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Corticomotor excitability of gluteus maximus: influence on hip extensor strength and hip mechanics

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Corticomotor excitability of gluteus maximus: influence on hip extensor strength and hip mechanics

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Content CORTICOMOTOR EXCITABILITY OF GLUTEUS MAXIMUS:
INFLUENCE ON HIP EXTENSOR STRENGTH AND HIP MECHANICS
By
Yo Shih
A Dissertation Presented to the
FACULTY OF THE USC GRADUATE SCHOOL
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
DOCTOR OF PHILOSOPHY
(BIOKINESIOLOGY)
December 2019
ii

DEDICATION

This dissertation is dedicated to my family

My parents and grandparents for their full support of pursuing my dream
My brother, Lee Stone, who always backs me up whenever I need him
My husband, Kit Leong, who decided to join me on this adventure

iii

ACKOWLEDGEMENTS
Six years is not a short time, enough for a newborn to grow into a “grade-schooler”. I
exponentially grew during my time at the USC Division of Biokinesiology and Physical
Therapy. It was initially intimidating to me to navigate myself in this big division, however later
on, I found it a blessing to have the chance to know and interact with so many brilliant,
enthusiastic and creative human beings.
Completing a PhD dissertation is a challenging task and I would not have finished it
without the guidance and support from a number of people. I would like to thank my advisor, Dr.
Christopher Powers for setting a high standard during the process. His ability of always making
strong arguments helped me to clarify the boundary of my work and enabled me to strengthen
my communication skills. His impact upon the physical therapy and biomechanics research
fields is a life-long mission I aspire to follow. I am very thankful for the guidance from Dr. Beth
Fisher who always boosted my confidence and I learned so much from her during our long hours
spent together in the writing process. I enjoyed the brain-storming with Dr. Jason Kutch in order
to explain unexpected data. I also learned from him the three elements for a motivated lab:
coffee, snacks, and a bottle of champagne for every publication. I appreciate Dr. George Salem
for asking questions that pushed me to think how my study can be applied to real-life problems. I
am extremely grateful for having Dr. Jo Smith on my committee. Her experiences in conducting
research across biomechanics and TMS labs were inspiration for my research direction. She
always understood my struggles for balancing my dissertation between the two different
approaches of human movement and I enjoyed our open-minded discussions very much.
In addition to my committee members, I received valuable feedback and inputs related to
this dissertation from division seminars and MBRL meetings. I would like to thank Drs. Susan
iv

Sigward and Lori Michener for their comments during MBRL meetings. I would especially like
to thank Dr. Kornelia Kulig for constantly checking-in with me at my spot in the basement and
always welcoming mind-mapping discussions, encouraging me to think about my research
within a broader scope of science.
I am forever grateful for having the intelligent discussions about science with former and
present MBRL, NAIL and AMPL lab members, Eugene, Matt, Jennifer, Abbi, Andrea, Michael,
Jasmine, Jia, Jonathan, Jordan, Steffi, Nicole, Sara, David, Alex, Andrew, Rini, and Amy. They
are always willing to provide feedback to me about my writings and presentations. I especially
would like to thank Yu-Chen, Irene, and Moheb. They were my go-to persons whenever I was
stuck in my own thinking process. Beyond science, I am extremely grateful to build up life-long
friendships with colleagues in the labs in which we shared lots of ups and downs of work and life
together. I would not have survived without the strong mental support from them. I would also
like to thank Drs. Seol Park and Roberta Brunelli for their assistance in data collection.
I would like to thank the division for the financial support and the teaching opportunities.
I am grateful to have had my teaching experience start with groups of smart, dedicated DPT
students who ignited my passion to teach. More importantly, the friendships with them that
extends to outside of the classroom have also made life in the basement much enjoyable. I would
also like to thank Drs. Larry and Sally Ho for seeing Kit and I as their family. They always make
sure we feel like home here, especially during holidays.
The support of family, friends, previous teachers and mentors from Taiwan has been
exceptional for me to keep going in this journey. I am always fully recharged physically (with
delicious foods) and mentally (with cheers) every time I have a chance to go back for a visit.
They always remind me of the reasons I made this decision to pursue my PhD. I would
v

especially like to thank Dr. Tzyy-Yuang Shiang for introducing me to this research field and
always willing to provide help to benefit me in my career.
I will never be able to thank Kit enough for his company. It is a luxury to have a
significant other taking care of my life and being the best cheerleader along this journey. I would
also like to tell myself, the one from six years ago: “You made a brave decision and I am so
proud of you.”

vi

TABLE OF CONTENTS
DEDICATION ................................................................................................................................ II
ACKOWLEDGEMENTS ............................................................................................................. III
LIST OF TABLES ....................................................................................................................... VII
LIST OF FIGURES ................................................................................................................... VIII
ABSTRACT .................................................................................................................................. IX
CHAPTER I: OVERVIEW............................................................................................................. 1
CHAPTER II: BACKGROUND AND SIGNIFICANCE .............................................................. 4
CHAPTER III: RELIABILITY OF A METHOD TO ASSESS CORTICOMOTOR
EXCITABILITY OF PROXIMAL LOWER EXTREMITY MUSCLES USING A
NORMALIZED EMG MOTOR THRESHOLDING PROCEDURE .......................................... 13
CHAPTER IV: INFLUENCE OF CORTICOMOTOR EXCITABILITY OF GLUTEUS
MAXIMUS ON HIP EXTENSOR STRENGTH: A SEX COMPARISON ................................ 25
CHAPTER V: CORTICOMOTOR EXCITABILITY OF GLUTEUS MAXIMUS IS
ASSOCIATED WITH SAGITTAL PLANE HIP KINEMATICS AND KINETICS DURING A
SINGLE LEG DROP JUMP TASK ............................................................................................. 38
CHAPTER VI: SUMMARY AND CONCLUSIONS .................................................................. 51
REFERENCES ............................................................................................................................. 57

vii

LIST OF TABLES
TABLE 3-1. RELIABILITY RESULTS FOR THE TMS MEASURES OF INTEREST FOR
GLUTEUS MAXIMUS ......................................................................................................... 20
TABLE 3-2. RELIABILITY RESULTS FOR THE TMS MEASURES OF INTEREST FOR
VASTUS LATERALIS ......................................................................................................... 21
TABLE 4-1. PARTICIPANT DEMOGRAPHICS (MEAN ± STANDARD DEVIATION) ........ 28
TABLE 5-1. PARTICIPANT DEMOGRAPHICS (MEAN ± STANDARD DEVIATION) ........ 41

viii

LIST OF FIGURES
FIGURE 4-1. REPRESENTATIVE IOC RESULTS FOR A FEMALE (LEFT) AND MALE
(RIGHT) PARTICIPANT. THE SPACED CIRCLES REPRESENT THE AVERAGE OF
THE 10 MEP AMPLITUDES. THE SOLID LINES REPRESENT THE REGRESSION
LINE OF MEPS FROM THE 100% AMT TO THE MAXIMUM MEP ............................... 31
FIGURE 4-2. COMPARISON OF PEAK HIP EXTENSOR TORQUE BETWEEN SEXES ...... 33
FIGURE 4-3. COMPARISON OF CORTICOMOTOR EXCITABILITY OF GLUTEUS
MAXIMUS BETWEEN SEXES ........................................................................................... 33
FIGURE 4-4. SCATTERPLOT SHOWING THE RELATIONSHIP OF THE GM IOC SLOPE
AND THE PEAK HIP EXTENSOR TORQUE FOR ALL PARTICIPANTS ....................... 34
FIGURE 5-1. SCATTERPLOTS OF THE GM IOC SLOPE AND THE HIP EXTENSOR
MOMENT ............................................................................................................................. 46
FIGURE 5-2. SCATTERPLOTS OF THE GM IOC SLOPE AND THE PEAK HIP ANGLE ..... 46
FIGURE 6-1. SUMMARY OF THE MAIN RESULTS ............................................................... 52

ix

ABSTRACT

Insufficient use of the hip extensors during sport related activities is thought to be
contributory to various knee injuries.
1,2
Diminished hip extensor strength has been reported to
underlie the movement behavior that exposes the knee to excessive loading.
1,3
In particular,
diminished force production of the gluteus maximus (GM) is thought to be problematic as this
muscle protects against excessive loading of the knee owing to its multi-planar control of the
hip.
2,4,5
It has been proposed that centrally mediated neural factors (i.e. diminished neural drive)
may be contributory to the diminished strength and movement behavior that underlies knee injury.
6

To date, the corticomotor excitability (CME) of specific lower extremity muscles within the
context of lower extremity strength and movement behavior has not been investigated. Given the
potential role of GM with respect to movement behavior associated with knee injury, the purpose
of this dissertation was to evaluate the extent to which CME of GM, as quantified using
transcranial magnetic stimulation (TMS), is predictive of hip extensor strength, and functional use
of the hip extensors during a sport specific task. To achieve this objective 3 studies were
undertaken.
Because of the methodological challenges associated with the assessment of proximal
lower extremity muscles using TMS, the purpose of Chapter III was to establish the reliability of
a method for measuring corticomotor excitability of gluteus maximus and vastus lateralis (VL)
using a normalized electromyography value as the criterion for identifying motor evoked potentials
(MEPs) during the motor thresholding procedure (as opposed to a fixed voltage value). Ten healthy
participants were recruited. TMS data were acquired using the input-output curve (IOC) procedure
while participants performed an isometric contraction of GM and VL (20% of maximal voluntary
isometric contraction). The active motor threshold for each muscle was determined using the
x

lowest stimulator intensity required to elicit 5 MEPs from 10 stimulations that exceeded 20%
MVIC. The average and peak slopes of the IOC data points were analyzed using linear regression
and sigmoid curve fitting respectively. TMS data were obtained on 2 separate days and compared
using random-effect intra-class correlation coefficients (ICCs). Slopes from both IOC fitting
methods as well as the maximum MEP of GM and VL were found to exhibit good to excellent
reliability (ICCs ranging from 0.75-0.99).
The purpose of Chapter IV was to compare hip extensor strength and CME of GM between
males and females. A secondary purpose was to determine if CME of GM is associated with hip
extensor strength. Thirty-two healthy individuals participated (15 males and 17 females). CME of
GM was assessed using the IOC procedure acquired from transcranial magnetic stimulation
(average slope). Hip extensor strength was measured using a dynamometer during a maximal
voluntary isometric contraction. One-tailed t-tests were used to compare CME of GM and peak
hip extensor torque between males and females. Linear regression analysis was used to determine
whether peak hip extensor torque was predicted by GM CME. When compared to males, females
demonstrate lower peak hip extensor torque (4.42 ± 1.11 vs. 6.15 ± 1.72 Nm/kg/m
2
, p<0.01) and
lower CME of GM (1.36 ± 1.07 vs. 2.67 ± 1.30, p<0.01). CME of GM was a significant predictor
of peak hip extensor torque for both males and females combined (r
2
=0.36, p<0.001).
The purpose of Chapter V was to determine the association between CME of the GM and
the kinetics and kinematics of the hip joint during single limb drop jump. Thirty-two healthy
individuals (17 females, 15 males) participated. The slope of the IOC obtained from TMS was
used to assess CME of GM. The average hip extensor moment and peak hip flexion angle during
the stance phase of the single leg drop jump task was calculated. Linear regression analysis was
used to determine whether the average hip extensor moment and peak hip flexion were predicted
xi

by CME of GM. Results revealed that the slope of the IOC of GM was a significant predictor of
the average hip extensor moment (r
2
=0.18, p=0.016) and peak hip flexion (r
2
=0.20, p=0.01).
As part of this dissertation, a reliable method to measure CME of GM was established.
Based on this method, findings of this dissertation revealed that CME of GM was predictive of
both hip extensor strength and functional use of the hip extensors during a sport-specific task.
Taken together, findings of this dissertation suggest that hip extensor strength and functional use
of the hip extensors may be due, in part, to descending neural drive of GM. Interventions aimed at
enhancing CME of GM may be beneficial in enhancing hip extensor strength and promoting
movement behavior to protect against knee injury.

1

CHAPTER I :
OVERVIEW

The knee is the most common site of lower extremity injury in a variety of sport settings.
7,8

Females experience a higher incidence of knee injury (i.e. tears of the anterior cruciate ligament
and patellofemoral pain) when compared to males.
8–10
Insufficient use of the hip extensors during
sport related activities is thought to be contributory to various knee injuries.
1,2
In addition,
diminished use of the hip in the sagittal plane has been associated with higher adductor moments
and valgus angles at the knee; both of which are known risk factors for knee injury.
5,11

It has been proposed that diminished hip extensor strength underlies the movement
behavior that exposes the knee to excessive loading.
1,3
In particular, diminished force production
of the gluteus maximus (GM) is thought to be problematic as this muscle protects against excessive
loading of the knee owing to its multi-planar control of the hip.
2,4,5
However, several studies have
reported that measures of hip extensor strength does not fully account for the variability in lower
extremity movement behavior.
It has been proposed that centrally mediated factors (i.e. diminished neural drive) may be
contributory to the diminished strength and movement behavior that underlies knee injury.
6

Transcranial magnetic stimulation (TMS) is a research tool that can quantify the descending neural
drive along the corticospinal pathway. By stimulating specific area of the motor cortex, motor-
evoked potentials (MEPs) can be elicited to gain insight into the level of corticomotor excitability
(CME) of specific muscles.
12
MEPs obtained using TMS procedures have been used to understand
the underlying neural mechanisms of movement execution.
To date, the CME of specific lower extremity muscles within the context of lower extremity
strength and movement behavior has not been investigated. Given the potential role of GM with
2

respect to movement behavior associated with knee injury, the purpose of this dissertation was to
evaluate the extent to which CME of GM, as quantified using transcranial magnetic stimulation
(TMS), is predictive of hip extensor strength, and functional use of the hip extensors during a sport
specific task. To achieve this objective, 3 studies with the following specific aims were undertaken:

Specific Aim 1:
To establish the reliability of a method for measuring CME of GM using normalized EMG
intensity as the criterion for identifying MEPs during the motor thresholding procedure.
Hypothesis 1:
A TMS method that uses normalized EMG intensity as the criterion for identifying MEPs
during the motor thresholding procedure will result in acceptable between day reliability
of various TMS outcome measures.

Specific Aim 2:
To compare hip extensor strength and corticomotor excitability (CME) of gluteus maximus
(GM) between males and females. A secondary purpose was to determine if CME of GM is
predictive of hip extensor strength.
Hypothesis 2a:
Females will exhibit lower hip extensor strength (peak hip extensor torque) than males.
Hypothesis 2b:
Females will exhibit lower CME of GM (average slope of the input-output curve) than
males.
Hypothesis 2c:
3

The peak hip extensor torque will be predicted by CME of GM for both males and
females combined.

Specific Aim 3:
To determine whether CME of GM is predictive of hip joint kinematics and kinetics during the
execution of a sports specific task.
Hypothesis 3a:
For both males and females, CME of GM will be predictive of the peak hip flexion angle
during the stance phase of a single limb drop jump task.
Hypothesis 3b:
For both males and females, CME of GM will be predictive of the average hip extensor
moment during the stance phase of a single limb drop jump task.

4

CHAPTER II :
BACKGROUND AND SIGNIFICANCE

STATEMENT OF THE PROBLEM
Various knee conditions such as anterior cruciate ligament (ACL) injury and
patellofemoral pain (PFP) are the most prevalent sports injury in a variety of sport settings.
7,8,13–16

A 2 to 3 times higher incidence of knee injuries has been reported in females compared to male
athletes.
8
The disproportional incidence of knee injury between the sexes has been attributed to the
movement behavior related to knee injury which is more commonly observed in female athletes.
The underlying causes of the movement behavior related to knee injury in females has been
extensively discussed based on sex differences in muscle strength,
17,18
neuromuscular
recruitment,
19–23
leg dexterity
24
and leg stiffness.
24,25
Although altered neuromuscular control
frequently has been mentioned as a potential cause of knee injuries, the role of the central nervous
system in relationship to lower extremity movement behavior remains unclear.

BIOMECHANICAL CONTRIBUTIONS TO KNEE INJURY: DIMINISHED USE OF THE HIP
EXTENSORS
Insufficient use of the hip extensors during sport related activities has been linked to
various knee conditions such as patellofemoral pain and tears of the anterior cruciate ligament.
1,2

More specifically, performing tasks such as running and jumping/landing with reduced hip flexion
and diminished hip extensor moments has been reported to result in greater use of the quadriceps
and increased knee loading.
1,2
In addition, diminished use of the hip in the sagittal plane has been
associated with higher adductor moments and valgus angles at the knee; both of which are known
risk factors for knee injury.
5,11

5

Pollard et al. reported that persons with the limited hip and knee flexion angle in sagittal
plane also display a tendency to collapse inward in the frontal plane. It was proposed that the
increased frontal plane motion is a compensation for diminished sagittal plane motion to attenuate
impact forces.
5
Specifically, the diminished use of the hip in kinematic (less flexion) and kinetic
(reduced hip extensor moment) result in excessive knee valgus and knee adductor moment which
has been shown to be detrimental to knee joint.
11,26
The increased knee valgus angle and moments
associated with the biomechanical strategy that relies on the quadriceps have been shown to
increase tension on the ACL
26,27
and the lateral pull of the quadriceps on the patella.
1
The
relationship between sagittal plane use of the hip extensors and the knee adductor moment is
highlighted by Stearns and Powers who reported that 4 weeks of hip focused training resulted in
improved use of the hip extensors and reduced knee adductor moments.
28

THE ROLE OF GLUTEUS MAXIMUS IN CONTRIBUTING TO KNEE INJURY
As noted above, the tendency of the hip is to collapse into adduction and internal rotation
as the hip flexes is contributory to knee injury.
11,26
This tri-planar motion is most commonly
observed during the weight acceptance phase of high-demand activities such as running or landing
from a jump.
29
As a single joint muscle, the gluteus maximus is best suited to provide 3-
dimensional stability of the hip, as this muscle resists the motions of hip flexion, adduction, and
internal rotation.
1,30

Apart from being a strong hip extensor, the gluteus maximus is the most powerful external
rotator of the hip.
30
Its external rotation capacity is supplemented by the actions of the deep hip
rotators (ie, piriformis) and the posterior fibers of the gluteus medius.
1,30
Furthermore, the upper
portion of the gluteus maximus has the ability to abduct the hip and demonstrates an activation
6

pattern similar to that of the gluteus medius. Thus, the frontal and transverse plane control afforded
by the gluteus maximus suggests that this muscle is well suited to protect the knee from abnormal
loading.
1,30

MUSCLE STRENGTH DOES NOT FULLY EXPLAIN MOVEMENT BEHAVIOR
ASSOCIATED WITH KNEE INJURY
Diminished strength of the hip extensors has been proposed to underlie the movement
behavior associated with knee injury as described above.
2,4,31
In particular, impaired force
production of the gluteus maximus (GM) is thought to be problematic as this muscle protects
against excessive loading of the knee owing to its multi-planar control of the hip.
2,4,5
To date, 2
studies have examined the influence of hip extensor strength on knee mechanics during functional
tasks. Stearns et al. reported diminished strength of the hip extensors relative to the knee extensors
was associated with higher knee extensor moments relative to hip extensor moments during a drop
jump task.
2
Teng et al. reported that hip extensor strength was inversely correlated to knee extensor
work during running.
3
However, it should be noted that in both of these studies, hip extensor
strength only explained 15-17% of the variation in movement behavior.
The influence of hip abductor and external rotator strength on hip and knee kinematics has
been investigated with equivocal findings.
17,32–35
Baldon et al. reported that eccentric hip abductor
torque and external rotator torque were correlated with frontal plane femur and knee motion
(r=0.49, p<0.004).
34
However, Homan et al. found no differences in knee valgus between
individuals with high and low hip abductor and external rotators strength.
35
Jacob et al. found that
the hip abductor peak torque did not correlate to the hip adduction or internal rotation during
landing tasks (r=-0.04~0.4, p>0.05).
17
Willson et al. also reported no significant correlation
7

between hip muscle strength and the corresponding hip joint excursions in the frontal and transvers
planes during single-leg jumps.
33
Based on above studies, muscle strength appears, at best, to
explain only a small amount of the variance in movement behavior related to knee injury.

ALTERED MOTOR CONTROL MAY UNDERLIE MOVEMENT BEHAVIOR CONSISTENT
WITH KNEE INJURY
Inadequate motor control has been suggested to underlie lower extremity movement
behavior related to knee injury.
6,19–23
Impaired lower extremity dexterity which reflects reduced
ability of motor control of leg movement has been observed in female athletes who demonstrated
movement behavior associated with knee injury compared to their male counterparts.
24
Evidence
in support of this premise is provided by studies that have shown that altered neuromuscular
activation of the gluteal muscles, such as reduced magnitude of muscle recruitment or a delay in
onset timing, is associated with knee injury.
36,37
Furthermore, it has been proposed that increased
use of the GM following skill acquisition training, as opposed to strengthening, underlies the
protective effect afforded by injury-prevention training.
6
Although previous studies imply that
altered motor control may underlie movement behavior consistent with knee injury, the role of the
central nervous system has not been clearly defined.

8

THE ROLE OF DESCENDING CORTICOSPINAL MOTOR TRACT IN THE CONTROL OF
MOVEMENT
Centrally-mediated neural control can be probed by evaluating the excitability of the
corticomotor pathway of a specific muscle.
12
This is done by measuring the amplitude of motor-
evoked potentials (MEP) produced by the muscle by stimulating the representational area of a
specific muscle in the motor cortex. The corticospinal motor tract is one of the major descending
pathways that deliver neural drive from the motor cortex to peripheral muscle.
38
The corticospinal
motor tract is responsible for several functions including excitation and inhibition of motor neurons,
descending control of afferent inputs, selective control of spinal reflexes.
39–41
Transcranial
magnetic stimulation (TMS) methods have been well-established in upper extremity muscles
during dexterous fine motor skill acquisition. In addition, the assessment of corticomotor
excitability (CME) has used in studies that aim to understand the underlying neural mechanisms
of movement execution, such as feedforward and feedback motor control.
42,43

To execute a voluntary movement, neural signals generated from the motor cortical region,
and delivered through the corticospinal motor pathway, elicit contraction of skeletal muscles. The
movement behavior that is characterized by the kinetics and kinematics at the joint represents an
interaction between the neural control, biomechanical capacity and task demand. A primary aim
of this dissertation is to gain insight into the neuromechanical association at the hip joint to
understand the centrally mediated factors that may underlie the movement behavior related to knee
injury. It is reasonable to speculate the functional use of the hip joint as part of the lower extremity
behavior of a sport specific task could be explained by CME of GM.

9

THE ROLE OF DESCENDING CORTICOSPINAL MOTOR TRACT IN MUSCLE FORCE
GENERATION
Maximum force development of a muscle is determined by 2 factors: 1) structural
morphology (ie, physiological cross-sectional area, fiber type, etc) and, 2) neural recruitment.
44

Changes in the physical characteristics of muscle (ie, hypertrophy) are thought to underlie the
strength gains associated with long-term muscle training.
45,46
Neural factors are thought to
contribute to early muscle strength gains (<6 weeks) in which strength improves without
hypertrophy.
47
Specifically, increased neural drive (as quantified by electromyography) has been
shown to underlie early strength gains during muscle training.
47,48

Previous studies reported that early strength gains observed following muscle training (<4
weeks) could be attributed to an increase in corticomotor excitability.
49,50
Specifically, enhanced
CME has been reported to occur in conjunction with increased muscle strength of muscles such as
tibialis anterior, soleus, and rectus femoris.
50–52
Specific to GM, Yani et al. reported that greater
levels of GM activation was accompanied by higher levels or CME of GM.
53
Taken together, such
findings suggest that increased corticospinal neural drive may contribute to the ability of a muscle
to generate force. To date, the association between corticospinal neural drive and maximum muscle
force output has not been determined.

TMS MEASUREMENTS AND REPRODUCIBILITY
Transcranial magnetic stimulation (TMS) is a non-invasive brain stimulation procedure
that can be used to investigate corticospinal motor excitability of specific muscles. As a result of
a rapid change of magnetic field from the coil placed on the skull, electrical current is induced in
the neurons of the motor cortex. With sufficient stimulator intensity, action potentials of neurons
10

are initiated along the cortical spinal tract as well as the motorneuron pool which innervates the
target muscle. A motor-evoked potential (MEP) is then observed in the contralateral muscle using
electromyography (EMG). From the recorded MEP signals, corticospinal motor excitability can
be quantified based on the maximal slope of the input-output curve
54
. The input-output curve (IOC)
has been shown to represent corticospinal motor excitability that recruits neurons from low to high
thresholds.
55,56
The IOC response from a range of stimulation intensities is thought to represent a
more characteristic profile of corticospinal motor excitability of a muscle than the MEP responses
from a single stimulation intensity.
Assessment of corticospinal motor excitability of the lower extremity muscles is
challenging for researchers based on the fact that the observed corticospinal motor excitability is
relatively low and the cortical representational areas are relatively small in the motor cortex. In
addition, an active contraction is necessary for measuring corticomotor excitability (CME) of
proximal lower extremity muscles.
57,58
Muscle activation during the TMS procedure stabilizes
cortical and spinal excitability and has been shown to elicit larger MEPs compared to the MEPs
elicited by the same intensity during a resting condition.
54,59
Given that the active state of a muscle
is important in eliciting MEPs of proximal lower extremity muscles, standardizing the level of
contraction during the motor thresholding procedure would appear to be important to facilitate the
comparison of TMS responses between muscles and/or individuals.
Another issue related to TMS evaluation of lower extremity muscles is the process of motor
thresholding. The conventional method used for motor thresholding of upper extremity muscles is
to determine the smallest stimulation intensity needed to elicit 5 out of 10 MEPs that are larger
than a fixed voltage value (i.e. 100 or 200 uV). This method poses a challenge for the assessment
of proximal lower extremity muscles as there are factors unrelated to muscle contraction that can
11

influence the electromyographic (EMG) signal. In particular, the GM has a greater amount of
subcutaneous fat overlying the muscle compared to other lower extremity muscles such as the VL.
Subcutaneous fat is known to act as a low-pass filter thus attenuating EMG signals.
60
With respect
to the motor thresholding procedure, a greater stimulator intensity likely would be required to elicit
a MEP at the GM hotspot compared to VL hotspot. The different stimulator intensities use to elicit
MEPs from two muscles could lead to a bias in terms of TMS outcome measures (i.e. input-output
curves, maximum MEPs, etc.).
The process of normalization is recommended to control for factors unrelated to muscle
contraction to facilitate comparison of EMG signals between muscles or among individuals.
61
The
most common method used in kinesiologic EMG research is to express EMG signals as a
percentage of a standardized level of activation (ie. maximum voluntary isometric contraction or
MVIC).
61
Given the need to standardize the level of muscle contraction during the motor
thresholding procedure, and to provide a comparable criterion for establishing MEPs, a TMS
method that utilizes normalized EMG amplitudes would appear to have advantages over
conventional methods that use fixed voltage values.
It has been suggested that using a double cone coil and testing under active contraction
conditions can facilitate the TMS assessment of the lower extremity muscles.
57,62
The
reproducibility of measuring corticospinal motor excitability of GM and VL has been verified by
the amplitude of MEPs at a single stimulation intensity of 120% active motor threshold (ICCs
ranging from 0.73-0.87).
57,63
To date, no study has determined the reliability of corticospinal motor
excitability of GM and VL by measuring the slope of the IOC from TMS.

12

SUMMARY
Current literature supports the premise that insufficient use of the hip extensors is
contributory to movement behavior related to knee injury. Based on the importance of the gluteus
maximus to the control of the hip and lower extremity movement related to knee injury, it is
reasonable to hypothesize that the centrally-mediated factors are associated with hip extensor
strength and the mechanics of the hip during landing. To test this this hypothesis, a reliable method
for the neuromechanical measurement of GM is needed. Results from this dissertation will enhance
the development of rehabilitation and injury prevention programs that target the modification of
movement behavior in persons with knee pain.

13

CHAPTER III :
RELIABILITY OF A METHOD TO ASSESS CORTICOMOTOR EXCITABILITY OF
PROXIMAL LOWER EXTREMITY MUSCLES USING A NORMALIZED EMG
MOTOR THRESHOLDING PROCEDURE

The purpose of this Chapter was to establish the reliability of a method for measuring corticomotor
excitability of gluteus maximus (GM) and vastus lateralis (VL) using a normalized EMG value as
the criterion for identifying MEPs during the motor thresholding procedure (as opposed to a fixed
voltage value). Ten healthy participants were recruited. TMS data were acquired using the input-
output curve (IOC) procedure while participants performed an isometric contraction of GM and
VL (20% of maximal voluntary isometric contraction). The active motor threshold for each muscle
was determined using the lowest stimulator intensity required to elicit 5 motor evoked potentials
(MEPs) from 10 stimulations that exceeded 20% MVIC. The average and peak slopes of the IOC
data points were analyzed using linear regression and sigmoid curve fitting respectively. TMS data
were obtained on 2 separate days and compared using random-effect intra-class correlation
coefficients (ICCs).

14

INTRODUCTION
Transcranial magnetic stimulation (TMS) is a research method that can be used to probe
the excitability of the corticospinal descending pathways of the central nervous system.
12,40
TMS
measures have been shown to be related to motor behaviors such as reaction time,
64
gait function,
65

as well as skill training induced-neuroplasticity.
66
TMS provides neurophysiological information
that may provide insight into how the central nervous system contributes to the modulation of
movement behavior. In particular, there is a growing interest in the TMS assessment of lower
extremity muscles such as the gluteus maximus (GM) and vastus lateralis (VL) to understand how
centrally mediated factors may contribute to various lower extremity injuries.
6,67–70

Although TMS protocols for upper extremity muscles have been well-established, there
are inherent challenges associated with TMS assessment of proximal lower extremity muscles.
Specifically, the cortical representational areas of proximal lower extremity muscles are small and
lie within the medial longitudinal fissure thereby requiring use of a double cone coil.
57
In addition,
an active contraction is necessary for measuring corticomotor excitability (CME) of proximal
lower extremity muscles.
57,58
Muscle activation during the TMS procedure stabilizes cortical and
spinal excitability and has been shown to elicit larger motor evoked potentials (MEPs) compared
to the MEPs elicited by the same intensity during a resting condition.
54,59
Given that the active
state of a muscle is important in eliciting MEPs of proximal lower extremity muscles,
standardizing the level of contraction during the motor thresholding procedure is important to
facilitate the comparison of TMS responses between muscles and/or individuals.
The conventional method used for motor thresholding of upper extremity muscles is to
determine the smallest stimulation intensity needed to elicit 5 out of 10 MEPs that are larger than
a fixed voltage value (i.e. 100 or 200 uV). This method poses a challenge for the assessment of
15

proximal lower extremity muscles as there are factors unrelated to muscle contraction that can
influence the electromyographic (EMG) signal. In particular, the GM has a greater amount of
subcutaneous fat overlying the muscle compared to other lower extremity muscles such as the VL.
Subcutaneous fat is known to act as a low-pass filter thus attenuating EMG signals.
60
With respect
to the motor thresholding procedure, a greater stimulator intensity likely would be required to elicit
a MEP at the GM hotspot compared to the VL hotspot. The different stimulator intensities used to
elicit MEPs from two muscles could lead to a bias in terms of TMS outcome measures (i.e. input-
output curves, maximum MEPs, etc.).
The process of normalization is recommended to control for factors unrelated to muscle
contraction to facilitate comparison of EMG signals between muscles or among individuals.
61
The
most common method used in kinesiologic EMG research is to express EMG signals as a
percentage of a standardized level of activation (ie. maximum voluntary isometric contraction or
MVIC).
61
Given the need to standardize the level of muscle contraction during the motor
thresholding procedure, and to provide a comparable criterion for establishing MEPs, a TMS
method that utilizes normalized EMG amplitudes would appear to have advantages over
conventional methods that use fixed voltage values.
The purpose of the current study was to establish the reliability of a method for measuring
CME of the GM and VL using normalized EMG intensity as the criterion for identifying MEPs
during the motor thresholding procedure. We hypothesized that this method would result in
acceptable between day reliability of various TMS outcome measures, thus facilitating comparison
of data between muscles and/or individuals. A reliable TMS methodology for proximal lower
extremity muscles is an important step in understanding how centrally-mediated factors may
contribute to lower extremity motor behavior.
16

METHODS
Participants
Ten healthy, active participants between the ages of 21 and 36 were recruited for this study
(5 females, 5 males). To be eligible, participants had to engage in some form of physical activity
for at least 30 min, 2 times a week and be at least 18 years of age. Participants were excluded if
they reported a previous history of lower extremity pathology or trauma, or lower extremity pain
during sport or activities of daily living. Additional exclusion criteria included any “yes” answer
on the TMS safety questionnaire indicating if they had metal, electrical, magnetic implants; a
personal or family history of epilepsy; or the possibility of being pregnant.
71
Participants were
required to attend 2 test sessions on 2 separate days within a week.

Procedures
Prior to testing, participants provided informed written consent as approved by the
Institutional Review Board of the Health Sciences Campus at the University of Southern California.
Participants were asked to keep their daily routine consistent on both testing days (including
caffeine intake). For the TMS procedures describe below, stimulations were applied on the primary
motor cortex contralateral to the dominant leg (i.e. preferred leg to kick a ball).
Before initiating the TMS assessment, EMG signals of VL and GM were collected during
a MVIC for the purposes of (1) providing the target contraction level during the TMS procedure,
and (2) establishing the criteria for the identification of a MEP during motor thresholding. The
skin over the VL and GM were shaved and prepared with alcohol to decrease skin impedance.
Surface EMG electrodes (bipolar Ag/AgCl with 22mm inter-electrode distance) were placed over
17

the muscle belly of VL and GM. The electrode for VL was positioned 1/3 of the distance between
patella to anterior superior iliac spine.
72
For GM, the electrode position was the mid-point between
the ischial tuberosity and the mid-point of the greater trochanter and the sacrum.
72
To allow for
consistent electrode placement between testing days, electrode positions were marked with a
permanent marker. The EMG signal was sampled at 5000 Hz and amplified using a gain of 2000.
Following electrode placement, MVIC trials of VL and GM were performed. For the VL
MVIC trials, participants were seated with the hip and knee in 90° and 60° of flexion, respectively.
A non-stretchable belt was placed at the distal end of the tibia to provide resistance. Participants
were instructed to extend the knee as hard as possible and hold for 5 seconds. For the GM MVIC
trials, participants were positioned prone with the hips at the edge of a treatment table. The tested
leg was positioned in 90° of flexion, 45° of hip abduction, and end range of hip external rotation.
Participants were instructed to push simultaneously into hip extension, abduction, external rotation
against manual resistance provided by the examiner for 5 seconds.
73
Verbal encouragement was
provided during the MVIC trials to facilitate a maximum effort. Two MVIC trials were performed
for each muscle. The largest averaged 0.2 s root mean square value of the EMG signal from the
two trials was used as the MVIC value for the TMS procedures described below.
TMS assessments were performed with a single-pulse magnetic stimulator (MagStim 2002,
The Magstim Company Ltd, Whitland, UK) using a 110 mm double cone coil. The Brainsight
Neuronavigation System (Rogue Research Inc, Montreal, Canada) was used to ensure accurate
coil placement during both TMS assessments. Reflective markers were fixed to the participant’s
head and the TMS coil as part of the neuronavigation procedure. Landmarks on the participants’
head were co-registered using an infrared marker tracking system. The coil position and orientation
18

were then tracked relative to the positions of these markers on a 3-D reconstruction of a template
magnetic resonance image of the brain.
Stimulations were delivered in the supine position during an active contraction of the GM
and VL. For the GM contraction, participants were instructed to “squeeze their buttocks”. For the
VL contraction, participants were instructed to “tighten their thigh muscle”. During the active
contractions, real-time visual feedback reflecting the root mean square (RMS) averaged amplitude
of the EMG signal was provided. Participants were instructed to match the RMS signal to the target
contraction level set at 20% MVIC. Twenty percent MVIC was chosen as the target value a
previous study reported better reliability of MEPs obtained from an upper extremity muscle during
low level contractions (20-25% MVIC) compared to high level contractions (75-100% MVIC).
74

Prior to active motor thresholding, the optimal coil position on the scalp (i.e. “hotspot”) for
the muscle of interest was identified by systematically delivering stimulations over a 4 cm x 4 cm
area lateral to the vertex of the contralateral side of the testing leg. The hotspots of GM and VL
were located separately and identified as the position on the scalp that elicited the largest and most
consistent MEPs. The position of each hotspot was recorded in Brainsight so that the TMS could
be applied at the same position for the second testing session.
Following the determination of the hotspot location, active motor thresholding (AMT) was
performed. The active motor threshold (AMT) of GM and VL was determined as the smallest
stimulation intensity that elicited 5 MEPs out of 10 stimulations. A MEP was identified as the
TMS-induced EMG activation that was larger than background activation (>20% MVIC) within
40 ms of the stimulation.
19

Following motor thresholding, the IOC procedure was performed for each muscle.
Stimulations were performed over the hotspot at intensities ranging from 100 to 200% AMT in
10% increments. Ten stimulations were delivered at each of the stimulator intensities.

Data Analysis
The average of the peak-to-peak amplitude of the 10 MEPs obtained at each stimulator
intensity of the IOC procedure was calculated. An IOC for GM and VL was obtained by plotting
the average MEP amplitude against its corresponding percentage of AMT. The average and peak
slopes of the IOC data points were analyzed using linear regression and sigmoid curve fitting,
respectively. To calculate the average slope using linear regression, only data points from 100%
AMT to the maximum average MEP were used.
75
To calculated peak slope, a Boltzman sigmoid
function with non-linear least-mean square was fit to data points obtained from all stimulator
intensities.
54

Statistical Analysis
To evaluate between day test-retest reliability of the peak and average slopes of the IOC,
as well at the maximum MEP amplitude obtained from VL and GM, a random-effect intra-class
correlation coefficient (ICC) was calculated using PASW statistics 18 (SPSS, Inc.). The ICC 2,1
and the upper and lower bound of 95% confidence interval were reported for each of the variables.
ICC values less than 0.5 were interpreted as poor reliability, ICCs between 0.5 and 0.75 were
interpreted as moderate reliability, ICCs between 0.75 and 0.9 were interpreted as good reliability,
and ICCs greater than 0.9 were interpreted as excellent reliability.
76,77
The ICC 95% confidence
intervals (CI), standard error of measurement (SEM) and the minimal detectable change (MDC)
20

were reported for all variables of interests. The standard error of measurement (SEM) was
calculated as (Standard Deviation x √ (1 – ICC score)) to determine the random systematic
measurement error. The MDC was calculated as (1.96 ×√2×SEM).

RESULTS
The reliability coefficients for the TMS measurements as well as the SEM and MDC values
for GM and VL are presented in Tables 3-1 and 3-2, respectively. For GM, reliability of average
and peak slopes obtained from the IOC procedure as well as the maximum MEP achieved excellent
reliability (ICCs > 0.9; Table 3-1). With respect to the VL, the reliability of the TMS measures of
interest ranged from good to excellent (ICCs ranging from 0.75-0.91; Table 3-2).

Table 3-1. Reliability results for the TMS measures of interest for gluteus maximus.
Day 1
(mean ± SD)
Day2
(mean ± SD)
ICC 95% CI SEM MDC
Average slope 2.00 ± 1.43 1.80 ±1.35 0.97 0.87-0.99 0.25 0.70
Peak slope 3.33 ± 2.29 3.53 ± 2.56 0.91 0.63-0.98 0.73 2.03
Maximum MEP (mV) 1.87 ±1.24 1.84 ±1.19 0.99 0.96-1.00 0.12 0.34
Abbreviations: SD: standard deviation; CI: confidence interval; SEM: standard error of
measurement; MDC: minimal detectable change.

21

Table 3-2. Reliability results for the TMS measures of interest for vastus lateralis.
Day 1
(mean ± SD)
Day2
(mean ± SD)
ICC 95% CI SEM MDC
Average slope 1.21 ± 1.29 1.12 ±0.99 0.91 0.63-0.98 0.35 0.96
Peak slope 2.39 ± 2.86 2.08 ±1.45 0.75 -0.04-0.94 1.13 3.13
Maximum MEP (mV) 1.04 ± 0.46 1.17 ±0.61 0.86 0.46-0.96 0.21 0.57
Abbreviations: SD: standard deviation; CI: confidence interval; SEM: standard error of
measurement; MDC: minimal detectable change.

DISCUSSION
With the growing interest in TMS assessment of lower extremity muscles, there is a need
to establish methods that are reliable and procedures that allow for valid comparison of outcome
measures across muscles. The purpose of the current study was to establish the reliability of a
method for measuring CME of proximal lower extremity muscles. By using normalized EMG
during the motor thresholding procedure, we sought to minimize 2 potential sources of error that
could lead to bias when comparing TMS results across muscles by 1) providing a comparable level
of active contraction during the thresholding and by 2) establishing a consistent criterion for the
identification of MEPs. Importantly, the use of normalized EMG to establish the criterion for
motor thresholding as reported in the current study, resulted in the successful attainment of MEPs
from all 10 participants for each muscle on both testing days.
Data obtained from the IOC procedure represents collection of MEPs and provides a more
comprehensive evaluation of CME compared to MEP amplitudes from a single stimulation
intensity.
54,78
All TMS measurements related to the IOC in the current study demonstrated good to
22

excellent reliability. Although sigmoid curve fitting is the most common method used to analyze
the IOC,
54,56
the linear slope method also exhibited excellent reliability. Our range of ICC values
were superior to a previous TMS study of the first dorsal interossei that reported poor to excellent
reliability (ICCs>ranging from 0.19 to 0.90) for both linear regression and sigmoid curve fitting
methods.
75
With respect to lower extremity muscles, our results are consistent with a previous
study that reported good reliability of the peak slope obtained from the IOC using sigmoid curve
fitting for the tibialis anterior (ICC 0.78).
79

Our ICC values for maximum MEP are somewhat better than previous reliability studies
in which the GM and VL were evaluated. For example, the ICCs for test-retest reliability for MEP
amplitude at a single stimulation intensity has been reported to range from 0.76-0.83 for GM
57

and 0.82-0.97 for VL.
80
Our relatively low SEMs and MDCs for maximum MEPs of VL and GM
indicate that such measures would be sensitive enough to detect real change owing to an
intervention or to identify differences between muscles.
It could be argued that the good to excellent levels of reliability reported in the current
study may be attributed to the use of normalized EMG to provide a consistent level of active
contraction during thresholding and to establish a standardized criterion for the determination of
MEPs. This is important as previous research has reported enhanced MEP amplitude of GM with
greater activation levels.
53
With respect to VL, Temesi et al. reported the peak IOC slope during
50% MVIC was significantly steeper than the peak slope obtained during 10% MVIC.
81
It is clear
that MEP amplitudes are influenced by the contraction level and would be a source of unwanted
variability. Controlling for such variability would appear to be most important in evaluating
maximum MEP or the MEP at a single stimulator intensity.
23

Given the large amount of subcutaneous fat overlying the GM, obtaining consistent MEPs
from this muscle would appear to be difficult. Indeed, a previous single-pulse TMS study of GM
reported that MEP amplitude was successfully measured in less than one-third of participants using
the traditional fixed voltage value protocol during motor thresholding.
69
It is likely that MEP
amplitudes were being attenuated by varying levels of subcutaneous fat overlying GM across
individuals and thus were smaller than the 100 uV criteria for an active contraction condition or
hidden within the background level of activation.
For participants in which significant subcutaneous fat is present, use of the 100 uV criteria
would require a higher stimulator intensity to achieve a MEP. Using normalized EMG, the MEP
amplitude and the criteria are expressed as a percentage of MVIC which would require a lower
stimulator intensity to achieve a MEP. Therefore, the motor thresholding would be more tolerable
for participants as the stimulation intensity would be minimized as well the number of required
stimulations during thresholding. On the other end of the spectrum, the background EMG from a
pre-stimulus contraction can be larger than 100 uV criteria and therefore MEPs may be embedded
in the background EMG signal and difficult to detect. Applying the normalized EMG methodology
is particularly important when more than one muscle (ie. GM and VL) are examined and compared
in the same study.
There are several limitations of our study that should be considered when interpreting the
results. First, we only recruited young, healthy participants. As such, our findings may not be
generalizable to various patient populations. Second, the TMS procedure described above was
performed with participants performing an isometric contraction in a supine position. Our findings
may not apply to TMS procedures performed in standing or during active movement (i.e. walking).
Third, we only evaluated the reliability of certain TMS outcome measures related to the IOC.
24

Whether or not other measures would exhibit the high levels of reliability reported here remains
to be determined (i.e. MEP latency, cortical silent period, etc.). Lastly, the use of normalized EMG
for the purposes of this study assumed that all participants provided a maximum effort during the
MVIC.

CONCLUSION
A reliable method to measure CME of proximal lower extremity muscles has been
described. Specifically, we used normalized EMG to 1) provide a consistent target contraction
level during the motor thresholding procedure and 2) establish a consistent criterion for the
identification of a MEP (as opposed to a fixed voltage). Better standardization of TMS procedures
is necessary to facilitate comparison of outcome measures between lower extremity muscles and
individuals.

25

CHAPTER IV :
INFLUENCE OF CORTICOMOTOR EXCITABILITY OF GLUTEUS MAXIMUS ON
HIP EXTENSOR STRENGTH: A SEX COMPARISON

The purpose of this Chapter was to compare hip extensor strength and corticomotor excitability
(CME) of gluteus maximus (GM) between males and females. A secondary purpose was to
determine if CME of GM is associated with hip extensor strength. Thirty-two healthy individuals
participated (15 males and 17 females). CME of GM was assessed using the input-output curve
(IOC) procedure acquired from transcranial magnetic stimulation (average slope). Hip extensor
strength was measured by a dynamometer during a maximal voluntary isometric contraction. One-
tailed t-tests were used to compare CME of GM and peak hip extensor torque between males and
females. Linear regression analysis was used to determine whether peak hip extensor torque was
predicted by GM CME

26

INTRODUCTION
Females experience a higher incidence of knee injury (i.e. tears of the anterior cruciate
ligament and patellofemoral pain) when compared to males.
8–10
The disproportional incidence of
knee injury between the sexes has been attributed to faulty movement patterns owing to diminished
hip muscle strength.
17,82,83
In particular, diminished strength of the gluteus maximus has been
proposed to underlie several knee injuries.
31,84,85
As a single joint muscle, the gluteus maximus is
best suited to provide multi-planar control of the hip and knee as this muscle resists the motions
of hip flexion, adduction, and internal rotation.
30

Maximum force development of a muscle is determined by 2 factors: 1) structural
morphology (ie, physiological cross-sectional area, fiber type, etc) and, 2) neural recruitment.
44

Changes in the physical characteristics of muscle (ie, hypertrophy) are thought to underlie the
strength gains associated with long-term muscle training.
45,46
However, neural factors are thought
to contribute to early muscle strength gains (<6 weeks) in which strength improves without
hypertrophy.
47
Specifically, increased neural drive (as quantified by electromyography) has been
shown to underlie early strength gains during muscle training.
47,48

Transcranial magnetic stimulation (TMS) is a method that has been used to evaluate the
descending neural drive along the corticomotor pathway of various muscles. In regards to muscle
strength, previous studies reported that early strength gains observed following muscle training
(<4 weeks) could be attributed to an increase in CME.
49,50
Specifically, enhanced CME has been
reported to occur in conjunction with increased muscle strength of muscles such as tibialis anterior,
soleus, and rectus femoris.
50–52
Specific to GM, Yani et al. reported that greater levels of GM
activation was accompanied by higher levels or CME of GM.
53
Taken together, such findings
suggest that increased corticospinal neural drive may contribute to the ability of a muscle to
27

generate force. To date, the association between corticospinal neural drive and maximum torque
output has not been determined.
Given the importance of hip strength in relation to knee injury in females, the current
investigation sought to determine whether sex differences in hip extensor strength could be
explained, in part, by diminished CME of GM. We hypothesized that females would exhibit lower
peak hip extensor torque and CME of GM compared to males. We also hypothesized that CME of
GM would be positively associated with hip extensor strength for both males and females.

METHOD
Participants
Thirty-two active non-disabled participants between ages of 21 and 36 were recruited for
this study (17 females, 15 males; Table 4-1). To be eligible, participants had to engage in some
form of physical activity for at least 30 min, 2 times a week and be at least 18 years of age.
Participants were excluded if they reported a previous history of lower extremity pathology or
trauma, or lower extremity pain during sport or activities of daily living. Additional exclusion
criteria included any “yes” answer on the TMS safety questionnaire indicating if they had metal,
electrical, magnetic implants; a personal or family history of epilepsy; or the possibility of being
pregnant.
71

28

Table 4-1. Participant demographics (Mean ± Standard Deviation)

Females Males p
Age (yr) 26.7 ± 3.4 28.5 ± 5.3 0.264
Height (cm) 163.2 ± 5.5 180.2 ± 5.6 <0.001
Weight (kg) 60.2 ± 7.3 82.2 ± 10.4 <0.001
BMI (kg/m
2
) 22.6 ± 2.82 25.2 ± 1.9 <0.001

Procedures
Prior to testing, participants provided informed written consent as approved by the
Institutional Review Board of the Health Sciences Campus at the University of Southern California.
Participants were asked to keep their daily routine consistent on both testing days (including
caffeine intake). For the TMS procedures describe below, stimulations were applied to the primary
motor cortex contralateral to the dominant leg (i.e. preferred leg to kick a ball). Hip extensor
strength was evaluated on the dominant leg. TMS and strength data were obtained on 2 separate
days within a week.
Hip extensor strength was assessed during a maximal voluntary isometric contraction
(MVIC) using a motor-driven dynamometer (Cybex with HUMAX NORM; Computer Sports
Medicine Inc, Stoughton, MA). Participants were positioned prone with the pelvis placed on the
edge of the testing table. The hip and knee joints were positioned at 60° and 90° of flexion,
respectively. The axis of the dynamometer was aligned with the greater trochanter of the tested
leg. The resistance pad was positioned just proximal to the knee joint line and secured to the distal
thigh with a strap. Participants performed two, 5s trials in which they pushed with maximum effort
against the resistance pad. Verbal encouragement was provided. A one-minute rest period was
29

provided between MVIC trials to minimize muscle fatigue. The largest peak torque value from the
2 trials was used for statistical analysis. Peak hip extensor torque was normalized by body mass
index (body mass in kg divided by the body height in meters squared).
Prior to initiating the TMS assessment, EMG signals of GM were collected during a MVIC
for the purposes of 1) providing the target contraction level during the TMS procedure, and 2)
establishing the criteria for the identification of a MEP during motor thresholding. The skin over
the GM was shaved and prepared with alcohol to decrease skin impedance. Surface EMG
electrodes (bipolar Ag/AgCl with 22 mm inter-electrode distance) were placed over the muscle
belly of GM. For GM, the electrode position was the mid-point between the ischial tuberosity and
the mid-point of the greater trochanter and the sacrum.
72
To allow for consistent electrode
placement between testing days, electrode positions were marked with a permanent marker. The
EMG signal was sampled at 5000 Hz and amplified using a gain of 2000.
Following electrode placement, MVIC trials were performed. Participants were positioned
prone with the hips at the edge of a treatment table. The tested leg was positioned in 90° of flexion,
45° of hip abduction, and end range of hip external rotation. Participants were instructed to push
simultaneously into hip extension, abduction, external rotation against manual resistance provided
by the examiner for 5 seconds.
73
Verbal encouragement was provided during the MVIC trials to
facilitate a maximum effort. The largest averaged 0.2 s root mean square value of the EMG signal
from the two trials was used as the MVIC value for the TMS procedures described below.
All TMS assessments were performed with a single-pulse magnetic stimulator (MagStim
2002, The Magstim Company Ltd, Whitland, UK) using a 110 mm double cone coil. The
Brainsight Neuronavigation System (Rogue Research Inc, Montreal, Canada) was used to ensure
accurate coil placement during both TMS assessments. Reflective markers were fixed to the
30

participant’s head and the TMS coil as part of the neuronavigation procedure. Landmarks on the
participants’ head were co-registered using an infrared marker tracking system. The coil position
and orientation were then tracked relative to the positions of these markers on a 3-D reconstruction
of a template magnetic resonance image of the brain.
Stimulations were delivered in the supine position during an active contraction of the GM.
Participants were instructed to “squeeze their buttocks”. During the active contractions, real-time
visual feedback reflecting the root mean square (RMS) average amplitude of the EMG signal was
provided. Participants were instructed to match the RMS signal to the target contraction level set
at 20% MVIC. Twenty percent MVIC was chosen as the target value as a previous study reported
better reliability of MEPs obtained from an upper extremity muscle during low level contractions
(20-25% MVIC) compared to high level contractions (75-100% MVIC).
74

Prior to active motor thresholding, the optimal coil position on the scalp (i.e. “hotspot”) for
GM was identified by systematically delivering stimulations over a 4 cm x 4 cm area lateral to the
vertex of the contralateral side of the testing leg. The hotspot was located as the position on the
scalp that elicited the largest and most consistent MEPs.
Following the determination of the hotspot location, active motor thresholding (AMT) was
performed. The AMT was determined as the smallest stimulation intensity that elicited 5 MEPs
out of 10 stimulations. A MEP was identified as the TMS-induced EMG activation that was larger
than background activation (>20% MVIC) within 40 ms of the stimulation.
Following motor thresholding, the IOC procedure was performed. Stimulations were
performed over the hotspot at intensities ranging from 100 to 200% AMT in 10% increments. Ten
stimulations were delivered at each of the stimulator intensities.

31

Data Analysis
The average of the peak-to-peak amplitude of the 10 MEPs obtained at each stimulator
intensity of the IOC procedure was calculated. An IOC was obtained by plotting the average MEP
amplitude against its corresponding percentage of AMT. The average slope of the IOC data points
were analyzed with linear regression using the data points from 100% AMT to the maximum
average MEP.
75
The average slope of the regression line was used as the indicator of CME of GM.
Representative data from a male and female participate are shown in Figure 4-1.

Figure 4-1. Representative IOC results for a female (left) and male (right) participant. The circles
represent the average of the 10 MEP amplitudes at a given stimulator intensity. The solid lines
represent the regression line of MEPs from 100% AMT to the maximum MEP.

Statistical Analysis
Independent t-tests were used to compare males to females, based on peak hip extensor
torque, and CME of GM. Linear regression analysis was used to determine whether peak hip
extensor torque (dependent variable) was predicted by CME of GM. First, we tested for the effect
32

of sex on hip extensor peak torque controlling for CME of GM. If significant, we then tested for
the presence of a CME of GM * sex interaction. If the interaction was significant, separate
regression analyses were performed for males and females. All statistical analyses were performed
using PASW statistics 18.0.0 (IBM Corporation, Armonk, NY).

RESULTS
On average, females demonstrated significantly lower peak hip extensor torque compared
to males (4.42 ± 1.11 vs. 6.15 ± 1.72 Nm/kg/m
2
, p=0.002; Figure 4-2). Similarly, females
demonstrated significantly lower CME of GM (average slope of the IOC curve) compared to males
(1.36 ± 1.07 vs. 2.67 ± 1.30, p=0.004; Figure 4-3). In terms of the regression analysis, sex was not
a significant predictor of hip extensor peak torque when controlling for CME of GM. The
regression analysis for both males and females combined revealed CME of GM was a significant
predictor of peak hip extensor torque (r
2
= 0.36, p<0.000; Figure 4-4).

33

Figure 4-2. Comparison of peak hip extensor torque between sexes.
(* indicates statistical difference; p<0.05)

Figure 4-3. Comparison of corticomotor excitability of gluteus maximus between sexes.
(* indicates statistical difference; p<0.05)

34

Figure 4-4. Scatterplot showing the relationship of the GM IOC slope and the peak hip extensor
torque for all participants.

DISCUSSION
The purpose of current study was to investigate whether reduced CME of GM is
contributory to sex differences in hip extensor strength. Consistent with our hypothesis, we found
that females exhibited less CME of GM and lower peak hip extensor torque compared to males.
In addition, we found that CME of GM was predictive of peak hip extensor torque for both males
and females combined. Our findings support the premise that increased corticospinal neural drive
plays a role in a muscle’s ability to generate maximum torque.
Our finding of diminished hip extensor strength in females is consistent with previous
studies.
2,86
On average, females in the current study exhibited 28% lower hip extensor strength
35

values compared to their male counterparts. This percent difference between the sexes is
comparable to what has previously been reported for hip extensor strength (32-38%).
2,86

A novel finding of the current study was the fact that females exhibited lower CME of
GM compared to males. On average, the slope of the IOC in males was almost twice that of the
females. A review of the literature only identified one study that examined sex differences in TMS
measures. Pitcher et al. compared the peak slope of the IOC of the first dorsal interosseous (FDI)
between males and females and found no significant difference between the sexes.
87
It should be
noted however, that strength of the FDI was not evaluated. It is possible that FDI strength did not
vary between males and females thus resulting in a non-significant TMS finding. It is likely that
sex differences in CME may be muscle specific as opposed to a generalized sex effect across all
muscles.
Given the cross-sectional nature of our study, it is not possible to establish the cause of
the diminished hip extensor strength and neural drive associated with GM. However, previous
biomechanical studies have reported that females exhibit diminished use of the hip extensors and
less activation of the gluteus maximus during functional task such as jumping/landing and
squatting.
2,37,88
It is possible that diminished CME of GM observed in females may be a result of
reduced use of the hip extensor muscle group during various functional tasks. Exercise related
neuroplasticity following long-term use of a muscle has been observed in ballet dancers who
exhibit increased CME of the ankle flexors compared to non-dancers.
89
It is logical to assume that
chronic disuse of a muscle group may lead to reduced CME and in turn, diminished strength.
Future research is needed to confirm whether greater functional use of the hip extensors is
associated with greater CME of GM.
36

Apart from the sex differences in hip extensor strength and CME of GM, we also found
that CME of GM was predictive of hip extensor strength for both males and females combined.
The fact that a CME of GM * sex interaction was not observed suggests that this relationship was
similar between males and females. It should be noted however that CME of GM only explained
36% of the variance in peak hip extensor torque. While our findings confirm the hypothesis that
CME of GM is a contributor to hip extensor strength, we only examined one of the 3 primary hip
extensors. The hamstrings and adductor magnus also are large hip extensors and contribute to
maximum hip extensor torque production.
Our results add to the existing body of literature suggesting that maximum torque output
is mediated, in part, through the CNS.
50–52
However, it should be recognized that corticomotor
excitability as measured in the current study reflects the responsiveness of the entire corticospinal
motor pathway. As such, it cannot be determined whether muscle force output was mediated to a
greater extent by cortical or spinal circuits. Nonetheless, previous research involving human
subjects,
53,90
and non-human primates,
91,92
suggests that muscle force output may be mediated
cortically. Although it is debatable whether the force generation is modulated at the level of the
spinal motoneuron,
93,94
excitability of the spinal motoneuron pool likely is modulated by
supraspinal centers.
The results of our study have clinical implications regarding the enhancement of hip
extensor strength. A previous study from our research group has shown that CME of GM is
modifiable and can be upregulated following 6 days of activation training.
67
As such, an
intervention focused on modulating CME of GM may be effective for facilitating hip extensor
strength. By increasing CME, GM may be “primed” as part of a long-term strengthening
37

program.
67
Additional study is needed to determine whether increasing CME of GM results in
improvement of hip extensor strength.
The results of the current study should be interpreted in light of several limitations. First,
our TMS measurements and strength testing were not performed simultaneously. Despite this
limitation however, a significant relationship between peak hip extensor torque and CME of GM
was found. Second, we only measured CME of GM It is possible that a higher level of
predictability would have been evident if the CME from other hip extensors (hamstrings and
adductor magnus) were obtained. Third, we only recruited young, active participants. As such, our
findings may not be generalizable to various patient populations.

CONCLUSION
Results of this study revealed that females exhibited less CME of GM and lower peak hip
extensor torque compared to males. In addition, we found that CME of GM was predictive of peak
hip extensor torque for both males and females combined. Our findings support the premise that
increased corticospinal neural drive plays a role in a muscles ability to generate torque.
Interventions aiming to enhance modulation of CME of GM may be useful to improve hip extensor
torque output.

38

CHAPTER V :
CORTICOMOTOR EXCITABILITY OF GLUTEUS MAXIMUS IS ASSOCIATED
WITH SAGITTAL PLANE HIP KINEMATICS AND KINETICS DURING A SINGLE
LEG DROP JUMP TASK

The purpose of this Chapter was to determine the association between corticomotor excitability
(CME) of gluteus maximus (GM) and sagittal plane hip kinetics and kinematics during a single
leg drop jump task. Thirty-two healthy individuals (17 females, 15 males) participated. The slope
of the input-output curve (IOC) obtained from transcranial magnetic stimulation (TMS) was used
to assess CME of GM. The average hip extensor moment and peak hip flexion angle during the
stance phase of the single leg drop jump task was calculated. Linear regression analysis was used
to determine whether the average hip extensor moment and peak hip flexion were predicted by
CME of GM.

39

INTRODUCTION
Insufficient use of the hip extensors during sport related activities has been linked to
various knee conditions such as patellofemoral pain and tears of the anterior cruciate ligament.
1

More specifically, performing tasks such as running and jumping/landing with reduced hip flexion
and diminished hip extensor moments has been reported to result in greater use of the quadriceps
and increased knee loading.
1,2
In addition, diminished use of the hip in the sagittal plane has been
associated with higher adductor moments and valgus angles at the knee; both of which are known
risk factors for knee injury.
5,11

It has been proposed that diminished hip extensor strength underlies the movement
behavior that exposes the knee to excessive loading.
1,3
In particular, diminished force production
of the gluteus maximus (GM) is thought to be problematic as this muscle protects against excessive
loading of the knee owing to its multi-planar control of the hip.
2,4,5
To date, 2 studies have
examined the influence of hip extensor strength on knee mechanics during functional tasks. Stearns
et al. reported diminished strength of the hip extensors relative to the knee extensors was associated
with higher knee extensor moments relative to hip extensor moments during a drop jump task.
2

Teng et al. reported that hip extensor strength was inversely correlated to knee extensor work
during running.
3
However, it should be noted that in both of these studies, hip extensor strength
only explained 15-17% of the variation in movement behavior.
Given that muscular strength does not fully account for the variability in lower extremity
movement behavior related to knee injury, it has been proposed that altered motor control may be
contributory.
6,95–97
Evidence in support of this premise is provided by studies that have shown that
altered neuromuscular activation of the gluteus muscles, such as reduced magnitude of muscle
recruitment or a delay in onset timing, is associated with knee injury.
36,37
Furthermore, it has been
40

proposed that increased use of the GM following skill acquisition training, as opposed to
strengthening, underlies the protective effect afforded by injury-prevention training.
6

Transcranial magnetic stimulation (TMS) is a research tool that can quantify the
descending neural drive along the corticospinal pathway. By stimulating specific area of the motor
cortex, motor-evoked potentials (MEPs) can be elicited to gain insight into the level of
corticomotor excitability (CME) of specific muscles.
12
MEPs obtained using TMS procedures
have been used to understand the underlying neural mechanisms of movement execution, such as
feedforward and feedback motor control.
42,43

To date, the CME of specific lower extremity muscles within the context of lower extremity
movement behavior has not been investigated. Given the potential role of GM with respect to
movement behavior associated with knee injury, the purpose of the current study was to evaluate
the extent to which CME of GM, as quantified using transcranial magnetic stimulation (TMS),
underlies use of the hip during a sport specific task. More specifically, we sought to determine
whether CME of GM is predictive of hip joint kinematics and kinetics during the execution of a
challenging single leg movement. We hypothesized that the GM CME would be a significant
predictor of peak hip flexion and the average hip extensor moment during the stance phase of
single leg drop jump.

METHODS
Participants
Thirty-two healthy, active participants between ages of 21 and 36 were recruited for this
study (17 females, 15 males; Table 5-1). To be eligible, participants had to engage in some form
of physical activity for at least 30 min, 2 times a week and be at least 18 years of age. Participants
41

were excluded if they reported a previous history of lower extremity pathology or trauma, or lower
extremity pain during sport or activities of daily living. Additional exclusion criteria included any
“yes” answer on the TMS safety questionnaire indicating if they had metal, electrical, magnetic
implants; a personal or family history of epilepsy; or the possibility of being pregnant.
71

Table 5-1. Participant demographics (Mean ± Standard Deviation)

Female Male p
Age (yr) 26.7 ± 3.4 28.5 ± 5.3 0.264
Height (cm) 163.2 ± 5.5 180.2 ± 5.6 <0.001
Weight (kg) 60.2 ± 7.3 82.2 ± 10.4 <0.001
BMI (kg/m
2
) 22.6 ± 2.82 25.2 ± 1.9 <0.001

Procedures
Prior to initiating testing, participants provided informed written consent as approved by
the Institutional Review Board of the Health Sciences Campus at the University of Southern
California. Participants were asked to keep their daily routine consistent on both testing days
(including caffeine intake). For the TMS procedures describe below, the stimulations were applied
to the primary motor cortex contralateral to the dominant leg (i.e. preferred leg to kick a ball). Hip
kinematics and kinetics during the single leg drop jump were quantified from the dominant leg.
TMS and biomechanical data were obtained during separate testing sessions within one week.
Lower extremity kinematics and kinetics were collected using a three-dimensional motion
analysis system (Qualisys Inc., Gothenburg, Sweden) and a single force plate (AMTI, Newton,
MA, USA). Reflective markers were placed on the following bony landmarks: the distal end of
42

the second toes, first and fifth metatarsal heads, medial and lateral malleoli, medial and lateral
epicondyles of the femurs, greater trochanters, iliac crests, and L5–S1 junction. In addition,
tracking marker clusters with 4 markers mounted on semi-rigid plastic plates were placed on the
lateral surface of the participant’s thighs, shanks, and heel counter of the shoes. A static standing
trial used for calibration purposes was collected to define the segmental coordinate systems and
joint axes. After the static trial, markers on bony landmarks were removed except for those at the
iliac crest and L5–S1 junction. The tracking marker clusters remained on the participants during
testing.
Following the set-up described above, participants were instructed to perform a single-leg
drop jump task. Participants stood with their dominant leg on a 0.2 m platform and were instructed
to hop off the platform, land with their dominant leg on a force plate, and then jump as high as
possible. Five trials were collected.
Before initiating the TMS assessment, EMG signals of GM were collected during a MVIC
for the purposes of (1) providing the target contraction level during the TMS procedure, and (2)
establishing the criteria for the identification of a MEP during motor thresholding. The skin over
the GM was shaved and prepared with alcohol to decrease skin impedance. Surface EMG
electrodes (bipolar Ag/AgCl with 22 mm inter-electrode distance) were placed over the muscle
belly of GM. For GM, the electrode position was the mid-point between the ischial tuberosity and
the mid-point of the greater trochanter and the sacrum.
72
To allow for consistent electrode
placement between testing days, electrode positions were marked with a permanent marker. The
EMG signal was sampled at 5000 Hz and amplified using a gain of 2000.
Following electrode placement, MVIC trials were performed. Participants were positioned
prone with the hips at the edge of a treatment table. The tested leg was positioned in 90° of flexion,
43

45° of hip abduction, and end range of hip external rotation. Participants were instructed to push
simultaneously into hip extension, abduction, external rotation against manual resistance provided
by the examiner for 5 seconds.
73
Verbal encouragement was provided during the MVIC trials to
facilitate a maximum effort. The largest averaged 0.2 s root mean square value of the EMG signal
from the two trials was used as the MVIC value for the TMS procedures described below.
All TMS assessments were performed with a single-pulse magnetic stimulator (MagStim
2002, The Magstim Company Ltd, Whitland, UK) using a 110 mm double cone coil. The
Brainsight Neuronavigation System (Rogue Research Inc, Montreal, Canada) was used to ensure
accurate coil placement during both TMS assessments. Reflective markers were fixed to the
participant’s head and the TMS coil as part of the neuronavigation procedure. Landmarks on the
participants’ head were co-registered using an infrared marker tracking system. The coil position
and orientation were then tracked relative to the positions of these markers on a 3-D reconstruction
of a template magnetic resonance image of the brain.
Stimulations were delivered in the supine position during an active contraction of the GM.
Participants were instructed to “squeeze their buttocks”. During the active contractions, real-time
visual feedback reflecting the root mean square (RMS) averaged amplitude of the EMG signal was
provided. Participants were instructed to match the RMS signal to the target contraction level set
at 20% MVIC. Twenty percent MVIC was chosen as the target value a previous study reported
better reliability of MEPs obtained from an upper extremity muscle during low level contractions
(20-25% MVIC) compared to high level contractions (75-100% MVIC).
74

Prior to active motor thresholding, the optimal coil position on the scalp (i.e. “hotspot”) for
the muscle of interest was identified by systematically delivering stimulations over a 4 cm x 4 cm
44

area lateral to the vertex of the contralateral side of the testing leg. The hotspot was located as the
position on the scalp that elicited the largest and most consistent MEPs.
Following the determination of the hotspot location, active motor thresholding (AMT) was
performed. The active motor threshold (AMT) was determined as the smallest stimulation intensity
that elicited 5 MEPs out of 10 stimulations. A MEP was identified as the TMS-induced EMG
activation that was larger than background activation (>20% MVIC) within 40 ms of the
stimulation.
Following motor thresholding, the IOC procedure was performed. Stimulations were
performed over the hotspot at intensities ranging from 100 to 200% AMT in 10% increments. Ten
stimulations were delivered at each of the stimulator intensities.

Data Analysis
To calculate hip joint kinematics and kinetics, reflective marker coordinates and ground
reaction force data were input into Visual 3D (C-Motion, Germantown, MD) and MATLAB
software (MathWorks, Inc., Natick, MA). Marker trajectories data were low-pass filtered at 10
Hz using a 4
th
order Butterworth filter. The local coordinate systems of the pelvis, thigh, shank,
and foot segments were derived from the standing calibration trial. Joint kinematics were
calculated using Cardan angles with a rotation sequence of flexion/extension, abduction/adduction
and internal/external rotation. Hip kinematics were calculated as the motion of the thigh segment
relative to the pelvis segment.
98
Net joint moments were calculated used inverse dynamics
equations and normalized by body mass. The variables of interest included the peak hip flexion
angle and the average hip extensor moment during the stance phase of the single leg drop jump
task.
45

The average of the peak-to-peak amplitude of the 10 MEPs obtained at each stimulator
intensity of the IOC procedure was calculated. An IOC was obtained by plotting the average MEP
amplitude against its corresponding percentage of AMT. The average slope of the IOC data points
were analyzed using linear regression using the data points from 100% AMT to the maximum
average MEP.
75
The average slope of the regression line was used as the indicator of CME of GM.

Statistical Analysis
Linear regression analysis was used to determine whether the average hip extensor moment
and peak hip flexion (dependent variables) were predicted by CME of GM. First, we tested for the
presence of a CME of GM * sex interaction using a multiple linear regression model. If significant,
we ran separate regression analyses for males and females. All statistical analyses were performed
using PASW statistics 18.0.0 (IBM Corporation, Armonk, NY).

RESULTS
The mean peak hip flexion angle and average hip extensor moment for the participants in
this study were 62.1° ± 14.7° and 1.58 ± 0.4 Nm/kg, respectively. In terms of the regression
analyses, no CME of GM * sex interaction was found for the prediction of the average hip extensor
moment and peak hip flexion angle. Therefore, linear regression equations were derived for males
and females combined. With respect to average hip extensor moment, CME of GM was found to
be a significant predictor (r
2
=0.18, p=0.016; Figure 5-1). In addition, CME of GM was found to
be a significant predictor of the peak hip flexion angle (r
2
=0.20, p=0.01; Figure 5-2).

46

Figure 5-1. Scatterplot of the average IOC slope of GM and the hip extensor moment.

Figure 5-2. Scatterplot of the average IOC slope of GM and the peak hip flexion angle.

47

DISCUSSION
The purpose of the current study was to determine the association between CME of GM
and hip joint kinetics and kinematics during a sport-specific task. Consistent with our hypotheses,
we found that CME of GM was a significant predictor of peak hip flexion and the average hip
extensor moment during a single limb drop jump. Our results indicate that functional use of the
hip extensors is due in part, to descending neural drive of the GM.
As mentioned above, movement behavior characterized by reduced use of the hip extensors
has been linked to various knee injuries.
28,99
Although diminished hip extensor strength has been
shown to be associated with such movement behavior, diminished neural drive of the GM also
appears to be contributory. Our finding of a predictive relationship between descending neural
drive of a specific muscle and its functional use is consistent with a previous study that reported a
relationship between corticomotor excitability of shoulder muscles (i.e. pectoralis and deltoid
muscles) and the intersegmental dynamics of an upper extremity reaching movement.
100
Taken
together, our results add to the body of literature suggesting that CME of specific muscles may
contribute to the modulation of movement behavior.
Despite our finding of the average slope of the IOC being a significant predictor of
functional use of the hip, only 18-20% of the variance of hip kinematics and kinetics could be
explained by CME of GM. It is interesting to note that the variance in movement behavior
explained by CME of GM is similar to studies that evaluated strength as a predictor of movement
mechanics. For example, Stearns et al found the knee to hip strength ratio explained only 17% of
the variation in the knee to hip moment ratio.
2
Similarly, Teng and Powers reported that hip
extensor strength explained only 15% of the variation of knee extensor work during running.
3
The
relatively low level of predictability of movement behavior among studies that have examined
48

measures of muscular strength and neural drive highlights the complexity of attempting to explain
movement behavior from a single construct.
Movement behavior is a complex interaction between neural control, biomechanical
capacity, and task demand. To address our hypothesis related to the motor control aspects of the
drop jump task, we chose the slope of the IOC to quantify excitability of the descending
corticospinal pathway. A larger slope of the IOC represents greater excitability and recruitment
efficiency of a given muscle.
54,56
It should be noted however, that the IOC is affected by multiple
regions along the descending corticospinal motor pathway, and as such, it could not be determined
whether movement behavior as measured in the current study was mediated to a greater extent by
cortical or spinal structures. However, there is evidence to suggest that different phases of the drop
jump maneuver are modulated by different circuits. Taube et al. reported that the spinal
contribution for the soleus muscle was strongest immediately following ground contact and
progressively declined during the stance phase owing to the stretch reflex.
101
In contrast,
supraspinal/cortical contribution for the soleus muscle was higher during the push-off phase.
101
It
is possible that GM follows a similar pattern of modulation, however additional research would be
necessary to clarify this hypothesis.
We speculate that the increased CME of GM in persons who exhibit larger hip extensor
moments and larger peak hip flexion angles may be a reflection of experience-dependent
neuroplasticity. For example, increased CME of GM would be expected in persons who habitually
use the hip extensors to a greater degree during specific tasks. This premise would be consistent
with the known influence of long-term repetition of specific movements in relationship to the CME
of specific muscles in athletes and professional dancers.
89,102,103
For example, enhanced CME of
49

the soleus has been demonstrated in ballet dancers who repetitively perform jump maneuvers
compared with non-dancers.
89

Our results have clinical implications regarding the facilitation of movement behavior to
protect against knee injury. There is preliminary evidence to suggest that motor skill training that
emphasizes functional use of the hip extensors can result in experience-dependent neuroplasticity.
6

In contrast, non-skill training such as muscle strengthening has been reported to elicit no to
minimal changes in CME.
104
While strengthening would be important for building movement
capacity, motor skill training would appear to be required to make use of such capacity through
the facilitation of corticomotor excitability and recruitment efficiency of a given muscle.
The results of our study should be interpreted in light of several limitations. Our IOC
procedure based on single pulse TMS only reflects the summation of the excitatory and inhibitory
neural circuit along the corticospinal pathway originating from the contralateral motor cortex. As
such, the IOC procedure was not able to quantify the influence of intracortical
inhibition/facilitation or/and the contributions from the ipsilateral corticomotor pathway.
Furthermore, we only measured CME of one of the 3 primary hip extensors. It is possible that a
more robust relationship between TMS measures and hip kinematics & kinetics would have been
evident if the CME from other hip extensors (i.e. hamstrings & adductor magnus) were obtained.
Lastly, we only investigated the relationship between GM CME and hip kinematics & kinetics
during a single-leg drop jump. Our results may not extend to other tasks that require varying levels
of hip control such as running and cutting.

50

CONCLUSION
Results of the current study revealed that greater functional use of the hip was associated
with enhanced descending neural drive of GM. Specifically, CME of GM was predictive of the
average hip extensor moment and peak hip flexion during a sport-specific task. The results of the
current study suggest that lower extremity biomechanics may be due, in part, to centrally-mediated
factors.
51

CHAPTER VI :
SUMMARY AND CONCLUSIONS

The purpose of this dissertation was to evaluate the extent to which corticomotor
excitability (CME) of gluteus maximus (GM), as quantified using transcranial magnetic
stimulation (TMS), is predictive of hip extensor strength, and hip kinematics and kinetics during
a sport specific task. To achieve this objective, 3 studies were conducted. The purpose of Chapter
III was to establish the reliability of a method for measuring CME of GM using normalized EMG
intensity as the criterion for identifying MEPs during the motor thresholding procedure. The
purpose of Chapter IV was to compare hip extensor strength and CME of GM between males and
females. A secondary purpose was to determine if CME of GM was predictive of hip extensor
strength. The purpose of Chapter V was to determine whether CME of GM is predictive of hip
joint kinematics and kinetics during the execution of a sports specific task.
The results of Chapter III found that the CME (measured by slopes from IOC fitting
methods and the maximum MEP) of GM and VL exhibited good to excellent reliability (ICCs
ranging from 0.75-0.99). The results of Chapter IV found that when compared to males, females
demonstrate lower peak hip extensor torque (4.42 ± 1.11 vs. 6.15 ± 1.72 Nm/kg/m
2
, p<0.01) and
lower CME of GM (1.36 ± 1.07 vs. 2.67 ± 1.30, p<0.01). CME of GM was a significant predictor
of peak hip extensor torque for both males and females combined (r
2
=0.36, p<0.001, Figure 6-1).
The results of Chapter V revealed that the CME of GM was a predictor of the average hip extensor
moment (r
2
=0.18, p=0.016) and peak hip flexion during a single limb drop jump (r
2
=0.20, p=0.01,
Figure 6-1).
52

Figure 6-1. Summary of dissertation findings

As part of this dissertation, a reliable method to assess CME of proximal lower extremity
muscles was established (Chapter III). Compared to distal lower extremity muscles such us
gastrocnemius and soleus, GM has an anatomical constraint in that it cannot be evaluated with
neurophysiological measurements such as v-wave and H-reflex testing. As such TMS is one of
few measurement techniques that can provide insight into the central influences underlying use of
this muscle.
The established protocol using normalized EMG, instead of the traditional fixed voltage
criteria during motor thresholding procedure can facilitate the comparison of CME between
muscles and individuals. The described protocol is especially important for proximal lower
extremity muscles which the factors unrelated to muscle contraction (ie. the amount of
subcutaneous tissue) could greatly influence the amplitude of the recorded signals through EMG.
The EMG normalization process standardizes the level of contraction during TMS acquisition as
well as provides a consistent criterion for identifying MEP during motor thresholding between
Corticomotor Excitability of Gluteus
Maximus
Hip Extensor Strength Hip Kinematics/Kinetics
r
2
= 0.18-0.20
r
2
= 0.36
53

muscles. The minimal detectable change of the slopes of the input-output curve and maximum
MEP established in Chapter III provide a basis from which the true changes of corticomotor
excitability in response to an intervention or training. The established method in this dissertation
for measuring CME of GM using TMS will extend this research tool to investigate how the central
nervous system modulates various proximal lower extremity muscles.
The neural contribution of muscle force development was confirmed from the results from
Chapter IV. Specifically, the neural drive of GM was moderately associated with hip extensor
strength in that individuals who exhibited greater CEM of GM generated greater hip extensor
torque. It is interesting to note that several studies have reported diminished hip muscle strength
in females compared to males.
2,86
It is possible that centrally mediated factors may play a role in
the sex differences in hip strength. Similar to Chapter IV, the neural component of movement
behavior related to knee injury was confirmed with respect of the results from Chapter V. The
CME of GM was associated with hip kinematics and kinetics during a landing task. Although
cause and effect relationships could not be established based on the study design, it is possible that
chronic disuse of the GM may have resulted in diminished CME of GM.
A common finding of Chapters IV and V was that the amount of the variation of hip
extensor strength and hip kinematics and kinetics that could be explained by CME of GM was
relatively small (range 18-36%). There are several potential reasons for this finding. In this
dissertation, CME of GM was quantified using the IOC generated through a single-pulse TMS
protocol. The IOC procedure based on MEP amplitude provides only a glimpse into the central
nervous control of motor system. The slope of the IOC reflects the summation of the excitability
along the corticospinal tract, however, the single-pulse stimulation for the measurement of CME
were delivered from the primary motor cortex. The TMS outcome measure in this dissertation did
54

not include the corticospinal tracts originated from premotor or supplementary motor area which
were also contributing to the voluntary movement. Furthermore, IOC procedure was not able to
quantify the influence of intracortical inhibition/facilitation and/or the contribution from the
ipsilateral corticomotor pathway or extrapyramidal tracts (i.e. reticulospinal tracts). Moreover,
TMS measurements was obtained during a 20% MVIC with visual feedback which was different
from the MVIC test for muscle strength testing or the single leg drop jump for the hip mechanics
analysis. The outcome measures of CME from a well-controlled condition such as 20% MVIC
may not reflect the modulation of the corticospinal control during the MVIC or single leg drop
jump. Recent studies pointed out the neural control of merely a single muscle may not be an
efficient way for nervous system to manage movement.
105,106
Instead, muscle synergies which
involves coordination among multiple muscles would be reasonable for the nervous system to
manage muscle activations based on demand of the specific functional task.
105,106

When considering the results of Chapter IV and V, CME of GM explained more of the
variation of the hip extensor strength (36%) than hip kinematics and kinetics (18-20%). When the
methods for measurement of hip extensor strength and hip kinematics/kinetics are compared, hip
extensor strength was tested in a relatively static position with the focus on one joint movement
under maximal isometric contraction while hip kinematics/kinetics was tested during a single leg
drop jump with maximal effort to jump height. As a dynamic task, hip kinematics/kinetics during
single leg drop jump was potentially influenced by a more complicated motor program which
incorporated voluntary movement, balance control, coordination of the whole-body segment
movement including upper, lower limbs and the trunk. It is plausible that in addition to the
corticospinal tract which is primarily responsible for voluntary movement, other descending
55

pathways such as the reticulospinal pathway with a role in automatic movement control for
postural adjustments also contributed to the single leg drop jump.
107

IMPLICATIONS FOR REHABILITATION AND INJURY PREVENTION
The results of this dissertation have clinical implications regarding the enhancement of hip
extensor strength and facilitation of movement behavior that may protect against knee injury.
Improving hip muscle strength and hip kinematics is a common treatment goal for knee injury
prevention. The findings of this dissertation highlight the importance of centrally mediated factors
in hip extensor force generation as well as hip kinematics and kinetics. Specifically, enhanced
CME of GM may be beneficial for facilitating hip extensor force development and the use of hip
during functional tasks.
Interventions that utilize techniques to enhance CME of GM may facilitate traditional hip
muscle strengthening as well as hip focused lower extremity training program. The combined
treatment of neural modulation and physical therapy has been applied in neurological
patients.
108,109
Repetitive TMS preceding physical therapy was shown to be optimal to boost
neuroplasticity in chronic stroke patients with motor impairment.
108
The “primed” central nervous
system was able to elevate the effect of functional motor training. The modulation of corticomotor
excitability also may be initiated by a bottom up approach. A previous study has shown that the
CME of GM was enhanced after a 6 days of activation exercise program.
67
The 6 days of activation
exercises would not be expected to induce structural adaptation in the skeletal muscle, however,
the enhanced CME of GM may be able to contribute to improved use of the hip muscular during
sports specific tasks.
In addition to neural modulation, incorporation of motor control/learning principals into
strengthening and neuromuscular training may be beneficial to promote facilitation of CME of
56

GM. For example, the trajectory tracing training with visual feedback provided has been shown to
upregulate CME of upper and lower extremity muscles.
104,110
Adopting an external focus of
attention during finger movements was shown to alter the CME of first dorsal interossei.
111
The
combined interventions emphasis on the facilitation of CME of GM may especially be helpful for
individuals who are not able to engage the hip with traditional treatment or training.

FUTURE DIRECTION
The design of this dissertation was a cross-sectional in nature. As such, cause-effect
relationships could not be determined. Longitudinal intervention studies are necessary to
determine whether the upregulation of CME of GM results in increased hip extensor strength and
improved hip kinematics and kinetics. Additionally, the determination of CME for other hip
muscles such as gluteus medius, hamstring, and adductor magnus and the relationship to lower
extremity movement related to knee injury is necessary. Furthermore, additional study is needed
to determine whether the relationships observed in this dissertation hold true in other functional
tasks and muscles.

57

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Abstract (if available)

Abstract Insufficient use of the hip extensors during sport related activities is thought to be contributory to various knee injuries. Diminished hip extensor strength has been reported to underlie the movement behavior that exposes the knee to excessive loading. In particular, diminished force production of the gluteus maximus (GM) is thought to be problematic as this muscle protects against excessive loading of the knee owing to its multi-planar control of the hip. It has been proposed that centrally mediated neural factors (i.e. diminished neural drive) may be contributory to the diminished strength and movement behavior that underlies knee injury. To date, the corticomotor excitability (CME) of specific lower extremity muscles within the context of lower extremity strength and movement behavior has not been investigated. Given the potential role of GM with respect to movement behavior associated with knee injury, the purpose of this dissertation was to evaluate the extent to which CME of GM, as quantified using transcranial magnetic stimulation (TMS), is predictive of hip extensor strength, and functional use of the hip extensors during a sport specific task. To achieve this objective 3 studies were undertaken. ❧ Because of the methodological challenges associated with the assessment of proximal lower extremity muscles using TMS, the purpose of Chapter III was to establish the reliability of a method for measuring corticomotor excitability of gluteus maximus and vastus lateralis (VL) using a normalized electromyography value as the criterion for identifying motor evoked potentials (MEPs) during the motor thresholding procedure (as opposed to a fixed voltage value). Ten healthy participants were recruited. TMS data were acquired using the input-output curve (IOC) procedure while participants performed an isometric contraction of GM and VL (20% of maximal voluntary isometric contraction). The active motor threshold for each muscle was determined using the lowest stimulator intensity required to elicit 5 MEPs from 10 stimulations that exceeded 20% MVIC. The average and peak slopes of the IOC data points were analyzed using linear regression and sigmoid curve fitting respectively. TMS data were obtained on 2 separate days and compared using random-effect intra-class correlation coefficients (ICCs). Slopes from both IOC fitting methods as well as the maximum MEP of GM and VL were found to exhibit good to excellent reliability (ICCs ranging from 0.75-0.99). ❧ The purpose of Chapter IV was to compare hip extensor strength and CME of GM between males and females. A secondary purpose was to determine if CME of GM is associated with hip extensor strength. Thirty-two healthy individuals participated (15 males and 17 females). CME of GM was assessed using the IOC procedure acquired from transcranial magnetic stimulation (average slope). Hip extensor strength was measured using a dynamometer during a maximal voluntary isometric contraction. One-tailed t-tests were used to compare CME of GM and peak hip extensor torque between males and females. Linear regression analysis was used to determine whether peak hip extensor torque was predicted by GM CME. When compared to males, females demonstrate lower peak hip extensor torque (4.42 ± 1.11 vs. 6.15 ± 1.72 Nm/kg/m², p<0.01) and lower CME of GM (1.36 ± 1.07 vs. 2.67 ± 1.30, p<0.01). CME of GM was a significant predictor of peak hip extensor torque for both males and females combined (r²=0.36, p<0.001). ❧ The purpose of Chapter V was to determine the association between CME of the GM and the kinetics and kinematics of the hip joint during single limb drop jump. Thirty-two healthy individuals (17 females, 15 males) participated. The slope of the IOC obtained from TMS was used to assess CME of GM. The average hip extensor moment and peak hip flexion angle during the stance phase of the single leg drop jump task was calculated. Linear regression analysis was used to determine whether the average hip extensor moment and peak hip flexion were predicted by CME of GM. Results revealed that the slope of the IOC of GM was a significant predictor of the average hip extensor moment (r²=0.18, p=0.016) and peak hip flexion (r²=0.20, p=0.01). ❧ As part of this dissertation, a reliable method to measure CME of GM was established. Based on this method, findings of this dissertation revealed that CME of GM was predictive of both hip extensor strength and functional use of the hip extensors during a sport-specific task. Taken together, findings of this dissertation suggest that hip extensor strength and functional use of the hip extensors may be due, in part, to descending neural drive of GM. Interventions aimed at enhancing CME of GM may be beneficial in enhancing hip extensor strength and promoting movement behavior to protect against knee injury.

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University of Southern California Dissertations and Theses

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Asset Metadata

Creator Shih, Yo (author)

Core Title Corticomotor excitability of gluteus maximus: influence on hip extensor strength and hip mechanics

School School of Dentistry

Degree Doctor of Philosophy

Degree Program Biokinesiology

Publication Date 12/04/2019

Defense Date 07/23/2019

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag brain-behavior relationship,knee injury prevention,motor control,OAI-PMH Harvest,transcranial magnetic stimulation

Language English

Contributor Electronically uploaded by the author (provenance)

Advisor Powers, Christopher M. (committee chair), Fisher, Beth E. (committee member), Kutch, Jason J. (committee member), Salem, George (committee member), Smith, Jo Armour (committee member)

Creator Email yoshih@usc.edu,yoshihpt@gmail.com

Permanent Link (DOI) https://doi.org/10.25549/usctheses-c89-241929

Unique identifier UC11674230

Identifier etd-ShihYo-7982.pdf (filename),usctheses-c89-241929 (legacy record id)

Legacy Identifier etd-ShihYo-7982.pdf

Dmrecord 241929

Document Type Dissertation

Rights Shih, Yo

Type texts

Source University of Southern California (contributing entity), University of Southern California Dissertations and Theses (collection)

Access Conditions The author retains rights to his/her dissertation, thesis or other graduate work according to U.S. copyright law. Electronic access is being provided by the USC Libraries in agreement with the a...

Repository Name University of Southern California Digital Library

Repository Location USC Digital Library, University of Southern California, University Park Campus MC 2810, 3434 South Grand Avenue, 2nd Floor, Los Angeles, California 90089-2810, USA