1992 Journal of Neurophysiology

JOURNALOF Vol. 67. No.

NEUROPHYSIOLOGY 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

I. This study addressed potential neural mechanisms of the strength increase that occur before muscle hypertrophy. In particu- lar we examined whether such strength increases may result from training-induced changes in voluntary motor programs. We compared the maximal voluntary force production after a training program of repetitive maximal isometric muscle contractions with force output after a training program that did not involve repetitive activation of muscle; that is, after mental training.

2. Subjects trained their left hypothenar muscles for 4 wk, five sessions per week. One group produced repeated maximal isometric contractions of the abductor muscles of the fifth digit’s metacarpophalangeal joint. A second group imagined producing these same, effortful isometric contractions. A third group did not train their fifth digit. Maximal abduction force, flexion/extension force and electrically evoked twitch force (abduction) of the fifth digit were measured along with maximal integrated electromyograms (EMG) of the hypothenar muscles from both hands before and after training.

3. Average abduction force of the left fifth digit increased 22% for the Imagining group and 30% for the Contraction group. The mean increase for the Control group was 3.7%.

4. The maximal abduction force of the right (untrained) fifth digit increased significantly in both the Imagining and Contrac- tion groups after training ( 10 and 14%, respectively), but not in the Control group (2.3%). These results are consistent with previous studies of training effects on contralateral limbs.

5. The abduction twitch force evoked by supramaximal electrical stimulations of the ulnar nerve was unchanged in all three groups after training, consistent with an absence of muscle hypertrophy. The maximal force of the left great toe extensors for individual subjects remained unchanged after training, which argues against strength increases due to general increases in effort level.

6. Increases in abduction and flexion forces of the fifth digit were poorly correlated in subjects of both training groups. The fifth finger abduction force and the hypothenar integrated EMG increases were not well correlated in these subjects either. To- gether these results indicate that training-induced changes of synergist and antagonist muscle activation patterns may have contributed to force increases in some of the subjects.

7. Strength increases can be achieved without repeated muscle activation. These force gains appear to result from practice effects on central motor programming/planning. The results of these experiments add to existing evidence for the neural origin of strength increases that occur before muscle hypertrophy.

INTRODUCTION

Skeletal muscle strength gains from isometric strength training are believed to result from two principal factors. Whereas muscle hypertrophy occurs in the later stages of training (Enoka 1988; Komi 1986; McDonagh and Davies

1984; Sale 1986), strength gains achieved during the first weeks of training reflect an increased ability to activate motoneurons and therefore appear to be neural in origin. Abundant evidence demonstrates neural changes that occur soon after training begins. Voluntary strength increases rapidly before the muscles exhibit hypertrophy (Fukunaga 1976; Ikai and Fukunaga 1970; Jones and Rutherford 1987; Liberson and Asa 1959; Moritani and de Vries 1979; Rose et al. 1957; Tesch et al. 1983) and before increases in electrically evoked tension occur (Davies and Young 1983; McDonagh et al. 1983 ) . These early voluntary strength increases are accompanied by increased integrated electromyograms (EMG) (Komi 1986; Sale 1986) and increased reflex gains (Milner-Brown et al. 1975; Sale et al. 1982, 1983a,b; Upton and Radford 1975 ). The greatest strength gains occur at the trained joint angles (Gardner 1963; Lindh 1979; Meyers 1967 ). Finally, training of one limb is associated with increased voluntary strength in the contralateral (untrained) muscles (e.g., Hellebrandt et al. 1947; Houston et al. 1983; Rose et al. 1957; see Enoka 1988; Sale 1986 for a review), even though the contralateral muscles remain virtually quiescent during training (Houston et al. 1983; Panin et al. 196 1; Yasuda and Miyamura 1983).

The neural mechanisms of these strength gains are poorly understood. However, the previously noted phenomenon of increased strength from muscles contralateral to those that were trained raises the intriguing possibility that early strength gains may be induced without repetitive muscle activation; that is without repetitive activation of motoneu- Tons, spinal interneurons, or possibly, descending motor pathways. Instead, early strength gains may depend on changes in the central programming of a maximal voluntary contraction. If so, it may be possible to induce changes in the motor program for a maximal voluntary contraction via mental practice (that is, imagining performance of a skilled movement without overt or covert muscle activation).

Research on skill acquisition has demonstrated clearly that mental practice leads to improved performance (e.g., Rawlings et al. 1972; Vandell et al. 1943; also see Corbin 1972; Fets and Landers 1983; Hall 1985; Richardson 1967 for a summary). Individuals asked to imagine themselves performing skilled, serial movements of the digits manifested increased cerebral blood flow in nonprimary motor regions of the cerebral cortex without evidence of activating the primary motor cortex (Roland et al. 1980). It is possible therefore that repeated imagined muscle contractions may alter the program for maximal torque production at a 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 of synergist and antagonist muscles across a joint to yield increased torque in the desired direction. The latter phenomenon, changes in muscle “coordination,” may occur particularly for strength training involving multijoint movements or movements at a joint with multidirectional freedom (Rutherford and Jones 1986). The contribution of this improved coordination to early strength gains remains unclear.

This investigation addressed whether imagined maximal muscle contraction training increases maximal voluntary contraction (MVC) force and compared any strength increases with those found in the early periods of training by the use of MVCs. Our experimental design included attempts to control or measure effort level, strength increases not specific to the trained muscle, and muscle hypertrophy. After 20 sessions, imagined maximal contraction and MVC training produced comparable levels of voluntary strength increase.

METHODS

subjects

The subjects were 30 healthy individuals (2 l-29 yr of age) who claimed not to have participated in regular muscular training in the two years before this study. Ten subjects each were randomly assigned to one of three groups. Subjects in the Imagining group were trained by an imagined maximal muscle contraction method; subjects in the Contraction group produced MVCs during their training. The Control group was instructed to refrain from strength training and sports activities using the hand. In- formed consent was obtained from each subject before the experiment. Three subjects ( 1 in the Control group and 2 in the Contrac- tion group) failed to return for posttraining testing.

General aperimentul procedures

The experiment consisted of a pretraining measurement session, a 4-wk (20-session) training period focused on increasing abduction force of the metacarpophalangeal joint of the left fifth digit, and a posttraining measurement session. Abduction of the left fifth digit was selected because the muscles of abduction are used principally in tasks such as opening the grip and thus are not typically engaged in sustained, high force output in most activities of daily living. Training effects (neural changes and muscle fiber hypertrophy) may be achieved more easily. The following data were collected from each subject’s ipsilateral and contralateral hands during the pre- and posttraining measurement sessions: I) maximal isometric abduction force at the metacarpophalangeal joint of the fifth digit; 2) flexion/extension force at the metacarpophalangeal joint of the fifth digit during maximal abduction force production (measured to indicate possible changes in muscle coordination): 3) twitch force (abduction) of the fifth digit generated by supramaximal electrical stimulation of the ulnar nerve (taken as a possible indication of muscle hypertrophy; however, cf. DIS-

CUSSION): 4) surface EMG during the maximal abduction force task from electrodes placed on the hypothenar eminence approxi- mately over the abductor digiti minimi (although other hypothenar muscles, or the interossei may have contributed to this EMG during a maximal force exertion because of their proximity to the recording electrodes). In addition, the maximal extension force of the left great toe served as a control for nonspecific training effects such as strength gains in untrained muscles.

Equipment

Horizontal (abduction) force of the fifth digit was measured with a cantilever-beam transducer instrumented with strain gauges (Fig. 1). A second force transducer was mounted orthogo- nally on the first to measure the vertical ( flexion-extension) force. The transducers were constructed of two stainless steel bars 2.5 x 7.0 X 0.1 cm. The cross talk of the vertical force transducer to the horizontal transducer was 0.45%, indicating a near orthogonal relation between the steel bars. The end of the beam that measured the vertical force was securely attached to a rigid microscope stand to allow adjustments of the transducer system’s position. A metal tube ( 12 mm long and 15 mm diam) was secured to the free end of the transducer that measured the abduction force. The tube could be moved from one side of the bar to another so that the same transducers were used for both hands (Fig. 1). A similar transducer system was used to measure the extension force of the left great toe.

Procedures

The training programs for the Imagining and Contraction groups lasted 4 wk with five training sessions per week. The subjects were trained Monday through Friday of each week in the Motor Control Laboratory at The University of Iowa. IMAGINEDCONTRACTION TRAINING. Duringeachtrainingses- sion, subjects in the Imagining group were instructed to perform 15 imagined maximal contractions of the left abductor digiti minimi with a 20-s rest after every second trial. Subjects were told that the training involved imagining muscle contractions and that all the upper limb muscles, especially the trained muscle, should be relaxed as much as possible. In short, they were instructed to maximally activate the brain but not to activate the muscle. Hypoth- enar EMG (see EMG MEASUREMENTS) was monitored during most of these training sessions. Subjects were seated comfortably in a chair with their left arm resting on a table. The hand was kept open and relaxed with the palm facing downward. On a verbal signal to begin, the subject was instructed to concentrate on the left fifth finger and imagine the finger pushing maximally against the horizontal force transducer that was used during the pretraining test. The imaginary maximal finger abduction was to be maintained

FIG. 1. Finger force measurement equipment and subject positioning. A: transducer for abduction force. B: transducer for extension/flexion force. C, D, and F: finger, hand, wrist, and arm restraints. E: surface EMG electrodes. G: reference electrode. Stimulation electrodes are located at the 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. During this 15-s period, the subject was instructed to keep imagining a voice shouting “harder, harder. . . .”

MVC TRAINING. The subjects in the Contraction group sat in a chair with their left arms resting on a table. The hand was relaxed, with palm facing downward and the distal part of the fifth digit positioned against a stop that was rigidly fixed to the table surface. The subject abducted his/her left fifth digit as forcefully as possible. During each training session, subjects in the Contraction group were instructed to perform 15 MVCs of the left abductor digiti minimi with 20 s of rest separating each contraction. Each trial lasted - 10 s.

CONTROL GROUP. Subjects in the Control group were not trained, but participated in the measurements before and after training. The subjects were instructed strictly to avoid any physi- cal exercise or mental training of the hypothenar muscles during the time period between the pre- and posttests.

PRE- AND POSTTRAINING FORCE MEASURES. The subjects rested their arms on the table with the palm of the hand facing downward and slid the fifth digit into the metal tube on the force transducer (Fig. 1). The distal edge of the tube (the edge away from the subject) was aligned with the base of the fingernail during both pre- and posttests. The index, middle, and ring fingers were stabilized on the table with a strap. An aluminum bar mounted on the table was placed between the fourth and fifth digits to maintain an angle of - 5’ between the digits; this ensured roughly similar muscle lengths during both pre- and posttests. Straps were used to prevent arm motion or vertical motion of the wrist (Fig. 1).

Each subject warmed up with several submaximal contractions, then executed five or six maximal contractions of the abductor digiti minimi lasting -4 s with a resting period of at least 30 s between trials. Each subject was instructed to exert a lateral force with the fifth digit against the force transducer. The transducers were stiff ( 15 N yielded a 1 -mm displacement of the unfixed end of the steel bar), and therefore the contractions were virtually isometric because most subjects’ peak abduction forces were <20 N.

An inherent difficulty in strength training studies is the possibility that subjects did not use truly maximal efforts for producing forces in pretraining tests. Therefore we attempted to increase subjects’ motivation during the pretraining test. Each subject was asked about his/her height and weight after a few attempts at MVC. A horizontal trace was then indicated on the oscilloscope that was 5- 10% higher than the subject’s most recent force trace. The subject was then told that previous research indicated that 80% of people his/ her size can reach the indicated target. EMG MEASUREMENTS. Bipolar surface EMG of the abductor digiti minimi muscle was obtained during the maximal finger force measures of each hand. Before the fifth finger was inserted into the metal tube, the skin overlying the muscle was cleansed with alcohol. Burdick Cor-Gel Electrolyte was applied to a pair of in vivo metric (IVM) silver silver-chloride electrodes (4 mm diam). These electrodes were applied to the skin over the abductor digiti minimi muscle belly and oriented in a line roughly parallel to the muscle fibers with - 15 mm between the centers of the electrodes. The location of each electrode on the skin was carefully measured in relation to anatomic landmarks and marked with permanent ink during the pretest to facilitate electrode locations for the posttest. The indifferent electrode was placed on the skin overlying the lateral epicondyle of the humerus. TWITCH FORCE. The abduction force resulting from supramaxi- ma1 electrical stimulation of the ulnar nerve at the elbow was measured with the apparatus described previously. The stimulat- ing electrodes were two chlorided silver disks, 10 mm diam, that were mounted in a perspex holder with their centers 30 mm apart.

These electrodes were treated with an electrolyte paste, placed on the skin overlying the ulnar nerve located between the medial epicondyle and the olecranon of the ulna, and held in place with an elastic strap. The stimuli consisted of rectangular voltage pulses 0.2 ms in duration delivered from a stimulator (Grass model S88 with a Grass model SIUS stimulus isolation unit). The stimulus intensity was set 30 V greater than that for a maximal M response. There were 10 twitch trials (providing twitch force and M-wave data) in each test with 10 s rest between each pair of trials. TOE FORCE. Isometric force measures were obtained from the left great toe of seated subjects by the use of procedures comparable with those described for the finger force measures. Each subject performed five to six trials of maximal toe extension force and rested for at least 30 s between every two trials.

Data recording and analysis

The force transducer signals were amplified and low-pass fil- tered at 500 Hz (Biocommunication Electronics model 205). EMG signals were differentially preamplified ( 10,000 MQ input impedance) with a gain of 100 and a bandpass of 25-10,000 Hz ( Biocommunication Electronics model 30 1) ; subsequent amplifi- cation occurred with a low-pass cutoff of 2,500 Hz. All data were recorded on an eight-channel (Vetter model D) FM tape recorder (DC-l, 125 Hz) and stored for later analysis. Signals were then digitized with an analog-to-digital converter with 12-bit resolu- tion. The force and EMG signals were digitized at 1,000 samples/ s, and the M-wave and twitch responses were digitized at 3,000 samples/s.

For each trial of digitized data, the peak abduction force and the corresponding vertical force were measured ( Fig. 2). The highest abduction force obtained from among the recorded trials was taken as the maximal abduction forces were measured similarly.

force of the fifth digit. The toe

EMG signals were rectified and integrated over a 3-s period that contained the peak abduction force. A normalized integrated EMG value was calculated from the ratio of the highest integrated EMG and the subject’s average M-wave value (the standard deviation was < 1% of the mean M-wave in most of the subjects). This ratio was used as the dependent EMG measure.

Statistical analyses

One-way analyses of variance were performed because our primary interest was to compare the data for a specific variable (e.g.,

\ ABDUCTION FORCE


0 1 2 3 4 5 6 7 8 9 10

SUBJECT

0’ ’ ’ ’ ’ ’ ’ ’ ’ 012 3 4 5 6 7 8 9

SUBJECT

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 tion force changes after training. Open squares, pretrain-

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

-A

abduction force of each group. z g 20

Z

s 10

0

IMAGINING CONTRACTION CONTROL

GROUP

abduction force) of the pretest with that of the posttest of each subject in the two groups demonstrated a force increase hand in each group. The dependent measures were maximal abduction force and its corresponding vertical force of the fifth digit,

(Fig. 3, A and B), but the size of the increase was more

twitch force, EMG to M-wave ratio of the hypothenar muscles of variable across subjects in the Imagining group than in the

two hands, and the extension force of the left great toe. The proba- c on t raction group (Fig. 3 D). The difference in the mean

bility of 0.05 was selected as the level of significance for all statisti- abduction force increase between these two groups after

cal analyses. training was not statistically significant (P > 0.1). In con- trast, the untrained (Control) group showed only a 3.7%

RESULTS increase in the abduction force (P > 0.08; Fig. 3, C and 0).

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. Changes in abduction.force ofthe trained and untrained hands, EMG, twitch force, and vertical force . qfthe trained hand qfier training

Tested Variables Groups Pre Post %Increase

Abduction force, trained hand

Abduction force, contralateral hand

EMG

Imagining” Contraction b Control’ Imagining Contraction Control Imagining

Flexion force

Twitch force

Contraction Control Imagining Contraction Control Imagining Contraction Control

9.14 + 3.38 11.15 z!I 3.9 22.03 d 14.01 + 3.28 18.20 + 3.97 29.75 d 12.13 AI 3.23 12.57 2 3.21 3.68 9.43 f 3.23 10.41 AI 3.28 10.45”

13.01 k 2.92 14.85 + 3.41 14.13f 11.34 IL 3.36 11.61 + 3.38 2.3 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 1.62 t 0.67 2.33 + 0.93 43.80f 1.74 + 0.45 1.71 I!I 0.51 -1.63 4.36 k 1.42 5.78 of: 2.30 32.2 1 7.06 f: 3.41 9.07 Ifr 3.14 28.39 6.13 AI 1.52 5.81 AI 1.57 -5.20 3.18 + 1.00 3.21 k 1.19 1.04 4.57 + 1.92 4.46 + 1.68 -2.48 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.


EMGIMMC

500 ms

EMGMVC

FIG. 4. Comparison between raw surface EMG from an imagined maximal contraction and that from an MVC. Top trace: during an imagined maximal muscle contraction (EMG IMMC) of the left 5th digit. Bottom trace: during a maximal abduction contraction (EMG MVC) of the same digit. The figure indicates that the muscle was inactive during the imagined contraction training. From subject 9 in the Imagining group.

nificantly different (P > 0.5, Fig. 5 ) . The force change observed for the right hand of the Control group between the pre- and posttests was not significant (a 2.3% increase, P > 0.3).

Strength of the control muscles

Extensors of the left great toe were used as nontrained, nonhand control muscles within each subject. The extension force measured from the great toe increased 3 t 4.74% (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 groups. These changes did not achieve statistical significance.

Muscle activity changes

A finding of increased EMG levels in the two training groups would be consistent with increased motoneuron activation as a mechanism for the observed abduction

0 1 2 3 4 5 6 7 6 9 10

SUBJECT

20

16

5F I

B

8 0

012 3 4 5 6 7 6 9 IMAGINING CONTRACTION CONTROL

SUBJECT GROUP

20

1 m

16

0 0 0

strength increases. The left hypothenar muscle EMG data are listed for the three groups in Table 1. The integrated EMG normalized to the M-wave (see METHODS) of the trained hand in the Imagining group increased after training 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 effect from the data of subject 10 (Table 1 ), whose EMG level substantially decreased with a seemingly paradoxical increase 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 was not registered electromyographically, or 2) improved coordination of muscles, such as a decrease in activity of antagonist muscles (see DISCUSSION). The left hypothenar EMG of the Contraction group demonstrated a significant 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 the Control group remained unchanged (- 1.6%, P > 0.5; Fig. 6, C and D). In the right (untrained) hand, no significant EMG change was found in any of the three groups after training even though the Imagining and Contraction groups increased their strength significantly.

A Pearson product-moment correlation coefficient analysis across subjects indicated that increases in the abduction force were not strongly correlated with increases in the hypothenar EMG in either the Imagining group ( r = 0.57, P > 0.08) or the Contraction group ( r = 0.09, P > 0.5 ).

Flexion force of thejjlh digit

Finger flexion forces were monitored as an indirect indication of potential changes in activation patterns across muscles because of training ( Fig. 7 ). That is, proportional increases in abduction and flexion forces are consistent with increased strength in abductor digiti minimi given its flexion and abduction moment arms at the metacarpophalangeal joint (Brand 1985; Thomine 198 1). In the trained

l B

8 cl m O

0

l

0

01 ’ ’ ’ ’ ’ ’ ’ 0 1 2 3 4 5 6 7 0 FIG. 5. Individual and groun right (contralateral

SUBJECT

I

\ 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: mean and standard deviation of percent increases of the right 5th finger abduction force of each group.


6-

A 4-

B O5

0 n n w

F 03 -

a4- m

I CT

2 Id

s3- !

CT cl

m

:

li*

m

0 0

z*- m W 0 8

. l n

z n . 0 FIG. 6. 0 Wl- 0 Cl l

Individual and group left hypothenar inte- 1 - 0 cl O grated EMG changes after training. Integrated EMG

Cl was normalized by measuring the ratio of integrated 0, ’ ’ ’ ’ ’ ’ ’ ’ ’ 0 I I 1 1 , , to test mea- 0 1 2 3 4 5 6 7 8 9 10 EMG M-wave. Open pretraining squares, 0

1 2 3 SUB:EC:

6 7 8 SUBJECT sures. Filled squares, posttraining test measures. A-C . -. a - ..-.. ̂as m kg. 3. U: mean and standard deviation of percent

150 - increases of the left hypothenar integrated EMG of

C D each group. Note a large EMG increase (subject 7) and 120 - decrease (subject 10) in the Imagining group, large in-

I ifi go- creases of subjects I and 2 in the Contraction group.

2 Also note the large variations of EMG increases among n subjects in the 2 experimental groups.

0 s ! n . 0 0 n 0

5 60 -

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 increased 32% (P > 0.1) for the Imagining group. The Con- traction group showed an increase of 28.4% (P > 0.2), and the Control group showed a 5.2% decrease (P > 0.5) of the metacarpophalangeal flexion force (Table 1). Many subjects in the two training groups manifested flexion force increases that were disproportional to their abduction force increases. Moreover, some subjects showed no flexion force increase, whereas others showed decreased flexion force despite abduction force increases. These findings are summa- rized in Table 2 with the use of ratios of the percent flexion force increase to percent abduction force increase from each subject. A ratio of 1 indicates flexion force increases that were proportional to increases in abduction force. Pearson product-moment correlation coefficient analyses of the percent changes in abduction and flexion force were not significant for either the Imagining group ( r = 0.16, P >

strength may have resulted from improved coordination of the various muscles controlling the digit. This may represent another type of neural adaptation that occurs besides increases in net excitatory drive to the prime mover. How- ever, unambiguous interpretations in this regard would require observation of all muscles that cross the metacarpophalangeal joint, particularly because most have moment arms in more than one plane.

In the untrained hand, the Imagining group demonstrated an increase of 19.64% (P > 0.4) in the fifth finger vertical force, and the Contraction group had an increase of - 12% (P > 0.7). The vertical force of the right fifth digit of the Control group remained virtually unchanged (a 1% decrease, P > 0.9) after training. The flexion force increases were not proportional to the abduction force increases.

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

0 1 2 3 4 5 6 7 8 9 10

SUBJECT

m 0

B

m l

0

0

0 1 2 3

SUBiEC? 6 7 8

FIG. 7. Individual and group left 5th digit flexion force changes after training. Open squares, pretraining test values. Filled squares, posttraining test values. A-C as in Fig. 3. D : mean and standard deviation of percent increases of the left 5th digit flexion force of each group. Although no group showed significant changes in flexion force, some subjects demonstrated 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


TABLE 2. Ratios of %increase inflexion force to that of . ahduct ion &force of’the left 5 th digit of individual subjects

Groups

Subjects Imagining” Contraction b Control’

I -2.48 d 6.74 2 0.16 0.33 3 2.06 -0.68 4 0.63 -0.28 5 4.62 0.08 6 0.23 1.39 7 0.6 1 1.27 8 3.68 3.16 9 5.80

10 4.13

- 1.49 E” 0.83 Of 1.68 2.05 1.83

-6.46

a 11 = 10. bag = 8. ‘n = 9. dA negative ratio indicates a decrease in the flexion force. “The abduction force increase was zero for this subject. fThe flexion force increase was zero for this subject.

used as the twitch force for each subject. No significant change was found in the twitch force after training in any of the three groups (P > 0.5, Table 1) . On average, the Imagin- ing group increased 1.04 t 14.94% (SD), the Contraction group decreased 2.48 t 11.3% (SD), and the Control group increased 2.9 1 t 10.69% (SD).

DISCUSSION

The maximal force increases in subjects who trained using effortful muscle contractions were similar to those who only imagined producing similar contractions during training. It is therefore possible that similar mechanisms were responsible for the strength gains in the two groups. If so, the increased strength that occurs early in a conventional training regimen, during the so-called “neural” phase, may not result from repetitive muscle activation. The possible origins of these strength increases may include programming/planning levels of a hierarchically organized motor system (Hasan et al. 1985; Brooks 1986). It is necessary first to consider alternative explanations to neural mechanisms that may underlie the observed strength increases.

When measuring maximal voluntary contractions, one must very carefully consider psychological or emotional factors that may yield apparent strength increases. It is unlikely that the strength gains in the present study resulted from psychological or emotional factors given the Control group’s lack of strength gain and the virtual absence of strength increases of the left great toe extensors in any group. Also, sham information provided to subjects con- cerning their performance during the pretraining strength test appeared to be highly motivating (see METHODS) and, hopefully, reduced the likelihood of increased effort for the posttraining measures.

Muscle hypertrophy also can significantly influence muscle strength after training. If the mass of a muscle is en- larged by increasing the cross-sectional area of each fiber, or the number of the fibers after training, a larger muscle strength output is expected from the increased number of parallel sarcomeres in the muscle (Edgerton et al. 1986). However, repeated production of high-intensity muscle activation is typically required for muscle hypertrophy (Atha

198 1; Goldberg et al. 1975; Goldspink and Howells 1974; MacDougall 1986). Also in some studies, muscle hypertrophy was not found even after 20 sessions of near maximal intensity strength training (Fukunaga 1976; Ikai and Fukunaga 1970). In the present study, surface EMG recorded in all subjects during the 4-wk period of imagined contraction training indicated that the trained muscle was virtually inactive during the training sessions (Fig. 4). This does not preclude the possibility that other active training may have occurred through daily living activities during the 4-wk training period despite our strict cautions against such activity. However, 1t seems training of this type co uld ind

highly uce mu

unlikely that casual scle hypertroph Y, Par-

ticularly after such a short period. The lack of change in evoked twitch tension in the pres-

ent experiment may also be used to argue against hypertrophy (Close 1972) and is consistent with previous studies that failed to induce evoked muscle tension increases even after 5 wk of high-intensity strength training (Davies and Young 1983; McDonagh et al. 1983). Nevertheless, it is unwise to infer that unchanged or decreased evoked twitch tensions reflect an absence of muscle hypertrophy. Studies of joint immobilization have reported inconsistent changes of twitch force, or ratios of twitch force to tetanic tension, of 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 twitch force after muscle atrophy may be due to immobilization-induced changes in muscle, including modifications of mechanical properties of a muscle fiber (Sale et al. 1982 ), or alterations from the sarcoplasm

in iC

speed or d uration of calcium release reticulum (Reiser et al. 1988).

Two possible neural mechanisms jtir strength increase

At least two mechanisms may have contributed to the increased force produced by both training groups. The hypothenar EMG increases indicate that the abduction force gain occurred from increased muscle activation (Hakkinen et al. 198 1,1985; Hakkinen and Komi 1983,1986; Komi et al. 1978; Moritani and de Vries 1979), most likely the abductor digiti minimi. Increased motoneuron activation has been acknowledged as an important source of strength increase during the first weeks of conventional strength training (Enoka 1988; Komi 1986; McDonagh and Davies 1984; Sale 1986). It also appears that some subjects devel- oped better strategies for activating the muscles crossing the metacarpophalangeal joint, as indicated by a disproportional increase in the finger’s flexion force as compared with the abduction force increase after training. Fl exion and abduction force changes should be yoked to each other (with the relationship determ ned by the ratio of the abductor m uscles’ moment arms n each direction) 9 provided that other muscles’ activation levels remain unchanged. Rutherford and Jones ( 1986) suggested that the increased capacity to lift weights with practiced lower leg extension movements was partial1 .y due to an increase in the skill of coordinating all muscle groups involved in the movement, including those used to stabilize the body. Improved muscle coordi nation at a joint with multi ple degrees of freedom should be considered as a potential mechanism in the early so-called neural phase of strength training.


The poor correlation between the increases in EMG and abduction force of the fifth digit may also be interpreted to indicate that some of the strength increase was due to activation of the fifth finger’s other muscles in a manner for more efficient metacarpophalangeal abduction torque production. However, such interpretations are hazardous because EMG often reflects an imperfect sampling of the neural activation of a muscle, and changes in isometric force and EMG level are not always simply related, particularly at high muscle activation levels (Howard and Enoka 199 1; for a review see Soderberg and Cook 1984). Also, it is unlikely that EMG recording during MVCs with surface electrodes on the hypothenar eminence reflect only the activity of the abductor digiti minimi. The difficulties in inter- preting EMG-force relationships in the present study are illustrated by the finding that the contralateral (untrained) hand strength increases in many subjects were not accompanied by EMG increases. A definitive demonstration of the role of learning more efficient muscle activation patterns for torque production requires separately recording the activity of each muscle that crosses the joint. For abduction of the fifth digit, one must record from the fourth palmar in- terosseous, a primary antagonist to abduction. The size and location of this muscle makes it difficult, although not im- possible to place indwelling electrodes.

Strength increases ftrom changes in the motor program

Because it was unlikely that the strength increases in the Imagining group were due to hypertrophy or psychological factors, the repeated imagined contractions must be considered as the factor initiating the increased motoneuron activation and improved coordination. It is reasonable to consider the nervous system levels that may have been involved in this process. At the lower levels of a hierarchically organized motor system, strength increases in general have been attributed to changes in the physiological properties of spinal motoneurons, interneurons and associated reflex pathways, and descending pathways (Hakkinen and Komi 1986; Komi et al. 1978; Milner-Brown et al. 1975; Sale et al. 1983a,b; Upton and Radford 1975) and/or the morphological properties of these neurons (Geinismann et al. 197 1; Gerchman et al. 1975; Gilliam et al. 1977; Kamen et al. 1984; Tomanek and Tipton 1967 ). The ultimate result of these changes is greater net motoneuron excitation on maximal effort contractions. However, muscle activity is expected to signal activation of these levels, and repeated exe- cutions of motor commands may be required before neural changes are induced at these lower levels of the motor system. Although powerful muscle contractions occurred during the MVC training, muscles were quiescent during the imagined training, making it unlikely that the neural changes responsible for the strength increases in the Imagin- ing group occurred at the motor system’s executional level. With this interpretation we assume that the Imagining group did not change the frequency, duration, or level of activation of the hypothenar muscles during the 4-wk training period. In support of this assumption, we have observed similar effects in experiments involving a 5-wk period of joint immobilization that yielded measureable muscle atrophy (Yue et al. 1991).

We suggest instead that the neural changes after the mental training occurred at programming or planning levels of the motor system, most likely involving nonprimary cerebral cortical motor areas. The altered “program” in turn may achieve strength gains via actions on spinal circuitry such as inhibition of Renshaw cells (Butler and Darling 1990), or other means of changing the excitatory and inhibi- tory influences on motoneurons. This interpretation is bol- stered by reports that neuronal activation, presumably associated with motor programming/ planning, can occur without activating muscle (Roland et al. 1980), and that mental training of motor skills (i.e., with quiescent muscles) can improve motor performance and skill acquisition (Corbin 1972; Fetz and Landers 1983; Hall 1985; Richard- son 1967). In these experiments it seems unlikely that descending pathways and spinal circuits were activated but inhibited at some point to prevent motoneuron activation. Given the similar strength increases in the Contraction and Imagining groups of the present experiment, it may be that short-term, high-intensity muscle contraction training pro- duces only adaptations of cortical programming/ planning areas.

One assumption necessary in suggesting that programming/planning changes underlie strength increases is that a maximal muscle contraction requires motor programming/planning. Although there is evidence that imagining a sequence of independent finger movements activates supplementary motor area neurons in humans (Roland et al. 1980), it is not known whether such activation occurs when performing a maximal contraction. However, Roland ( 1985) suggested that a maximal muscle contraction may require programming given the need for high effort levels. Roland and his colleagues ( 1980) reported evidence for low-level activation of the supplementary motor area during submaximal isometric contractions (Roland et al. 1980).

Strength increases Qf the contralateral (untrained) jinger

The finding of increased strength in the hand contralat- era1 to the trained hand is consistent with previous findings (cf. Enoka 1988; Sale 1986). The comparable levels of force increase in the contralateral untrained hand of the Imagining and Contraction groups prompts the speculation that changes in the motor program acquired via training of one hand may transfer to the contralateral hand. These training-induced changes may occur in areas that can influence both ipsi- and contralateral motor areas, such as the supplementary motor area. Brinkman ( 1984) observed that unilateral lesion of the supplementary motor area in monkeys produced a deficit in bimanual coordination. That is, the movements of both hands were similar even though successful task performance required very different movements of each hand. Section of the corpus callosum resulted in the disappearance of the synkinetic (“mir- rored”) movements and a return to independent action of the two hands. It was suggested that in normal monkeys, the supplementary motor area may provide information to the opposite hemisphere about the intended and/or ongo- ing movements (Brinkman 1984).


Strength increases in proximal versus distal muscles GOLDSPINK, G. AND HOWELLS, K. F. Work-induced hypertrophy in exercised 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

the loss of strength after periods of muscle disuse from joint and relaxation time, electromyographic and muscle fiber characteristics

immobilization, peripheral nerve injuries, and the like. of human skeletal muscle during training and detraining. Acta Physiol. 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.

may be relatively unused in the skills of daily living. Similar HAKKINEN, K. AND KOMI, P. V. Training induced changes in neuromuscu-

results must be demonstrated for proximal and often-used lar performance under voluntary and reflex conditions. Eur. J. AppZ. 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. Luschei for valuable comments on the manuscript and James A. Hadar for clerical and editorial assistance.

This research was supported by Grants YA l-9005- 1 from American Paralysis Association, 2408-95 from The University of Iowa Collegiate Association Council, and a grant in aid of research from Sigma Xi, The Scientific Research Society.

Address for reprint requests: K. J. Cole, Dept. of Exercise Science, The University of Iowa, Iowa City, IA 52242.

Received 20 May 199 1; accepted in final form 20 December 199 1.

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1992 Journal of Neurophysiology