Journal of Sport Rehabilitation, 2011.

20, 471-486
2011 Human Kinetics, Inc.

Rotator-Cuff Muscle-Recruitment
Strategies During Shoulder
Rehabilitation Exercises
Kathleen A. Swanik, Kellie Huxel Bliven,
and Charles Buz Swanik
Context: There are contradictory data on optimal muscle-activation strategies
for restoring shoulder stability. Further investigation of neuromuscular-control
strategies for glenohumeral-joint stability will guide clinicians in decisions
regarding appropriate rehabilitation exercises. Objectives: To determine whether
subscapularis, infraspinatus. and teres minor (anteroposterior force couple) muscle
activation differ between 4 shoulder exercises and describe coactivation ratios and
individual muscle-recruitment characteristics of rotator-cuff muscles throughout
each shoulder exercise. Design: Crossover. Setting: Laboratory. Participants:
healthy, physically active men, age 20.55 2.0 y. Interventions: 4 rehabilitation
exercises: pitchback, PNF D2 pattern with tubing, push-up plus, and slide board.
Main Outcomes Measures: Mean coactivation level, coactivation-ratio patterns,
and level (area) of muscle-activation patterns of the subscapularis, infraspinatus,
and teres minor throughout each exercise. Results: Coactivation levels varied
throughout each exercise. Subscapularis activity was consistently higher than that
of the infraspinatus and teres minor combined at the start of each exercise and in
end ranges of motion. Individual muscle-recruitment levels in the subscapularis
were also different between exercises. Conclusion: Results provide descriptive
data for determining normative coactivation-ratio values for muscle recruitment
for the functional exercises studied. Differences in subscapularis activation suggest
a reliance to resist anteriorly directed forces.
Keywords: force couple, EMG, therapeutic exercise, joint stability
Coactivation is the simultaneous contraction of muscles (ie, onset, duration,
and amount of activation) around a joint that establishes force couples to increase
compressive forces and optimize congruency between articulating surfaces,
which is important for stability.'^ The concept of force couples was introduced
by Sherrington' and studied at the shoulder by Inman et aP as it relates, directly

K. Swanik is with the Athletic Training Program. Neumann University, Aston. PA. Huxel Bliven is
with Interdisciplinary Health Sciences. A.T. Still University. Mesa, AZ. C. Swanik is with the Dept of
Kitiesiology and Applied Physiology, University of Delaware. Newark. DE.

471

472

Swanik, Huxel Bliven, and Swanik

and indirectly, to joint stability. One method to quantify the relationship between
force-couple mu.scles is to calculate coactivation ratios. An important force couple
for anteroposterior shoulder stability is the subscapularis opposed by the infraspinatus and teres minor. Cadaveric models suggest that muscle-coactivation ratios of
this force couple should vary with joint movement depending on the mechanical
advantage of each muscle.''-'' However, in vivo data quantifying changes throughout
a range of motion have not been reported for rehabilitation exercises. Consideration
ofthe.se variables may influence clinical decisions regarding the selection of specific
rehabilitation exercises and safe ranges of motion for individual patient needs.
Cadaveric research'*'"'' and in vivo studies'*^ suggest a theoretical paradigm
whereby simultaneous contraction of the force couple created between the subscapularis, infraspinatus, and teres minor is imperative for glenohumeral-joint
stability.^-'"-' ' Although several studies have investigated activation levels (ie, peak,
mean) of these muscles independently in the shoulder during rehabilitative and
throwing exercises,^-"""" there are no data on the level of coactivation, as quantified by the ratio between muscles in a force couple, particularly how these values
change to accommodate the range of motion and loads incurred while executing
specific tasks. Because the muscles that compose this force couple have differing
architecture and continuously changing moment arms and length-tension relationships," it may be a misleading oversimplification to suggest that certain exercises
promote stability through coactivation for every patient, without fully understanding
the changes that may occur as the extremity moves though the exercise's range of
motion. Furthermore, it could be argued that balanced coactivation ratios would
impair coordinated shoulder motion " during rehabilitation exercises and that selective recruitment of specific muscles, causing an imbalanced ratio, may be more
efficient for offsetting potentially deleterious joint loads. Most studies agree that
some coactivation is necessary to minimize shearing stresses and excessive motion
that could otherwise contribute to the early onset of osteoarthritis,'*-" overuse
injuries,''*'"'^' labral tears,'''^^ or instability. ^-^"^'' Others have implied that increased
coactivation ratios (ie, duration and quantity) may in fact be a precursor to knee
osteoarthritis.-' However, unbalanced coactivation ratios may also heighten joint
stiffness and limit motion at the shoulder, thus enhancing joint stability.-* Equal
coactivation ratios may only be necessary in positions of vulnerability-'*'^'-^** or
during the early motor-learning stages of new-skill acquisition,^'-'"' which raises
the question of what level of muscle coactivation occurs during the performance
of rehabilitation exercises with varying degrees of difficulty.^^-""-^^
Traditionally, closed-chain activities (exercises with a fixed ba.se) have been
identified as providing dynamic stability through muscle coactivation.-^-^-^^ However,
these exercises do not replicate most activities required of the upper extremity.
Activities of daily living, as well as most sport-specific requirements associated
with the shoulder, are open chain (distal segment not fixed). Finally, neuromuscular characteristics vary among different populations and therefore should also be
taken into consideration when integrating these tasks into individual rehabilitation programs for a safe and successful recovery. For this reason, clinicians have
relied on theoretical models for shoulder rehabilitation progression with regard to
coactivation relationships. Exercises to promote dynamic stability via force-couple
coactivation that are frequently used in clinical rehabilitation include pitchback
with a Plyoball, abduction/adduction motions on a slide board with the subject in

Glenohumeral Muscle Activation and Coactivation

473

a push-up position, push-up plus, and the proprioceptive neuromuscular facilitation

diagonal 2 (PNE D2) pattern.
This study aims to provide information about the role of shoulder-muscle
coactivation so clinicians have evidence of muscle recruitment in healthy individuals while they perform rehabilitation exercises, therefore promoting their use
in individualized programs. Specifically, our aims were to address the following
questions: Are mean rotator-cuff muscle-coactivation ratios different between the 4
shoulder exercises examined in this study? What is the role of coactivation levels,
as quantified by ratios, throughout the entire motion (ie, pattern) of a rehabilitation
exercise? If rotator-cuff muscle coactivation is not predominant, what muscles are
selectively recruited during each exercise?

Methods
A crossover design was used in this study. Electromyographic (EMG) signals were
recorded from the infraspinatus, teres minor, and subscapularis during the execution
of 4 shoulder rehabilitation exercises.
Thirty-three healthy, physically active men (age 20.55 2.0 y, height 176.34
4.6 cm, weight 77.31 12.5 kg) participated in this study. We tested the dominant
arm (right, n = 26; left, n = 7), defined as the arm used to throw a ball. Subjects
with a history of surgery, episodes of shoulder instability in the past year, or injury
within the past 6 months that caused suspension of physical activity were excluded.
In addition, all subjects underwent an upper extremity screen by an orthopedic
surgeon to rule out pathology and instability of the shoulder by assessing range of
motion, strength, glenohumeral laxity, rotator-cuff impingement, and neurologic
status. All subjects signed an informed consent approved by the university's institutional review board before testing.
We simultaneously recorded EMG activity from the infraspinatus, teres minor,
and subscapularis muscles during the following shoulder rehabilitation exercises:
pitchback with Plyoball, PNF D2 pattern, push-up plus, and slide board (Figure
IA-D). The ground electrode, a self-adhesive Ag/AgCl bipolar surface electrode
(272, Noraxon USA Inc, Scottsdale, AZ), was applied to the skin over the ipsilateral
clavicle according to standard skin-preparation and placement procedures." We
placed intramuscular fine-wire bipolar electrodes into the muscles under sterile
conditions using the single-needle technique described by Basmajian and DeLuca."
Dual 50.8-|j,m diameter Stablohm 800A stainless-steel wires insulated with heavy
polynylon (California Fine Wire Co, Grover, CA) were inserted following standard
procedures,'**'^" and placement was confirmed by monitoring EMG activity during
manual muscle testing using an oscilloscope (MyoResearch software; Noraxon
USA Inc)."' Bipolar electrodes were connected to spring cables on a Noraxon
Telemyo (Noraxon USA Inc) frequency-modulated electromyograph transmitter.''^
The .sampling rate was 2500 Hz, based on recommendations of the International Society of Electrophysiology and Kinesiology and previously established
guidelines.^' All raw data were preamplified (total gain 2000, common-mode
rejection ratio of 130 dB and filtered to produce a bandwidth of 10-2000 Hz). Raw
signals were converted from analog to digital using a 12-bit analog-to-digital card
(Keithley Metrabyte DAS-1000, Keithley Instruments, Inc, Tauton, MA). Data

1A

1B

IC

10

0%
Movement Cycle
Figure 1 Each of the 4 rehabilitation exercises studied is represented. The start, middle,
and end positions of the exercise are pictured and correspond with the depicted coactivation
patterns. A; During the pitchback exercise, the subject threw a weighted ball into an inclined
trampoline and the ball rebounded back to the subject. Beyond 20% of the movement,
coactivation values decreased. B; The PNF D2 movement was performed in the extension/
flexion direction using elastic tubing as resistance. Coactivation values increased at the
end range of motion. C; From a kneeling position, the subject performed a push-up-plus
exercise. Coactivation values increased during the "plus" portion of the exercise, when the
body was pushed up farther (using scapular protraction). D; From a kneeling position, the
subject perlbrmed the slide-board exercisehorizontal abduction/adduction on a plastic
sliding surface. Coactivation increased at the end range of horizontal abduction, when the
exercise was more difficult.
474

Glenohumeral Muscle Activation and Coactivation

475

were then full-wave rectified with a sixth-order Butterworth filter and smoothed
over a 15-millisecond moving window using MyoRe.search software (version 2.11,
Noraxon USA Inc). The amplitude of muscle activity was normalized using the
maximal voluntary contraction for each muscle elicited during standardized manual
muscle tests.'*' Normalized muscle-activity area was calculated as the sum of the
amplitudes of integrated EMG activity over the total time of the trial. The timenormalized EMG area of each muscle was used to calculate coactivation ratios and
to analyze individual muscle activity. Mean coactivation ratio was calculated using
the EMG-area values of muscles in the anteroposterior force couple, such that the
subscapularis was divided by the sum of the infraspinatus plus teres minor.^^ EMG
area was time-normalized into 100 data points to analyze mean coactivation-ratio
recruitment patterns that represented the entire range of motion for the exercise.
Every 10 data points were averaged to represent 10% of the total exercises (100/10
= 10). Each 10% increment of the motion was compared between exercises.
Muscle-activity data were collected during 4 shoulder rehabilitation exercises.
Each exercise was first described and demonstrated to the subject, followed by the
subject's performance of at least 3 practice trials. Verbal feedback was provided to
ensure proper form during the maneuvers. Data were collected during 10 exercise
repetitions with a 15-second rest between repetitions and a 3-minute rest between
exercises. Exercise order for each subject was determined using a Latin-square table.
The pitchback was executed from a kneeling position with the test arm in 90
shoulder abduction and 90 elbow flexion (Figure 1 A). The subject was instructed
to throw a 1-kg weighted Plyoball toward a 45 to 60 inclined trampoline, positioned 2 m away, and catch the ball as it rebounded. Subjects were encouraged to
throw the ball as hard as possible, catch it, and return to the start position before
the next repetition. Each repetition was performed in approximately 1.5 seconds.
The diagonal movement pattern of shoulder abduction/flexion was followed
for the PNF D2 pattern (Figure lB).'*^ Subjects assumed a kneeling position and
started with the dominant-arm hand in front of the opposite hip. They were instructed
to flex and horizontally abduct the shoulder 180 and 140, respectively, until the
arm was overhead. Elastic tubing (moderate tension) was secured by the subject's
contralateral knee and used as resistance during the movement pattern. The amount
of resistance was set according to manufacturer guidelines so the subject could
perform no more than 15 repetitions.'*^ Each repetition was performed in approximately 4 seconds.
The push-up plus started with the subject in a prone position with hands
shoulder width apart and chest on the floor (Figure lC). Subjects were instructed
to perform a traditional push-up supporting body weight on their hands and feet
(toes). The "plus" component of the exercise required actively and maximally
protracting the .scapulae at the top of the push-up before moving back down to the
floor. Each repetition was performed in approximately 3 seconds.
Horizontal shoulder abduction/adduction was performed on a slide board
(Exertools, Novato, CA; Figure ID). Subjects started in a push-up position with
their elbows extended and body weight distributed on their hands and knees. They
initiated horizontal shoulder abduction while maintaining elbow, trunk, and hip
extension. Subjects were encouraged to horizontally abduct as far as possible while
maintaining elbow extension. When the end range of horizontal abduction was
reached (self-determined based on elbow-extension criteria), the subject returned

476

Swanik, Huxel Bliven, and Swanik

to the start position of horizontal adduction. Subjects wore cotton coverings on

their hands to decrease friction. Each repetition was performed in approximately
3 seconds.
Descriptive and inferential statistics were calculated using EMG data. Differences in mean coactivation ratio between the 4 shoulder rehabilitation exercises
were determined by a 1 -way analysis of variance. Analyses of muscle-coactivation
levels during a movement pattern were based on previously published procedures'-'**
in which the entire exercise was divided into 10% increments. This allowed differences in mean coactivation ratio of each period between the 4 shoulder rehabilitation
exercises to be determined using nonparametric Wilcoxon rank-sum tests. Differences in EMG area under the curve for the subscapularis between the 4 shoulder
rehabilitation exercises were determined using a 1-way analysis of variance. The
same analysis was performed for the EMG area under the curve for the infraspinatus
and teres minor. Tukey's honestly significant difference with Bonferroni correction
(P = ,0\25) was used for post hoc analyses when significant differences were found.
All data were analyzed using the Statistical Package for Social Sciences (version
12.0, SPSS Inc, Chicago, IL) for Microsoft Windows. The a level was set at P <
.05 a priori for statistical significance.

Results
Mean coactivation ratios ranged from 47% to 60% (Figure 2) for the 4 rehabilitation
exercises examined. There were no differences (P > .05) in the mean coactivation
ratios among the 4 exercises completed in this study.
There were statistically significant differences (P < .05) in each 10% increment
of mean coactivation-recruitment patterns between the 4 shoulder rehabilitation
exercises studied (Figure lA-D). In general, the most prominent differences of
higher coactivation ratios (eg, subscapularis activation more than infraspinatus and
teres minor) for an exercise corresponded with exercise initiation (-0-20% of the
1

0.9
0.8
2 0.6
o 0.5

0.2
0.1
0
Pitchback

PNF D2

Push Up +

Slideboard

Figure 2 Mean coactivation between the 4 rehabilitation exercises.

Glenohumeral Muscle Activation and Coactivation

477

exerci.se) and when the glenohumeral joint was in a position of vulnerability at end
ranges of motion (flexion, abduction, and/or external rotation).
Analysis of each muscle individually revealed statistically significant differences (P < .05) in subscapularis activation but not infraspinatus or teres minor
between the 4 shoulder rehabilitation exercises (Figure 3). Subscapularis-muscle
activity was significantly greater during the push-up-plus exerci.se (88.8%
77.5%/s) than in the pitchback (48.4% 40.5%/s) and PNF D2 (44.4% 39.9%/s)
exercises (Figure 3).

Discussion

This study was conducted to determine whether coactivation levels, as measured

by a ratio, between the subscapularis, infraspinatus, and teres minor necessary
for anteroposterior stabilization of the glenohumeral joint'-'* differ between 4
clinically used shoulder rehabilitation exercises. "'''^^'* In addition, we determined
whether coactivation levels change throughout an exercise's range of motion (eg,
movement pattern) and whether the activation of individual muscle-recruitment
levels differs between the 4 exercises. In addition to variability between exercises,
there were large differences in muscle recruitment between subjects, suggesting
individualized responses to exercises and the need to base decisions on exercises
in a rehabilitation program on individualized patient needs. The results of this
study are 3-fold. EMG data revealed that mean coactivation-ratio patterns differ
between the rehabilitation exercises studied. Patterns demonstrate how coactivation
ratios vary, or fluctuate, within the execution of each exercise (Figure 1). Finally,
imbalanced coactivation ratios may reflect a greater reliance on individual muscle
recruitment, specifically the subscapularis, or activation of muscles not analyzed.
250

Pitchback DpNFDI a Push Up-^ QSIideboard

Figure 3 Individual activation of each muscle for the 4 rehabilitation exercises.

478

Swanik, Huxel Bliven, and Swanik

during these exercises. These may be strategies used at the start of exercise to initiate movement and in end-range positions that are vulnerable to offset shear forces
and maintain joint stability.'^'o
We examined the role of the glenohumeral force couple created between the
subscapularis, infraspinatus, and teres minor."^-- The synergism between these
muscles, particularly during humeral flexion and abduction,----'^'*^ maintains joint
stability through humeral-head centering and compression while resisting the superior shear force and anteroposterior translations.''''^^" Previous studies report that
muscle coactivation is greater in weight bearing (ie, coactivation ratio balanced and
closer to 1:1), which advocates shoulder rehabilitation exercises such the push-up
plus to enhance joint stability.'-'* *^''* Our results show that mean coactivation ratios
are comparable between the 4 rehabilitation exercises studied regardless of whether
they have a weight-bearing component. There appears to be substantial variation
between subjects, so decisions to include a rehabilitation exercise should be based
on desired improvements in function for individualized patient needs. For example,
our results indicate that initiation of movements and/or positions of vulnerability
are factors with greater influence on coactivation-ratio levels. However, to fully
appreciate muscle activation in response to functional demands, coactivation ratios
should be quantified throughout the rehabilitation exercise instead of relying on
a single value that may be misleading or more appropriate for isolated positions.
To our knowledge, this is the first study to examine these muscles simultaneously throughout the range of motion used to perform rehabilitation exercises and
report a pattern of coactivation ratios. Our data revealed that the coactivation ratio
varied greatly over the duration of each task and that the pattern of coactivation
ratios was different between exercises (Figure 1 ). It was further observed that
regardless of level of resistance, or complexity, coactivation ratios are imbalanced
and considerably greater, meaning subscapularis activity was more than that of
the infraspinatus and teres minor combined, during the initial of movement for
each exercise and in the middle of the exercise when the arm is in a vulnerable,
or end-range, position. This may suggest that coactivation assists with stability by
"setting" or positioning the humeral head before executing the movement.** -" The
quantitative and qualitative (Figures 4-7) differences observed in tbe coactivationratio patterns, both within and between tasks, may better reflect the demands placed
on this force couple during rehabilitation exercises and can be used for clinical
decisions regarding exercise selection and the apparent muscle effort needed during
specific ranges of motion as they relate to individual patient deficits. However, to
appreciate the variation in coactivation ratios through the exercise's range of motion
(measured in 10% increments) and resistance during the rehabilitation exercises
studied, one must also consider the recruitment of individual muscles that compose
this force couple.
Theoretically, if excessive shearing forces are imparted on the joint in the course
of rehabilitation exercises, selective muscle recruitment (asynchronous firing) may
occur to offset these joint loads in an attempt to maintain joint congruency.^"* '" This
was observed in association witb higher-velocity exercises or during multiplanar
tasks. For example, the pitchback (Eigure 1 A) closely resembles overhead throwing. Coactivation peaked at the beginning of the exercise (0-20% of the exercise's
range of motion), when anteriorly directed shear forces are high,''* and were
reduced during the other 10% increments of throwing. These coactivation-ratio

Pitchback
Subscapularis

Teres Minor
60

SO
40

"5.
c
o

30
20

10
0%

50%

100%

Movement Cycle

Figure 4 Activation of each muscle in the anteroposterior force couple during the
pitchback. The start, middle, and end position of the exercise are pictured and correspond
with the amplitude of muscle-activation pattern depicted.
479

PNFD2
Subscapularis

Infraspinatus
60
50
40

a.
E

30
20

<

10

Teres Minor

60
50
40

5.
B

30

I ^
~

10

0%

50%

100%

Movement Cycle
Figure 5 Activation of each muscle in the anteroposterior force couple during the PNF
D2. The start, middle, and end position of the exercise are pictured and correspond with the
amplitude of muscle-activation pattern depicted.
480

Push Up +
Subscapularis
60
50
40

o.
E 30
20

7
7

5 10

Infraspinatus

E
c

Teres Minor
60
50
40

o.

30
20

10

0%

50%

100%

Movement Cycle

Figure 6 Activation of each muscle in the anteroposterior force couple during the pushup plus. The start, middle, and end position ofthe exercise are pictured and correspond with
the amplitude of muscle-activation pattern depicted.
481

Slideboard
Subscapularis
60
a

50
40

<

30
20
10
0

Infraspinatus
60
50
40
E
<

30

10
0

Teres Minor

'S.

50%

100%

MovementCyde

Figure 7 Activation of each muscle in the anteroposterior force couple during the
slide-board exercise. The start, middle, and end position of the exercise are pictured and
correspond with the amplitude of muscle-activation pattern depicted.
482

Glenohumeral Muscle Activation and Coactivation

483

values suggest greater reliance on selective recruitment from the subscapularis as

an anterior check rein during maximal external rotation, which shifts to reliance
on the infraspinatus and teres minor during deceleration when these muscles are
eccentrically loaded. It is during these pha.ses of pitching that there is the highest
likelihood of injury.'^^''' Clinically, focusing on maximal external rotation to enhance
or elicit coactivation and selective activation during the deceleration portion of the
exercise may be appropriate and can be acbieved using eccentric training of the
infraspinatus and teres minor to prevent injury and promote stabilization.'"
When we examined individual muscle recruitment, the subscapularis was the
only muscle that had significant activation differences between the rehabilitation
exercises (Figure 3). Subscapularis-muscle activity was comparable between the
push-up-plus and slide-board exercises, although only the push-up plus was statistically significantly differentboth considerably greaterthan its activation
during the pitchback and PNF D2 exercises. Therefore, our results may be used to
verify the integration of the push-up-type positions (both push-up plus and slide
board) into rehabilitation programs to target the subscapularis. Tbe push-up plus
has also been advocated to recruit the scapular stabilizers.''''.SO Qur results show
that muscle recruitment increases at the start of the exercise's movement or when
the arm is at its end range during the exercise. Therefore, clinicians should carefully consider exercise selection in designing programs. Changes in joint angle and
resistance through the exercise's range of motion affect each muscle's activation
(EMG) response. These data can be used to maximize the most effective strategies to limit humeral-head translation and protect the glenohumeral joint through
dynamic stabilization.''''''^^'''*-^''-"'^''
There are limitations to our study. First, healthy men 18 to 25 years of age
were tested to answer our research questions; results provide normative data for
clinicians but do not reveal how muscles activate in patients with shoulder injury.
Second, other dynamic stabilizers of the shoulder such as the deltoid, supraspinatus,
pectoralis minor and major, biceps brachii, latissimus dorsi, and serratus anterior
that were not examined should be considered. Their roles in stability are well
established in the literature and may warrant use of these rehabilitation exercises
lor their synergistic activity and contributions to joint stability. Third, we evaluated the subscapularis-muscle activity from a single site. Some researchers suggest
differentiating the upper from lower subscapularis fibers as a result of separate
innervations.'" *^' We agree that this is important; however, we sought to emphasize
how these muscles function simultaneously as a group, regardless of innervation,
during dynamic movements. Finally, care must be taken when drawing inferences
from EMG data regarding joint loads or tension because muscle architecture and
length-tension changes may influence these
l*"2^s2

Conclusion
Overall, these data provide normative values on what may be considered "optimal"
muscle-recruitment strategies in healthy men specific to these rehabilitation exercises. Mean coactivation levels were high for all the exercises, but further analysis
throughout the motion cycle revealed greater variation with the highest levels at the
initiation of movement or in positions in which resistance was high. These data also
highlight the potential role for selective recruitment when high coactivation ratios

484

Swanik, Huxel Bliven, and Swanik

suggest higher reliance on the subscapularis to maintain glenohumeral stability,

particularly in positions that stress anterior joint stability. These findings may be
used to compare with pathologic populations to gain further insight to appropriate
and eiective rehabilitation for restoring dynamic stability.
Acknowledgments
Each author certifies that he or she has no financial affiliation (including research funding)
or involvement with any commercial associations (eg, consultancies, stock ownership, equity
interest, patent/licensing arrangements) that has a direct financial interest that might pose a
conflict of interest in connection with the submitted manuscript.

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