vious studiesof training effectson contralaterallimbs. understood. However, the previously noted phenomenon
5. The abductiontwitch force evokedby supramaximalelectri- of increased strength from muscles contralateral to those
cal stimulationsof the ulnar nerve was unchangedin all three that were trained raises the intriguing possibility that early
groupsafter training, consistentwith an absenceof musclehyper- strength gains may be induced without repetitive muscle
trophy. The maximal force of the left great toe extensorsfor indi- activation; that is without repetitive activation of motoneu-
vidual subjectsremainedunchangedafter training, which argues Tons, spinal interneurons, or possibly, descending motor
againststrengthincreases due to generalincreasesin effort level.
6. Increasesin abduction and flexion forces of the fifth digit pathways. Instead, early strength gains may depend on
were poorly correlated in subjectsof both training groups. The changes in the central programming of a maximal volun-
fifth finger abduction force and the hypothenar integratedEMG tary contraction. If so, it may be possible to induce changes
increaseswere not well correlated in these subjectseither. To- in the motor program for a maximal voluntary contraction
gethertheseresultsindicate that training-inducedchangesof syn- via mental practice (that is, imagining performance of a
ergistand antagonistmuscleactivation patternsmay havecontrib- skilled movement without overt or covert muscle activa-
uted to force increasesin someof the subjects. tion).
7. Strength increases can be achievedwithout repeatedmuscle Research on skill acquisition has demonstrated clearly
activation. Theseforce gainsappearto resultfrom practiceeffects that mental practice leads to improved performance (e.g.,
on central motor programming/planning.The resultsof theseex- Rawlings et al. 1972; Vandell et al. 1943; also see Corbin
perimentsadd to existingevidencefor the neuralorigin of strength
increasesthat occur before musclehypertrophy. 1972; Fets and Landers 1983; Hall 1985; Richardson 1967
for a summary). Individuals asked to imagine themselves
performing skilled, serial movements of the digits mani-
fested increased cerebral blood flow in nonprimary motor
INTRODUCTION
regions of the cerebral cortex without evidence of activating
Skeletal muscle strength gains from isometric strength the primary motor cortex (Roland et al. 1980). It is possi-
training are believed to result from two principal factors. ble therefore that repeated imagined muscle contractions
Whereas muscle hypertrophy occurs in the later stages of may alter the program for maximal torque production at a
training (Enoka 1988; Komi 1986; McDonagh and Davies joint. These central changes may yield increased motoneu-

1114 0022-3077/92 $2.00 Copyright 0 1992 The American Physiological Society

 STRENGTH CHANGES AFTER IMAGINED CONTRACTION TRAINING 1115

ron activation and/or change the relative activation levels Equipment

of synergist and antagonist muscles across a joint to yield Horizontal (abduction) force of the fifth digit was measured
increased torque in the desired direction. The latter phe- with a cantilever-beam transducer instrumented with strain
nomenon, changes in muscle “coordination,” may occur gauges(Fig. 1). A secondforce transducerwasmountedorthogo-
particularly for strength training involving multijoint move- nally on the first to measurethe vertical ( flexion-extension) force.
ments or movements at a joint with multidirectional free- The transducerswereconstructedof two stainlesssteelbars2.5 x
dom (Rutherford and Jones 1986). The contribution of 7.0 X 0.1 cm. The crosstalk of the vertical force transducerto the
this improved coordination to early strength gains remains horizontal transducer was 0.45%, indicating a near orthogonal
unclear. relation betweenthe steelbars.The endof the beamthat measured
This investigation addressed whether imagined maximal the vertical force wassecurelyattachedto a rigid microscopestand
muscle contraction training increases maximal voluntary to allow adjustmentsof the transducersystem’sposition. A metal
tube ( 12mm long and 15mm diam) wassecuredto the free endof
contraction (MVC) force and compared any strength in- the transducerthat measuredthe abduction force. The tube could
creases with those found in the early periods of training by be moved from one sideof the bar to another so that the same
the use of MVCs. Our experimental design included at- transducerswere used for both hands(Fig. 1). A similar trans-
tempts to control or measure effort level, strength increases ducer systemwasusedto measurethe extensionforce of the left
not specific to the trained muscle, and muscle hypertrophy. great toe.
After 20 sessions, imagined maximal contraction and MVC
training produced comparable levels of voluntary strength Procedures
increase.
The training programs for the Imagining and Contraction
groupslasted4 wk with five training sessions per week. The sub-
METHODS jects were trained Monday through Friday of each week in the
Motor Control Laboratory at The University of Iowa.
subjects IMAGINEDCONTRACTION TRAINING. Duringeachtrainingses-
sion, subjectsin the Imagining group were instructed to perform
The subjectswere30 healthy individuals(2 l-29 yr of age)who 15 imaginedmaximal contractions of the left abductor digiti min-
claimednot to have participated in regular musculartraining in imi with a 20-srestafter every secondtrial. Subjectsweretold that
the two yearsbeforethis study. Ten subjectseachwererandomly the training involved imagining musclecontractions and that all
assignedto one of three groups.Subjectsin the Imagining group the upper limb muscles,especiallythe trained muscle,shouldbe
were trained by an imagined maximal muscle contraction relaxedasmuch aspossible.In short, they wereinstructedto max-
method; subjectsin the Contraction group produced MVCs dur- imally activate the brain but not to activate the muscle.Hypoth-
ing their training. The Control group was instructed to refrain enarEMG (seeEMGMEASUREMENTS) wasmonitored during most
from strength training and sportsactivities using the hand. In- of thesetraining sessions. Subjectswere seatedcomfortably in a
formed consentwasobtainedfrom eachsubjectbeforethe experi- chair with their left arm restingon a table.The hand waskept open
ment. Three subjects( 1in the Control group and2 in the Contrac- and relaxedwith the palm facingdownward. On a verbal signalto
tion group) failed to return for posttrainingtesting. begin, the subjectwas instructed to concentrate on the left fifth
finger and imaginethe finger pushingmaximally againstthe hori-
zontal force transducerthat wasusedduring the pretraining test.
General aperimentul procedures The imaginary maximal finger abduction wasto be maintained
The experiment consistedof a pretraining measurementses-
sion, a 4-wk (20-session)training period focusedon increasing
abduction force of the metacarpophalangeal joint of the left fifth
digit, and a posttraining measurementsession.Abduction of the
left fifth digit wasselectedbecausethe musclesof abduction are
usedprincipally in taskssuchasopeningthe grip and thus are not
typically engagedin sustained,high force output in mostactivities
of daily living. Training effects(neural changesand musclefiber
hypertrophy) may be achieved more easily. The following data
were collected from each subject’sipsilateral and contralateral
handsduring the pre- and posttraining measurementsessions: I)
maximal isometric abduction force at the metacarpophalangeal
joint of the fifth digit; 2) flexion/extension force at the metacarpo-
phalangealjoint of the fifth digit during maximal abduction force
production (measuredto indicate possiblechangesin musclecoor-
dination): 3) twitch force (abduction) of the fifth digit generated
by supramaximalelectricalstimulation of the ulnar nerve (taken
asa possibleindication of musclehypertrophy; however, cf. DIS-
CUSSION): 4) surfaceEMG during the maximal abduction force
task from electrodesplacedon the hypothenar eminenceapproxi-
mately over the abductor digiti minimi (although other hypoth-
enar muscles,or the interosseimay have contributed to this EMG FIG. 1. Finger force measurement equipment and subject positioning.
during a maximal force exertion becauseof their proximity to the A: transducer for abduction force. B: transducer for extension/flexion
recordingelectrodes).In addition, the maximal extensionforce of force. C, D, and F: finger, hand, wrist, and arm restraints. E: surface EMG
the left greattoe servedasa control for nonspecifictraining effects electrodes. G: reference electrode. Stimulation electrodes are located at the
suchasstrengthgainsin untrained muscles. medial side of the elbow and are not visible in this drawing.
1116 G. YUE AND K. J. COLE

for 15 s in each trial before imagining a cessation of this pushing. Theseelectrodeswere treated with an electrolyte paste,placedon
During this 15-s period, the subject was instructed to keep imagin- the skin overlying the ulnar nerve located between the medial
ing a voice shouting “harder, harder. . . .” epicondyleand the olecranonof the ulna, and held in placewith
MVC TRAINING. The subjectsin the Contraction group sat in a an elasticstrap.The stimuli consistedof rectangularvoltagepulses
chair with their left armsrestingon a table. The hand wasrelaxed, 0.2 ms in duration delivered from a stimulator (GrassmodelS88
with palm facing downward and the distal part of the fifth digit with a Grassmodel SIUS stimulus isolation unit). The stimulus
positionedagainsta stop that wasrigidly fixed to the table surface. intensity wasset30 V greaterthan that for a maximal M response.
The subjectabductedhis/her left fifth digit asforcefully aspossi- There were 10 twitch trials (providing twitch force and M-wave
ble. During each training session,subjectsin the Contraction data) in eachtest with 10 s rest betweeneachpair of trials.
group were instructed to perform 15 MVCs of the left abductor TOE FORCE. Isometric force measureswere obtained from the
digiti minimi with 20 s of rest separatingeachcontraction. Each left great toe of seatedsubjectsby the useof procedurescompara-
trial lasted- 10s. ble with thosedescribedfor the fingerforce measures. Eachsubject
performed five to six trials of maximal toe extension force and
CONTROL GROUP. Subjects in the Control group were not restedfor at least30 s betweenevery two trials.
trained, but participated in the measurementsbefore and after
training. The subjectswere instructed strictly to avoid any physi-
cal exerciseor mental training of the hypothenar musclesduring Data recording and analysis
the time period betweenthe pre- and posttests. The force transducer signalswere amplified and low-passfil-
PRE- AND POSTTRAINING FORCE MEASURES. The subjects tered at 500 Hz (Biocommunication Electronics model 205).
restedtheir armson the table with the palm of the hand facing EMG signalswere differentially preamplified ( 10,000MQ input
downwardand slid the fifth digit into the metal tube on the force impedance)with a gain of 100and a bandpassof 25-10,000 Hz
transducer(Fig. 1). The distal edgeof the tube (the edgeaway ( BiocommunicationElectronicsmodel301) ; subsequentamplifi-
from the subject)wasalignedwith the baseof the fingernailduring cation occurred with a low-passcutoff of 2,500 Hz. All data were
both pre- and posttests.The index, middle, and ring fingerswere recordedon an eight-channel(Vetter model D) FM tape recorder
stabilizedon the tablewith a strap.An aluminum bar mounted on (DC-l, 125 Hz) and stored for later analysis.Signalswere then
the tablewasplacedbetweenthe fourth and fifth digitsto maintain digitized with an analog-to-digital converter with 12-bit resolu-
an angleof - 5’ betweenthe digits; this ensuredroughly similar tion. The force and EMG signalsweredigitized at 1,000samples/
musclelengthsduring both pre- and posttests.Strapswere usedto s, and the M-wave and twitch responseswere digitized at 3,000
prevent arm motion or vertical motion of the wrist (Fig. 1). samples/s.
Eachsubjectwarmedup with severalsubmaximalcontractions, For eachtrial of digitized data, the peak abduction forceand the
then executed five or six maximal contractions of the abductor correspondingvertical force were measured( Fig. 2). The highest
digiti minimi lasting -4 s with a restingperiod of at least 30 s abduction force obtained from among the recorded trials was
betweentrials. Each subjectwasinstructed to exert a lateral force taken as the maximal abduction force of the fifth digit. The toe
with the fifth digit againstthe force transducer.The transducers forceswere measuredsimilarly.
werestiff ( 15 N yielded a 1-mm displacementof the unfixed end EMG signalswererectified and integratedover a 3-speriod that
of the steelbar), and therefore the contractions were virtually contained the peak abduction force. A normalized integrated
isometric becausemost subjects’ peak abduction forces were EMG value wascalculatedfrom the ratio of the highestintegrated
<20 N. EMG and the subject’saverageM-wave value (the standarddevia-
An inherent difficulty in strengthtraining studiesisthe possibil- tion was < 1%of the meanM-wave in most of the subjects).This
ity that subjectsdid not usetruly maximal efforts for producing ratio wasusedasthe dependentEMG measure.
forcesin pretrainingtests.Thereforewe attemptedto increasesub-
jects’ motivation during the pretraining test. Each subject was Statistical analyses
askedabout his/her height and weight after a few attempts at
MVC. A horizontal trace wasthen indicated on the oscilloscope One-way analysesof variance were performedbecauseour pri-
that was5- 10%higherthan the subject’smost recent force trace. mary interestwasto comparethe data for a specificvariable(e.g.,
The subjectwasthen told that previous researchindicated that
80%of peoplehis/ her size can reachthe indicated target.
EMG MEASUREMENTS. Bipolar surface EMG of the abductor
digiti minimi muscle was obtained during the maximal finger
force measuresof eachhand. Before the fifth finger wasinserted
into the metal tube, the skin overlying the musclewascleansed \ ABDUCTION
with alcohol. Burdick Cor-Gel Electrolyte wasappliedto a pair of FORCE

in vivo metric (IVM) silver silver-chloride electrodes(4 mm

diam). Theseelectrodeswereappliedto the skin over the abductor
digiti minimi musclebelly and oriented in a line roughly parallel
to the musclefibers with - 15 mm betweenthe centersof the
electrodes.The location of eachelectrodeon the skinwascarefully
measuredin relation to anatomic landmarks and marked with
permanentink during the pretestto facilitate electrodelocations
for the posttest.The indifferent electrodewasplaced on the skin
overlying the lateral epicondyleof the humerus.
TWITCH FORCE. The abduction force resultingfrom supramaxi-
ma1electrical stimulation of the ulnar nerve at the elbow was
measuredwith the apparatusdescribedpreviously. The stimulat-
ing electrodesweretwo chlorided silver disks, 10 mm diam, that
weremountedin a perspexholder with their centers30 mm apart.
 STRENGTH CHANGES AFTER IMAGINED CONTRACTION TRAINING 1117

24

f‘
;18 -

a0 _
0 l2
IL

6
t
0’ ’ ’ ’ ’ ’ ’ ’ FIG. 3. Individual and group left 5th finger abduc-
0 1 2 3 4 5 6 7 8 9 10 0 1 2 3 4 5 6 7 8 tion force changes after training. Open squares, pretrain-
SUBJECT SUBJECT ing test values. Filled squares, posttraining test values. A :
from the Imagining group. B: from the Contraction
40 D group. C: fro m the Control group. D: mean and stan-
T dard deviation of percentage increases of left 5th finger
w 30 abduction force of each group.
z
g 20

s 10

-A
0’ ’ ’ ’ ’ ’ ’ ’ ’ 0
012 3 4 5 6 7 8 9 IMAGINING CONTRACTION CONTROL

SUBJECT GROUP

abduction force) of the pretest with that of the posttestof each subject in the two groups demonstrated a force increase
hand in eachgroup. The dependentmeasureswere maximal ab- (Fig. 3, A and B), but the size of the increase was more
duction force and its correspondingvertical force of the fifth digit, variable across subjects in the Imagining group than in the
twitch force, EMG to M-wave ratio of the hypothenar musclesof c on t raction group (Fig. 3 D). The difference in the mean
two hands,and the extensionforce of the left greattoe. The proba- abduction force increase between these two groups after
bility of 0.05 wasselectedasthe level of significancefor all statisti-
cal analyses. training was not statistically significant (P > 0.1). In con-
trast, the untrained (Control) group showed only a 3.7%
increase in the abduction force (P > 0.08; Fig. 3, C and 0).
RESULTS

Twined hand abduction .force Contralateral untrained hand abduction force

The Imagining group’s maximal voluntary abduction The untrained (right hand) fifth digit of the Imagining
force of the left fifth digit increased 22% (Fig. 3, A and D; group demonstrated a 10.45% abduction force increase on
Table 1) on average after a 4-wk, 20-session imagined con- average (P < 0.005, Fig. 5 and Table 1). Likewise, the ab-
traction training period (P < 0.001). EMG monitoring duction force of the right fifth finger of the Contraction
during 80% of this group’s training sessions confirmed that group showed a 14.43% increase (P < 0.02), which is con-
the hypothenar muscles remained quiescent (Fig. 4). The sistent with previous studies (see Enoka 1988; Sale 1986 for
abduction force of the left fifth digit of the Contraction a summary). The MVC force changes after training be-
group increased 29.75% (P < 0.00 1; Fig. 3, B and D). Every tween the Imagining and Contraction groups were not sig-

TABLE 1. Changesin abduction.forceofthe

. trained and untrained hands,EMG, twitch force, and verticalforce
qfthe trained hand qfier training

Tested Variables Groups Pre Post %Increase

Abduction force, trained hand Imagining” 9.14 + 3.38 11.15 z!I 3.9 22.03 d
Contraction b 14.01 + 3.28 18.20 + 3.97 29.75 d
Control’ 12.13 AI 3.23 12.57 2 3.21 3.68
Abduction force, contralateral hand Imagining 9.43 f 3.23 10.41 AI 3.28 10.45”
Contraction 13.01 k 2.92 14.85 + 3.41 14.13f
Control 11.34 IL 3.36 11.61 + 3.38 2.3
EMG Imagining 2.08 AI 1.42 2.53 f 0.91 21.73
(1.75 It 1.04)9 (2.35 f 0.76)8 34.34f
Contraction 1.62 t 0.67 2.33 + 0.93 43.80f
Control 1.74 + 0.45 1.71 I!I 0.51 -1.63
Flexion force Imagining 4.36 k 1.42 5.78 of:2.30 32.2 1
Contraction 7.06 f: 3.41 9.07 Ifr 3.14 28.39
Control 6.13 AI 1.52 5.81 AI 1.57 -5.20
Twitch force Imagining 3.18 + 1.00 3.21 k 1.19 1.04
Contraction 4.57 + 1.92 4.46 + 1.68 -2.48
Control 3.7 1 + 2.25 3.82 IL 2.21 2.91

Values are means + SD in N except values in EMG, which represent means k SD of the ratios of integrated EMG to M-wave. EMG, electromyogram.
an = 10. bn = 8. ‘n = 9. dP < 0.00 1. “P < 0.0 1. fP < 0.05. gValues from the analysis when the EMG scores from subject 10 were excluded.
1118 G. YUE AND K. J. COLE

strength increases. The left hypothenar muscle EMG data

EMGIMMC
are listed for the three groups in Table 1. The integrated
EMG normalized to the M-wave (see METHODS) of the
500 ms trained hand in the Imagining group increased after train-
EMGMVC
ing in 9 of the 10 subjects to an average of 2 1.73% (Fig. 6,
Table 1). However, this EMG increase fell short of our
designated level of statistical significance (P = 0.08). Fur-
ther statistical analyses of the data revealed a powerful ef-
fect from the data of subject 10 (Table 1 ), whose EMG level
substantially decreased with a seemingly paradoxical in-
crease in abduction force ( 13%, Fig. 3A ), and no change in
twitch force. Therefore, assuming that muscle hypertrophy
did not occur ( see DISCUSSION), the strength increase in this
subject must be due to I ) increased net muscle activity that
FIG. 4. Comparison between raw surface EMG from an imagined maxi- was not registered electromyographically, or 2) improved
mal contraction and that from an MVC. Top trace: during an imagined
maximal muscle contraction (EMG IMMC) of the left 5th digit. Bottom coordination of muscles, such as a decrease in activity of
trace: during a maximal abduction contraction (EMG MVC) of the same antagonist muscles (see DISCUSSION). The left hypothenar
digit. The figure indicates that the muscle was inactive during the imagined EMG of the Contraction group demonstrated a significant
contraction training. From subject 9 in the Imagining group. increase (43.8%) after training (P < 0.05; Fig. 6, B and 0).
The posttest EMG of the same muscles of the same limb in
nificantly different (P > 0.5, Fig. 5 ) . The force change ob- the Control group remained unchanged (- 1.6%, P > 0.5;
served for the right hand of the Control group between the Fig. 6, C and D). In the right (untrained) hand, no signifi-
pre- and posttests was not significant (a 2.3% increase, cant EMG change was found in any of the three groups
P > 0.3). after training even though the Imagining and Contraction
groups increased their strength significantly.
A Pearson product-moment correlation coefficient analy-
Strength of the control muscles
sis across subjects indicated that increases in the abduction
Extensors of the left great toe were used as nontrained, force were not strongly correlated with increases in the hy-
nonhand control muscles within each subject. The exten- pothenar EMG in either the Imagining group ( r = 0.57, P >
sion force measured from the great toe increased 3 t 4.74% 0.08) or the Contraction group ( r = 0.09, P > 0.5 ).
(SD) in the Imagining group and decreased 1.8 t 6.12%
(SD) and 3.1 t 4.8% (SD) in the Contraction and Control Flexion force of thejjlh digit
groups. These changes did not achieve statistical signifi-
cance. Finger flexion forces were monitored as an indirect indi-
cation of potential changes in activation patterns across
muscles because of training ( Fig. 7 ). That is, proportional
Muscle activity changes
increases in abduction and flexion forces are consistent
A finding of increased EMG levels in the two training with increased strength in abductor digiti minimi given its
groups would be consistent with increased motoneuron ac- flexion and abduction moment arms at the metacarpopha-
tivation as a mechanism for the observed abduction langeal joint (Brand 1985; Thomine 198 1). In the trained
20
1 m
l
B
16 8
0
0 0
cl m O
0

l
0

01 ’ ’ ’ ’ ’ ’ ’
0 1 2 3 4 5 6 7 6 9 10 0 1 2 3 4 5 6 7 0 FIG. 5. Individual and groun right (contralateral
\
SUBJECT SUBJECT untrained) 5th finger abd&ion foice changes after
training. Open squares, pretraining test values. Filled
squares, posttraining test values. A-C as in Fig. 3. D:
20 mean and standard deviation of percent increases of
B the right 5th finger abduction force of each group.
16

5F I
I
8
0

012 3 4 5 6 7 6 9 IMAGINING CONTRACTION CONTROL

SUBJECT GROUP
 STRENGTH CHANGES AFTER IMAGINED CONTRACTION TRAINING 1119

6- 4-
A B
0 n n w
O5
F 03 -
m
a4- I 2 Id
CT CT cl
m
s3- ! m li* 0 0

z*- : m
0 8 n
. l z n .0 FIG. 6. Individual and group left hypothenar inte-
W Cl l
Wl- 0
1 - cl O 0 0 grated EMG changes after training. Integrated EMG
Cl was normalized by measuring the ratio of integrated
0,0 1 ’ 2 ’ ’
3 4’ 5’ 6 ’ 7’ 8’ 9 ’ 10 0 0 I I 1 1 , , EMG to M-wave. Open squares, pretraining test mea-
sures. -. Filled - squares,
SUBJECT
1 2 3 6 7 8 posttraining test measures. A-C
. kg. a U: ..-.. deviation of^percent
SUB:EC:
as m 3. mean and standard
increases of the left hypothenar integrated EMG of
150 -
C D each group. Note a large EMG increase (subject 7) and
120 - decrease (subject 10) in the Imagining group, large in-
I creases of subjects I and 2 in the Contraction group.
ifi go-
Also note the large variations of EMG increases among
2
n subjects in the 2 experimental groups.
0 s 5 60 -

! n . 0 0 n 0 z
- 30 -
m s
0

0 12 3 4 5 6 7 8 9 IMAGINING CONTRACTION CONTROL

SUBJECT GROUP

(left) hand, the metacarpophalangeal flexion force in- strength may have resulted from improved coordination of
creased 32% (P > 0.1) for the Imagining group. The Con- the various muscles controlling the digit. This may repre-
traction group showed an increase of 28.4% (P > 0.2), and sent another type of neural adaptation that occurs besides
the Control group showed a 5.2% decrease (P > 0.5) of the increases in net excitatory drive to the prime mover. How-
metacarpophalangeal flexion force (Table 1). Many sub- ever, unambiguous interpretations in this regard would re-
jects in the two training groups manifested flexion force quire observation of all muscles that cross the metacarpo-
increases that were disproportional to their abduction force phalangeal joint, particularly because most have moment
increases. Moreover, some subjects showed no flexion force arms in more than one plane.
increase, whereas others showed decreased flexion force de- In the untrained hand, the Imagining group demon-
spite abduction force increases. These findings are summa- strated an increase of 19.64% (P > 0.4) in the fifth finger
rized in Table 2 with the use of ratios of the percent flexion vertical force, and the Contraction group had an increase of
force increase to percent abduction force increase from - 12% (P > 0.7). The vertical force of the right fifth digit of
each subject. A ratio of 1 indicates flexion force increases the Control group remained virtually unchanged (a 1% de-
that were proportional to increases in abduction force. crease, P > 0.9) after training. The flexion force increases
Pearson product-moment correlation coefficient analyses were not proportional to the abduction force increases.
of the percent changes in abduction and flexion force were
not significant for either the Imagining group ( r = 0.16, P > Left fifth digit twitch abduction force
0.5) or the Contraction group (r = 0.34, P > 0.3). It thus The twitch forces generated by supramaximal electrical
appears that in some subjects the increased abduction stimulations were measured, and an average of 10 trials was

m
l

m 0
0 0 FIG. 7. Individual and group left 5th digit flexion
force changes after training. Open squares, pretrain-
ing test values. Filled squares, posttraining test val-
0 1 2 3 4 5 6 7 8 9 10 0 1 2 3 6 7 8 ues. A-C as in Fig. 3. D : mean and standard devia-
SUBJECT SUBiEC? tion of percent increases of the left 5th digit flexion
force of each group. Although no group showed signif-
icant changes in flexion force, some subjects demon-
strated much larger increases than the others (A-C).
The Contraction and Imagining groups showed con-
siderably larger variations in flexion force increases
than those in abduction force (D).

0 12 3 4 5 6 7 8 9 IMAGINING CONTRACTION CONTROL

SUBJECT GROUP
1120 G. YUE AND K. J. COLE

TABLE 2. Ratios of %increaseinflexion .force to that of 198 1; Goldberg et al. 1975; Goldspink and Howells 1974;
ahduction&forceof’the left 5th digit of individual subjects MacDougall 1986). Also in some studies, muscle hyper-
trophy was not found even after 20 sessions of near maxi-
Groups mal intensity strength training (Fukunaga 1976; Ikai and
Fukunaga 1970). In the present study, surface EMG re-
Subjects Imagining” Contraction b Control’ corded in all subjects during the 4-wk period of imagined
I -2.48 d 6.74 - 1.49 contraction training indicated that the trained muscle was
2 0.16 0.33 E” virtually inactive during the training sessions (Fig. 4). This
3 2.06 -0.68 0.83 does not preclude the possibility that other active training
4 0.63 -0.28 Of may have occurred through daily living activities during the
5 4.62 0.08 1.68
6 0.23 1.39 2.05 4-wk training period despite our strict cautions against such
7 0.6 1 1.27 1.83 activity. However, 1t seems highly unlikely that casual
8 3.68 3.16 -6.46 training of this type co uld ind uce mu scle hypertroph Y,Par-
9 5.80 ticularly after such a short period.
10 4.13 The lack of change in evoked twitch tension in the pres-
a 11 = 10. bag= 8. ‘n = 9. dA negative ratio indicates a decrease in the ent experiment may also be used to argue against hyper-
flexion force. “The abduction force increase was zero for this subject. fThe trophy (Close 1972) and is consistent with previous studies
flexion force increase was zero for this subject. that failed to induce evoked muscle tension increases even
after 5 wk of high-intensity strength training (Davies and
used as the twitch force for each subject. No significant Young 1983; McDonagh et al. 1983). Nevertheless, it is
unwise to infer that unchanged or decreased evoked twitch
change was found in the twitch force after training in any of
the three groups (P > 0.5, Table 1) . On average, the Imagin- tensions reflect an absence of muscle hypertrophy. Studies
ing group increased 1.04 t 14.94% (SD), the Contraction of joint immobilization have reported inconsistent changes
group decreased 2.48 t 11.3% (SD), and the Control group of twitch force, or ratios of twitch force to tetanic tension, of
increased 2.9 1 t 10.69% (SD). a muscle with demonstrable atrophy (e.g., Mayer et al.
198 1; Reiser et al. 1988; Robinson et al. 199 1; Sale et al.
1982). It has been suggested that the inconsistent change in
DISCUSSION
twitch force after muscle atrophy may be due to immobili-
The maximal force increases in subjects who trained us- zation-induced changes in muscle, including modifications
ing effortful muscle contractions were similar to those who of mechanical properties of a muscle fiber (Sale et al.
only imagined producing similar contractions during train- 1982 ), or alterations in speed or d uration of calcium release
ing. It is therefore possible that similar mechanisms were from the sarcoplasm iC reticulum (Reiser et al. 1988).
responsible for the strength gains in the two groups. If so, Two possible neural mechanisms jtir strength increase
the increased strength that occurs early in a conventional
training regimen, during the so-called “neural” phase, may At least two mechanisms may have contributed to the
not result from repetitive muscle activation. The possible increased force produced by both training groups. The hy-
origins of these strength increases may include program- pothenar EMG increases indicate that the abduction force
ming/planning levels of a hierarchically organized motor gain occurred from increased muscle activation (Hakkinen
system (Hasan et al. 1985; Brooks 1986). It is necessary et al. 198 1,1985; Hakkinen and Komi 1983,1986; Komi et
first to consider alternative explanations to neural mecha- al. 1978; Moritani and de Vries 1979), most likely the ab-
nisms that may underlie the observed strength increases. ductor digiti minimi. Increased motoneuron activation has
When measuring maximal voluntary contractions, one been acknowledged as an important source of strength in-
must very carefully consider psychological or emotional crease during the first weeks of conventional strength train-
factors that may yield apparent strength increases. It is un- ing (Enoka 1988; Komi 1986; McDonagh and Davies
likely that the strength gains in the present study resulted 1984; Sale 1986). It also appears that some subjects devel-
from psychological or emotional factors given the Control oped better strategies for activating the muscles crossing the
group’s lack of strength gain and the virtual absence of metacarpophalangeal joint, as indicated by a dispropor-
strength increases of the left great toe extensors in any tional increase in the finger’s flexion force as compared
group. Also, sham information provided to subjects con- with the abduction force increase after training. Fl exion
cerning their performance during the pretraining strength and abduction force changes should be yoked to each other
test appeared to be highly motivating (see METHODS) and, (with the relationship determ ned by the ratio of the abduc-
hopefully, reduced the likelihood of increased effort for the tor m uscles’ moment arms n each direction) 9 provided
posttraining measures. that other muscles’ activation levels remain unchanged.
Muscle hypertrophy also can significantly influence mus- Rutherford and Jones ( 1986) suggested that the increased
cle strength after training. If the mass of a muscle is en- capacity to lift weights with practiced lower leg extension
larged by increasing the cross-sectional area of each fiber, or movements was partial1 .y due to an increase in the skill of
the number of the fibers after training, a larger muscle coordinating all muscle groups involved in the movement,
strength output is expected from the increased number of including those used to stabilize the body. Improved mus-
parallel sarcomeres in the muscle (Edgerton et al. 1986). cle coordi nation at a joint with multi ple degrees of freedom
However, repeated production of high-intensity muscle ac- should be considered as a potential mechanism in the early
tivation is typically required for muscle hypertrophy (Atha so-called neural phase of strength training.
 STRENGTH CHANGES AFTER IMAGINED CONTRACTION TRAINING 1121

The poor correlation between the increases in EMG and We suggest instead that the neural changes after the men-
abduction force of the fifth digit may also be interpreted to tal training occurred at programming or planning levels of
indicate that some of the strength increase was due to acti- the motor system, most likely involving nonprimary cere-
vation of the fifth finger’s other muscles in a manner for bral cortical motor areas. The altered “program” in turn
more efficient metacarpophalangeal abduction torque pro- may achieve strength gains via actions on spinal circuitry
duction. However, such interpretations are hazardous be- such as inhibition of Renshaw cells (Butler and Darling
cause EMG often reflects an imperfect sampling of the 1990), or other means of changing the excitatory and inhibi-
neural activation of a muscle, and changes in isometric tory influences on motoneurons. This interpretation is bol-
force and EMG level are not always simply related, particu- stered by reports that neuronal activation, presumably as-
larly at high muscle activation levels (Howard and Enoka sociated with motor programming/ planning, can occur
199 1; for a review see Soderberg and Cook 1984). Also, it is without activating muscle (Roland et al. 1980), and that
unlikely that EMG recording during MVCs with surface mental training of motor skills (i.e., with quiescent mus-
electrodes on the hypothenar eminence reflect only the ac- cles) can improve motor performance and skill acquisition
tivity of the abductor digiti minimi. The difficulties in inter- (Corbin 1972; Fetz and Landers 1983; Hall 1985; Richard-
preting EMG-force relationships in the present study are son 1967). In these experiments it seems unlikely that de-
illustrated by the finding that the contralateral (untrained) scending pathways and spinal circuits were activated but
hand strength increases in many subjects were not accompa- inhibited at some point to prevent motoneuron activation.
nied by EMG increases. A definitive demonstration of the Given the similar strength increases in the Contraction and
role of learning more efficient muscle activation patterns Imagining groups of the present experiment, it may be that
for torque production requires separately recording the ac- short-term, high-intensity muscle contraction training pro-
tivity of each muscle that crosses the joint. For abduction of duces only adaptations of cortical programming/ planning
the fifth digit, one must record from the fourth palmar in- areas.
terosseous, a primary antagonist to abduction. The size and One assumption necessary in suggesting that program-
location of this muscle makes it difficult, although not im- ming/planning changes underlie strength increases is that a
possible to place indwelling electrodes. maximal muscle contraction requires motor program-
ming/planning. Although there is evidence that imagining
Strength increases ftrom changes in the motor program a sequence of independent finger movements activates sup-
plementary motor area neurons in humans (Roland et al.
Because it was unlikely that the strength increases in the 1980), it is not known whether such activation occurs when
Imagining group were due to hypertrophy or psychological performing a maximal contraction. However, Roland
factors, the repeated imagined contractions must be consid- ( 1985) suggested that a maximal muscle contraction may
ered as the factor initiating the increased motoneuron acti- require programming given the need for high effort levels.
vation and improved coordination. It is reasonable to con- Roland and his colleagues ( 1980) reported evidence for
sider the nervous system levels that may have been involved low-level activation of the supplementary motor area dur-
in this process. At the lower levels of a hierarchically orga- ing submaximal isometric contractions (Roland et al.
nized motor system, strength increases in general have been 1980).
attributed to changes in the physiological properties of spi-
nal motoneurons, interneurons and associated reflex path-
ways, and descending pathways (Hakkinen and Komi Strength increases Qfthe contralateral (untrained) jinger
1986; Komi et al. 1978; Milner-Brown et al. 1975; Sale et
al. 1983a,b; Upton and Radford 1975) and/or the morpho- The finding of increased strength in the hand contralat-
logical properties of these neurons (Geinismann et al. 197 1; era1 to the trained hand is consistent with previous findings
Gerchman et al. 1975; Gilliam et al. 1977; Kamen et al. (cf. Enoka 1988; Sale 1986). The comparable levels of
1984; Tomanek and Tipton 1967 ). The ultimate result of force increase in the contralateral untrained hand of the
these changes is greater net motoneuron excitation on max- Imagining and Contraction groups prompts the speculation
imal effort contractions. However, muscle activity is ex- that changes in the motor program acquired via training of
pected to signal activation of these levels, and repeated exe- one hand may transfer to the contralateral hand. These
cutions of motor commands may be required before neural training-induced changes may occur in areas that can influ-
changes are induced at these lower levels of the motor sys- ence both ipsi- and contralateral motor areas, such as the
tem. Although powerful muscle contractions occurred dur- supplementary motor area. Brinkman ( 1984) observed
ing the MVC training, muscles were quiescent during the that unilateral lesion of the supplementary motor area in
imagined training, making it unlikely that the neural monkeys produced a deficit in bimanual coordination.
changes responsible for the strength increases in the Imagin- That is, the movements of both hands were similar even
ing group occurred at the motor system’s executional level. though successful task performance required very different
With this interpretation we assume that the Imagining movements of each hand. Section of the corpus callosum
group did not change the frequency, duration, or level of resulted in the disappearance of the synkinetic (“mir-
activation of the hypothenar muscles during the 4-wk train- rored”) movements and a return to independent action of
ing period. In support of this assumption, we have observed the two hands. It was suggested that in normal monkeys,
similar effects in experiments involving a 5-wk period of the supplementary motor area may provide information to
joint immobilization that yielded measureable muscle atro- the opposite hemisphere about the intended and/or ongo-
phy (Yue et al. 1991). ing movements (Brinkman 1984).
1122 G. YUE AND K. J. COLE

Strength increases in proximal versus distal muscles GOLDSPINK, G. AND HOWELLS, K. F. Work-induced hypertrophy in exer-
cised normal muscles of different ages and the reversibility of hyper-
The large strength increases observed for the Imagining trophy after cessation of exercise. J. Physiol. Land. 239: 179- 193, 1974.
group may indicate a therapeutic technique for combating HAIUUNEN, K., ALEN, M., AND KOMI, P. V. Changes in isometric force
and relaxation time, electromyographic and muscle fiber characteristics
the loss of strength after periods of muscle disuse from joint of human skeletal muscle during training and detraining. Acta Physiol.
immobilization, peripheral nerve injuries, and the like. Stand. 125: 573-585. 1985.
However, the present study focused on hand muscles, HAKIUNEN, K. AND KOMI, P. V. Electromyographic changes during
which show disproportionately large representations in the strength training and detraining. Med. Sci. Sports Exercise 15: 455-460,
primary motor cortex. Also, the fifth digit abductor muscles 1983.
HAKKINEN, K. AND KOMI, P. V. Training induced changes in neuromuscu-
may be relatively unused in the skills of daily living. Similar lar performance under voluntary and reflex conditions. Eur. J. AppZ.
results must be demonstrated for proximal and often-used Physiol. 55: 147-155, 1986.
muscles before the potential therapeutic benefits of imagi- HAI&NEN, K., KOMI, P. V., AND TESCH, P. Effect of combined concentric
nary techniques for strength preservation can be assessed. and eccentric strength training and detraining on force time, muscle
fiber and metabolic characteristics of leg extensor muscles. Stand. J.
Sports Sci. 3: 50-58, 198 1.
We thank Drs. Warren G. Darling, Carl G. Kukulka, and Erich S. HALL, C. R. Individual differences in the mental practice and imagery of
Luschei for valuable comments on the manuscript and James A. Hadar for motor skill performance. Can. J. AppZ. Sport Sci. 10: 17S-2 1S, 1985.
clerical and editorial assistance. HASAN, Z., ENOKA, R. M., AND STUART, D. G. The interface between
This research was supported by Grants YA l-9005- 1 from American biomechanics and neurophysiology in the study of movement: some
Paralysis Association, 2408-95 from The University of Iowa Collegiate recent approaches. Exercise Sport Sci. Rev. 13: 169-234, 1985.
Association Council, and a grant in aid of research from Sigma Xi, The HELLEBRANDT, F. A., PARRISH, A. M., AND HOUTZ, S. J. Cross education:
Scientific Research Society. the effect of unilateral exercise on the contralateral limb. Arch. Phys.
Address for reprint requests: K. J. Cole, Dept. of Exercise Science, The Med. 28: 76-85, 1947.
University of Iowa, Iowa City, IA 52242. HOUSTON, M. E., FROESE, E. A., VALERIOTE S. P., GREEN, H. J., AND
&WNEY, D. A. Muscle performance, morphology and metabolic capac-
Received 20 May 199 1; accepted in final form 20 December 199 1. ity during strength training and detraining: a one leg model. Eur. J.
AppZ. Physiol. 5 1: 25-35, 1983.
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