ARTICLE IN PRESS

Exercise Science and the Vocalist

*Aaron M. Johnson, and †Mary J. Sandage, *New York, New York, and yAuburn, Alabama

Abstract: The application of exercise science training knowledge has been of growing interest to voice professio-
nals. This tutorial, derived from the authors’ invited presentations from the “Exercise and the Voice” Special Ses-
sion at the 2018 Voice Foundation Symposium, proposes a foundational theoretical structure based in exercise
science, clarifies the wide range of variables that may influence voice training, and summarizes our present under-
standing of voice physiology from the perspective of muscle training. The body of literature on voice exercise was
then analyzed from the perspective of this framework, identifying what we currently know and what we still have
yet to learn.
Key Words: Voice physiology−Exercise science−Laryngeal muscles−Vocal training.

INTRODUCTION tutorial, skill acquisition and upregulation of physiological

Individual athletes have unique aptitudes and training needs variables that support extensive muscle engagement will be
that depend on many physiologic-based or performance- described within a theoretical framework for training.
based variables.1 Physiologic variables are related to an Frameworks for voice training that include these exercise
individual’s overall physical condition and include aspects science constructs of upregulation of muscle cellular func-
such as age, sex, overall health, genetic predisposition, and tion, neuromuscular function, and fatigue resistance, will
native muscle fiber type complement. Performance variables guide and shape a trajectory for voice training and provide
are specific to the type of training and include the duration a structure from which empirical studies of voice function
and intensity of the target exercise. These individual differ- can be assessed for strengths and limitations. Evaluating
ences between athletes are framed in established training what has been empirically studied to date is as important as
paradigms within which power, endurance, or mixed train- identifying what is not yet understood in the merger of exer-
ing programs are developed. Occupational voice require- cise physiology and voice training disciplines.
ments differ widely between individuals, even within the
same profession, eg, teachers. Some teachers are required to
EXERCISE SCIENCE COMPONENTS
instruct for shorter periods of time at a high sound intensity
Much of what is currently developed for voice training pro-
level in large spaces with acoustic challenges that must be
grams has been translated from the evidence available for
overcome by a combination of voice technique and amplifi-
limb skeletal muscle and cardiorespiratory fitness. There are
cation. Other teachers may speak to smaller groups in
many aspects of exercise science that play a foundational
smaller spaces over an 8 hour day. Contrasts may also be
role in performance training for the end goals of skill acqui-
drawn within vocal performers. The vocal dose and vocal
sition, fatigue management, and avoidance of injury.
calibration to the room acoustics can vary widely between a
Knowledge of muscle fiber types, bioenergetic profiles and
recital performance and a lead role in an opera. Despite
fatigability of the muscle fiber types in the context of tissue
these individual physiologic and performance differences,
adaptability drives development of sport training pro-
few, if any, voice habilitation and rehabilitation programs
grams.2 Skill acquisition has been well addressed in voice
have been tailored with these differences in mind.
training programs; however, a systemic lack of knowledge
In the field of occupational voice use and training, most
and awareness of muscle fiber types, bioenergetics, neuro-
clinicians and teachers understand the importance of the
muscular development, and tissue adaptability in the con-
specificity of training for targeted skill acquisition that
text of occupational voice use undermines our ability to
results in excellent technique. Less considered aspects of
develop the most effective voice habilitation and rehabilita-
vocal training are the upregulation of muscle bioenergetics
tion programs.
and the development of fatigue resistance to promote injury
prevention and more rapid performance recovery. In this
Muscle fiber types
Accepted for publication September 13, 2019. The two primary types of skeletal muscle fibers throughout
Funding: This work was partially supported by funding from The National Insti-
tute on Deafness and Other Communication Disorders (NIDCD/NIH), grant
the body are type I and type II, differentiated by their con-
K23DC014517 (Johnson, PI). traction speed and fatigability. Type II muscle fibers are the
Declarations of Interest: The authors have no conflicts of interest to declare.
From the *New York University Voice Center, Department of Otolaryngology −
muscle fibers that contribute the most to force production
Head and Neck Surgery, New York University School of Medicine, New York, New and are more fatigable than type I muscle fibers. Except for
York; and the yDepartment of Communication Disorders, Auburn University,
Auburn, Alabama.
the posterior cricoarytenoid muscle (PCA), the intrinsic
Address correspondence and reprint requests to Aaron M. Johnson, New York laryngeal muscles are generally understood to have more
University Voice Center, New York University Langone Health, 345 E. 37th Street,
Suite 306, New York, NY 10016. E-mail: aaron.johnson@nyulangone.org
type II muscle fibers than type I muscle fibers. The greater
Journal of Voice, Vol. &&, No. &&, pp. &&−&& prevalence of type II muscle fibers in the larynx is function-
0892-1997
© 2019 The Voice Foundation. Published by Elsevier Inc. All rights reserved.
ally important for rapid closure of the larynx for airway
https://doi.org/10.1016/j.jvoice.2019.09.007 protection, the primary biological role of the larynx. Type I
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2 Journal of Voice, Vol. &&, No. &&, 2019
muscle fibers are endurance fibers, useful primarily for pos-
tural support and activity that lasts for longer than 3
minutes. The PCA has a greater complement of type I mus-
cle fibers than type II muscle fibers which makes sense given
the PCA’s role in maintaining airway patency.
The extent to which individuals vary with regard to mus-
cle fiber type complement in the intrinsic laryngeal muscles
is not currently well understood.3 It may be that, like limb
skeletal muscles, there are individuals who are genetically
predisposed to a far larger complement of either type I or
type II muscle fiber types, providing physiological support
for vocal performers we would consider as outliers. Outliers
could manifest as either individuals who have little difficulty
with extensive use at one extreme or individuals prone to
voice disorder at the other extreme.
Bioenergetic profiles
Muscle bioenergetics describes the mechanisms and manner
by which muscles are supplied with adenosine triphosphate
(ATP), the primary fuel for muscle contraction and relaxa-
tion. Metabolic pathways include two anaerobic pathways,
the immediate energy system and glycolysis, and one aero-
bic system, oxidative phosphorylation. The energy system is
generally inferred by both the length of time one engages in
muscle activity and the amount of power produced by the
given muscle group.4 While all three metabolic pathways
are “turned on” at the start of muscle work, it is generally
understood in the limb skeletal muscle literature, that the
immediate energy system is depleted first, within the first
few seconds of exercise. Glycolysis is the second metabolic
pathway to be largely depleted, after about 1−2 minutes.
Glycolysis yields about 4 ATP per glucose molecule, mak-
ing it a rapidly accessible but rather inefficient bioenergetic
resource. Athletes who perform ballistic exercise (think
hammer thrower) or perform sprint distances are considered
to be anaerobic athletes.
After 2-3 minutes of exercise, the aerobic pathway, oxida-
tive phosphorylation, begins to provide an efficient means
of ATP production at around 34 ATP per glucose molecule.
Therefore, within the temporal framework of muscle
metabolism, the anaerobic metabolic pathways are largely
depleted within a very short time before the aerobic path-
way predominates. Endurance performance bioenergetically
translates to continuous exercise that lasts longer than 2-3
minutes, depending on how highly trained the muscle tissue,
with faster aerobic production of ATP with a higher fitness
level. In actuality, the three mechanisms work synergisti-
cally, with the aerobic system predominating after 2-3
minutes of continuous exercise, but glycolysis kicking in
should a sudden acceleration of movement be required.4
There is an emerging body of work that has applied the
temporal constructs of bioenergetic substrate utilization to
known voicing “on” and “off” intervals in physical educa-
tion teachers and classroom teachers.5−7 Given that
voiced intervals during connected speech in ecologically
valid contexts, as determined via voice dosimetry, were
overwhelmingly less than 3 seconds in length,5 it has been
hypothesized that the intrinsic laryngeal skeletal muscles
engaged for phonation are largely reliant on anaerobic
metabolism. This observation would be consistent with the
limited cadaver muscle fiber typing evidence indicating a
higher percentage of Type II muscle fibers in the all of the
intrinsic laryngeal skeletal muscles except for the PCA. A
primary reliance on anaerobic pathways for occupational
voice users would signal a particular type of voice training
that would target upregulation, fatigue resistance, and more
rapid recovery of the anaerobic energy systems with the spe-
cific activity of connected speech. Within the context of
accumulated voicing intervals over an entire work day, such
as with classroom teaching or call center support agents, it
may be hypothesized that a mixed athlete profile (anaero-
bic + aerobic) would more accurately account for both the
rapid acceleration and endurance characteristics of the
vocal dose. In this regard, a combined anaerobic/aerobic
muscle metabolism would be proposed.
The actual bioenergetic requirements for voice use is
largely theoretical at the time of this writing and the meta-
bolic profile for the intrinsic laryngeal muscles is not well
understood in vivo. Tellis et al8 used visible light spectros-
copy in vivo to monitor tissue oxygen and relative total
hemoglobin in the thyroarytenoid/lateral cricoarytenoid
(TA-LCA) complex. A decrease in oxygen was observed
during a sustained voicing task. It is difficult to determine
the role of oxygen utilization for production of ATP for this
task because glucose uptake was not concurrently mea-
sured. Without concurrent measurement of glucose utiliza-
tion, it would be impossible to determine if laryngeal
metabolism was primarily anaerobic or aerobic. Nanjundes-
waran, et al9 used well-established gas exchange analysis to
determine oxygen uptake during reading tasks and during
recovery from reading in a between group design, individu-
als describing vocal fatigue, vocally healthy sedentary indi-
viduals, and vocally healthy/cardiovascularly conditioned
participants. No significant differences in oxygen uptake
were identified between the groups. Better understanding of
intrinsic laryngeal skeletal muscle metabolism and adapta-
tions with exercise and detraining will be vital for future
evidenced-based development of voice habilitation and
rehabilitation programs.
Fatigability/fatigue resistance
Fatigue is a complex construct which requires consideration
of both psychological and physiological perspectives. In
some literature this is described as “central” versus “periph-
eral” fatigue.10 In other more recent literature, fatigue is
framed as “perceived” versus “performance” fatigability.11
Both constructs require consideration of the feeling/percep-
tion of fatigue versus the physiological inability to continue
to contract the muscle fibers at the same speed and degree
of force as required for the target behavior. To perceive that
the voice is tired after having used it for a long time is a dif-
ferent construct from having bioenergetic depletion from
 ARTICLE IN PRESS
Aaron M. Johnson and Mary J. Sandage Exercise Science and the Vocalist
Training Adaptations
Variables Neurological
Intensity Morphological
Duration Bioenergetic
Time
FIGURE 1. Exercise science theoretical framework.
extensive engagement of the laryngeal muscles. Quantifica-
tion of vocal fatigue is an ongoing research effort with
voice-related scales such as the Vocal Fatigue Index and the
Evaluation of the Ability to Sing Easily scale now available
for use.12,13 Fatigue has generally been considered a nega-
tive condition and the remedy has generally been cessation
of voice use or voice rest.
There are many idiosyncratic factors that may influence
perception of fatigue for voice tasks that include but are not
limited to the following: health status, prior training and
vocal fitness, self-efficacy, adequate sleep/rest, medication,
environment in which the voice tasks takes place, use of
amplification, etc. The measurement of voice fatigue may
be confounded by fatigue occurring in one or more of the
subsystems required for voicing, ie, respiration, phonation,
and articulation/vocal tract tuning. Additionally, vocal
fatigue has been attributed to changes in the vocal fold
cover resulting from repeated impact forces during voicing,
such as increased tissue viscosity and nonmuscular tissue
strain; however, the evidence to support this has been lim-
ited to theoretical modeling and lacks in vivo support.14
In exercise science performance fatigue is not avoided; it
is planned for and managed through targeted conditioning
programs. When the exercise expectations are known, just
as when the vocal dose and the acoustic requirements are
known, a training program can be designed to upregulate
those physiological processes needed to offset fatigue - what
can be referred to as fatigue management. Merging this exer-
cise construct with voice training programs requires a skill-
ful understanding of the end goal for voice production and
then adequate time and vocal training for the muscle tissue
and motor planning to adapt to the conditions imposed.
Muscle tissue upregulates in many aspects - metabolically,
neurologically, and morphologically - to be more efficient.
The ultimate goal of a fatigue management approach is
more rapid recovery from the vocal load imposed and
avoidance of injury. To date, there has been little differenti-
ation for occupation-specific voice load and, as a result,
many voice professionals are trained in the same way with
little thought put toward a fatigue management plan.
NEUROMUSCULAR TRAINING ADAPTATIONS
The SAID principle
The specific adaptation to imposed demand (SAID) principle
is the foundational framework from which any strength and
3
Outcomes
Skill Acquisition
Fatigue Resistance
Increased Strength
conditioning exercise program is designed for both endur-
ance and ballistic performance goals (Figure 1).15 Muscle
tissue adapts to the demands imposed upon it or the lack of
demand imposed upon it. This plasticity of muscle tissue is
complex and encompasses metabolic, morphologic, and
neurologic aspects of muscle tissue function.
A component of the SAID principle, overload, refers to
the “imposed demand” aspect of the overarching principle.
Overload is achieved when the muscle tissue is challenged
with increased intensity and/or duration of use. This chal-
lenge may be in the form of increased resistance loading,
increased repetition, increased duration of the muscle activ-
ity, or a combination of these factors.
The exercise principle of specificity, indicates that the
muscle will adapt to the activity trained. Specificity is real-
ized via muscle tissue adaptations that encompass motor
learning as well. Training for a specific task allows the
motor plan to be established so that optimal force and speed
of motion are achieved for the target behavior. For exam-
ple, the velopharyngeal closure differs between speech tasks
and other nonspeech tasks, such as blowing, sucking, etc.
Even within non-nasal consonant targets, the degree of velo-
pharyngeal closure differs, with more forceful and longer
closure for the /s/ phoneme than /p/.16
A final concept to consider within the larger framework
of the SAID principle is reversibility. If the muscle is not reg-
ularly challenged at the same (maintenance) or greater
(overload) degree, then the trained adaptations will downre-
gulate or reverse in order for the muscle tissue to achieve a
different level of homeostasis.
Applied to voice function, vocal training should be
designed in a manner that steadily imposes enough of a
demand on the physiology that the individual can achieve
the target performance level without overdoing it and risk-
ing injury. The type of demand imposed should match the
vocal requirements of the goal behavior. For example, prep-
aration for a recital should be different than training for
work as a classroom teacher. Analysis of these two different
scenarios has indicated that while the overall vocal dose
may be similar in distance, the dose is achieved over differ-
ent time spans and using a different average sound level.17
Sex & age considerations
Muscle morphology and response to exercise will differ
between most men and women. Women realize measurable
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4 Journal of Voice, Vol. &&, No. &&, 2019
muscle strength gains through both neuromuscular mecha-
nisms and hypertrophy, with a greater reliance on the for-
mer. Younger men will realize strength gains primarily
through muscle hypertrophy. In old age, men have a shift
toward neuromuscular mechanisms for strength gains with
less reliance on muscle hypertrophy. Lenell et al18 provides
a comprehensive review of the effects of sex hormones on
laryngeal muscle senescence.
Training adaptations in the muscles of voice
production
Exercises to increase strength and endurance of the limb
muscles have been extensively studied in the traditional exer-
cise physiology literature. Applying these findings to the
muscles of voice production presents several challenges. Voice
production is a complex, sensorimotor activity that requires
the coordination of three major subsystems: the respiratory,
phonatory, and resonating/articulatory systems. Many of the
respiratory, laryngeal, and cranial muscles that coordinate to
produce voice are functionally and microstructurally distinct
from the larger limb muscles.19 Little is known about neuro-
muscular adaptations of these muscles in response to training,
partially due to the difficulty in measuring the strength and
endurance of these muscles in vivo in humans. Furthermore,
the targets of vocal exercises and training are not typically to
increase muscle strength or endurance, but to improve vocal
function (eg, increase vocal range, improve vocal quality).
Improving vocal function likely depends on changing the
muscle activation in multiple subsystems and changing how
these subsystems coordinate. Therefore, it is difficult to study
specific neuromuscular adaptations underlying changes in
vocal function resulting from the simultaneous training of
these subsystems. Each of the vocal subsystems has been stud-
ied in isolation relative to specific neuromuscular deficits, giv-
ing some insight into the capability for training to improve
each individual subsystem.
Respiratory muscles
In typical voice production there is more than sufficient
strength and endurance of the respiratory muscles to pro-
duce voice. In voice therapy or singing training, coordina-
tion of respiratory muscles with the phonatory system is
often the goal rather than muscle strengthening. The capac-
ity for increasing respiratory muscle strength has been dem-
onstrated in respiratory muscle strength training (RMST)
programs for individuals who have compromised respira-
tory muscle strength due to a neurological injury, such as
stroke.20 RMST targets either the inspiratory or expiratory
muscles using a valved device to introduce a resistance dur-
ing inspiration or exhalation. Direct measurement of the
strength of the respiratory muscles is not possible in vivo.
Therefore, respiratory muscle strength is indirectly quanti-
fied by measuring changes in pulmonary function parame-
ters such as peak expiratory flow rate and maximum
expiratory or inspiratory pressures. This is a reasonable
approach given that increased respiratory muscle
engagement during these maneuvers has been shown using
electromyography.21
The evidence for building respiratory muscle strength is
strong; however, generalization of these proposed strength
gains to improvements in voice production remains
unknown.20 Analyzing respiratory muscle training through
the lens of exercise science training principles indicates a
mismatch with regard to the specificity of this training for
improved voice function. During the RMST tasks, phona-
tion is not coordinated with the isolated respiratory muscle
exercise. Therefore, RMST is a good example of a program
that is intended to build strength of respiratory muscles
which, as a subsystem of voice, could improve voice produc-
tion for specific individuals with respiratory muscle weak-
ness but may not be a necessary component of voice
habilitation or rehabilitation.22
More relevant for voice production is improved respiratory
muscle endurance to reduce fatigue or improve vocal perfor-
mance during extended periods of voicing, such as singing or
sustained speaking (eg, teaching, lecturing). Respiratory mus-
cle endurance can be trained in patients with conditions that
restrict respiration, such as chronic pulmonary obstructive
disease.23,24 In these cases, respiratory muscle endurance was
measured by calculating maximum voluntary ventilation, a
pulmonary function task. Maximum voluntary ventilation is
the total volume of air a person can inhale and exhale over a
certain amount of time, typically 12 seconds. In voicing,
increasing the duration of sustained exhalation may be of
more interest than increasing ventilatory capacity. Although
maximum phonation time has been used extensively as a sur-
rogate measure of laryngeal aerodynamic efficiency, no spe-
cific task targeting respiratory muscle endurance during
voicing has been established.
Muscles of the vocal tract
The muscles surrounding the vocal tract contribute to reso-
nance and articulation during voicing by changing the vocal
tract’s shape and length. Similar to the respiratory muscles,
typical voicing does not likely require greater than normal
strength and endurance of the muscles of the vocal tract.
Tongue strength during running speech has not been quanti-
fied; however, tongue strength measurement during swallow-
ing, a pressure-generating task, has shown that only one-third
to one-half of the maximum voluntary tongue strength is
engaged during swallowing depending on age.25 Additionally,
difficulty with articulatory precision does not necessarily cor-
relate with articulatory muscle weakness. In a study measur-
ing tongue strength in children, there was no difference in
tongue strength between children with an idiopathic speech
sound disorder and age- and sex-matched peers with typically
developing speech.26 However, that same study demonstrated
that children with a motor speech disorder did have decreased
tongue strength relative to children with either typically devel-
oping speech or a speech sound disorder.
The rapid, fine motor muscular movements needed for
articulation and resonance adjustments are best trained
 ARTICLE IN PRESS
Aaron M. Johnson and Mary J. Sandage Exercise Science and the Vocalist
(and treated when a deficit is present) by speech and voice
tasks, not by gross motor, nonspeech exercises.27 In con-
trast, swallowing is a gross motor function of the vocal tract
muscles and, as such, oropharyngeal muscle weakness is
assumed to be a significant contributor to oropharyngeal
dysphagia. Strengthening exercises for the muscles of the
vocal tract, with particular focus on the tongue, have been
developed to treat oropharyngeal dysphagia.
The tongue is a complex muscular hydrostat, consisting
of four intrinsic muscles and five extrinsic muscles.28 It is
the most mobile and versatile muscular structure that deter-
mines the size and shape of the vocal tract. It is also the pri-
mary component for articulatory postures and formant
tuning, responsible for producing the formant locations of
vowels and the constrictions necessary for most consonants
other than bilabial, labiodental, and glottal consonants.
Studies of tongue strengthening exercises in the context of
dysphagia rehabilitation have shown it is possible to
strengthen the tongue muscles with training.29 Tongue
strength can be assessed using devices that measure the pres-
sure generated by pushing different portions of the tongue
against a pressure transducer, such as the Iowa Oral Perfor-
mance Instrument and the Madison Oral Strengthening
Therapeutic device.30,31 These devices have also been used
to provide feedback during tongue strengthening programs
for patients with dysphagia.
Similar to measuring muscle strength in RMST, these
tongue devices measure performance of a group of muscles
and do not provide direct strength measurements of individ-
ual muscles. Also similar to RMST, these tongue training
exercises are not likely useful in vocal training unless an
individual has known tongue muscle weakness. Presently,
the neuromuscular adaptations to tongue strengthening
exercises are unable to be directly assessed in humans.
Interestingly, there is evidence that endurance and strength
of the tongue are correlated with particular types of physical
activity. For example, in a study of tongue strength in differ-
ent types of athletes, it was shown that weightlifters had
greater tongue strength than did runners, while runners had
greater tongue endurance than weightlifters.32 It may be that
endurance athletes, such as runners, have an innate muscle
fiber type composition throughout their body that predicates
their affinity for endurance exercises, while the contrary may
be true for athletes who excel at ballistic activities. Alterna-
tively, muscle fiber type composition in the tongue may shift
with specific types of training. For example, weightlifters
often rely on the Valsalva maneuver which would engage
the tongue musculature and, theoretically, increase its
strength. Further study is needed to understand these
potential relationships between general physical exercise
and the muscles voice production.
Laryngeal muscles
Sustaining a vowel at a constant pitch and loudness is a task
often used to clinically evaluate vocal fold vibration, either
through direct observation via endoscopy or indirectly
5
through auditory-perceptual or acoustic analysis. During
this task the laryngeal muscles adduct the vocal folds and
maintain a constant longitudinal tension. During more typi-
cal use, such as conversational speech, the intrinsic laryn-
geal muscles rapidly adduct and abduct the vocal folds to
create voiced and voiceless phonemes and continuously
adjust vocal fold tension to change pitch. The very fast
speed and small size of the laryngeal muscles makes them
phenotypically unique from the larger limb muscles. They
have more in common with other muscles in the body that
require fast, fine motor adjustments, such as the extraocular
eye muscles that rapidly adjust the position of the eye or the
muscles that precisely move the fingers to allow us to type
or play the piano. Therefore, it is difficult to confidently
apply exercise physiology knowledge from the limb muscles
to the laryngeal muscles.
As with the muscles of respiration and the vocal tract,
specifically targeting strength and endurance of the laryn-
geal muscles is not typically a target of vocal training. How-
ever, lack of laryngeal muscle strength and tonicity are
relevant concepts in the context of hypofunctional voice dis-
orders. For example, laryngeal muscle atrophy (loss of size
and strength) is thought to be the primary cause of presby-
phonia, a voice disorder related to advanced age. The evi-
dence for behavioral interventions to treat presbyphonia is
emerging but promising.33 Three approaches that have
yielded promising results are Vocal Function Exercises,
Phonation Resistance Training Exercise, and the Lee Silver-
man Voice Treatment.34−36 Each of these three interven-
tions incorporates one or more maximal vocal function task
(ie, maximum phonation time, maximum frequency, or
maximum intensity). These maximum function tasks do not
likely require maximum activation of the laryngeal muscles,
as would a maximum strength exercise applied to the limb
muscles. Laryngeal muscle contraction is much greater in
nonvocal activities such as swallowing or the Valsalva
maneuver. However, these maximum vocal function tasks
engage the laryngeal (and likely respiratory) muscles at lev-
els greater than that required for most voicing tasks, which
may result in improved function and neuromuscular adap-
tations via the principles of overload and specificity. As with
the respiratory and lingual muscles, these neuromuscular
mechanisms are difficult, if not impossible, to study in
humans in vivo.
Animal models of vocal exercise
Animal models provide direct access to the muscles that are
difficult or impossible to investigate in humans in vivo,
allowing direct investigation of the neuromuscular mecha-
nisms underlying vocal exercise.37 Additionally, animal
models allow us to examine neuromuscular training
response in both diseased and normal, noninjured states.
Although animal models have long been used to investigate
voice physiology, biology and biomechanics, there is limited
work using animal models to research neuromuscular
response to training or exercise.37 Two key challenges to
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6 Journal of Voice, Vol. &&, No. &&, 2019
this type of study are the differences in animal vocalization
mechanics and behaviors relative to human vocalizations,
and the difficulty in training animals to vocalize in a manner
that adequately represents human vocal training.
Investigation of neuromuscular responses to training
requires methodology to target the specific muscle(s) of inter-
est. This targeting has been accomplished in exercise models
of the animal vocal subsystems using three methods: resis-
tance loading, neuromuscular electrical stimulation (NMES),
and behavioral training. Resistance loading increases the
amount of work a muscle or set of muscles must do to achieve
a functional result. For example, muscle hypertrophy can be
induced in the limbs through compensatory overload in one
muscle after denervating or otherwise ablating a synergistic
muscle. NMES simulates exercise by electrically stimulating
the target muscles without the need for behavioral training.
The stimulation is applied directly to the nerve supplying the
target muscles which consequently mimics voluntary muscle
contraction, absent the motor planning component that
would be present in volitional muscle engagement. Behavioral
training uses operant conditioning to train animals to produce
a target behavior for a reward. The target behavior activates
the muscles of interest and can be trained to progressively
increase engagement of these muscles over time. Rewards in
these behavioral paradigms are typically food or water and
require the animals be motivated for the reward. Examples of
these approaches can be found in each vocal subsystem.
Animal models of respiratory muscle exercise
Resistance loading has been used to examine respiratory
muscle exercise in both rat and sheep models.38,39 In con-
trast to human studies, in which airway resistance is intro-
duced using an external device, in an animal model resistive
loading to the inspiratory or expiratory muscles can be
achieved by creating an upper airway obstruction with a tra-
cheal cannula. This obstruction increases the respiratory
muscle engagement needed to maintain ventilation. Results
using this model demonstrated an interesting mix of adapta-
tions consistent with both strength training, such as
increased mass of the diaphragm (muscle hypertrophy), and
endurance training, as evidenced by an increase in GLUT-4
protein and the proportion of Type I (fatigue resistant)
fibers. Therefore, the neuromuscular response of the respira-
tory muscles to exercise appears to be a hybrid response of
the traditional categories defined in the limb muscles,
highlighting the need for direct study of individual muscles
and muscle groups within the vocal subsystems rather than
extrapolating findings from the limb muscles.
Animal models of tongue muscle exercise
NMES of the tongue muscles via stimulation of the hypo-
glossal nerve activates all of the intrinsic and extrinsic
tongue muscles except for the palatoglossus muscle. Daily
NMES of the rat tongue for 8 weeks resulted in increased
fatigue resistance of the extrinsic tongue muscles, greater
twitch and tetanic forces, and, in general, a shift to more
fatigue-resistant muscle fiber types.40 Additionally, the rela-
tionship of the pre/post synaptic morphology in the neuro-
muscular junctions (NMJ) of the genioglossus muscle
changed with NMES, implicating possible improved synap-
tic efficiency.41
A caveat to use of NMES as a model of exercise is that it
differs from voluntary muscle contraction in two important
ways. First, the intensity of nerve stimulation in NMES
studies often results in supramaximal contraction of the
stimulated muscles (ie, greater intensity than what is possi-
ble with voluntary contraction). Second, NMES lacks the
element of motor planning and execution that is a feature of
skill acquisition to match muscle fiber engagement to task
requirements. Therefore, NMES informs us of the potential
neuromuscular response of muscle(s) to activation, but
translating that response to human behavior is tempered by
these aspects that reduce ecological validity.
The behavioral training model has also been applied to
the rat tongue using a resistance licking paradigm in which
water restriction was used to motivate rats to lick against a
force transducer for a water reward. The amount of licking
force necessary for the reward progressively increased over
8 weeks, thereby modeling a progressive resistance exercise
program. This paradigm resulted in increased tongue forces
and shifts in muscle fiber types in the intrinsic tongue
muscles from slow to fast or fast to slow, depending on the
muscle region.42,43 Tongue exercise did not increase muscle
fiber size in the intrinsic tongue muscles, but did result in a
trend toward larger cross-sectional muscle fiber area of the
genioglossus muscle, the primary protrusive extrinsic tongue
muscle used for licking. Although this program trains a pro-
trusive tongue maneuver which is not a typical action in
human speech or swallowing, it is a meaningful, functional
task for the rat and, therefore, may represent (relative to
NMES) a more homologous task to human tongue exercise.
Similar to the goals of human investigations of tongue
exercise, the motivation for these animal models is to under-
stand mechanisms underlying dysphagia treatments.
Although, relative to swallowing, the tongue muscles con-
tract at lower intensities during speech, these basic science
investigations help us understand the unique and complex
ways in which the tongue muscles respond to increased use.
Animal models of laryngeal muscle exercise
The laryngeal muscles are difficult to study due to their
small size, relative inaccessibility, and specialized function.
Both NMES and behavioral training have been used to
investigate the neuromuscular response of the intrinsic
laryngeal muscles to increased use.
Using an NMES rat model, McMullen et al44 stimulated
the recurrent laryngeal nerve at a supramaximal level for
2 hours/day for 1 or 2 weeks. Following either dose of
NMES, the TA muscle did not hypertrophy but changes in
NMJ morphology and mitochondria were consistent with
endurance training. These results could be explained by
either the duration or the intensity of the NMES protocol.
 ARTICLE IN PRESS
Aaron M. Johnson and Mary J. Sandage Exercise Science and the Vocalist
Early (within the first month) neuromuscular adaptations to
exercise are typically neural, not hypertrophic, whereas the
duration of NMES was either 1 or 2 weeks. The intensity of
the NMES was supramaximal, which may have not allowed
the muscles to fully recover between sessions, thereby forc-
ing the muscles to become more reliant on aerobic path-
ways. The length of time the muscle contraction was
activated was aligned with reliance on aerobic metabolism
which is not typically associated with muscle hypertrophy.3
In contrast, Karbiener et al45 demonstrated intrinsic
laryngeal muscle hypertrophy in an NMES sheep model.
Their NMES protocol stimulated the recurrent laryngeal
nerve for only 2 minutes each day for an overall duration of
29 days. Instead of using an intensity that resulted in supra-
maximal contraction of the muscles, they stimulated the
muscles with enough intensity to fatigue the adductory
muscles, as quantified functionally. Using a balloon catheter
to measure the laryngeal adductory pressure, they experi-
mentally determined the NMES parameters (intensity,
duration, etc) that resulted in muscle fatigue, as measured
by decreased adductory pressure over time. This combina-
tion, 4 weeks of daily sessions of short sets (2 minute) of
muscle contractions leading to fatigue, is consistent with the
parameters of strength training paradigms in the limb
muscles and, therefore, the resulting hypertrophy in the TA
is an expected neuromuscular adaptation. This adaptation
is consistent with the hypertrophy observed in type II skele-
tal muscles that occurs secondary to shorter duration muscle
efforts.3
NMES protocols for stimulating laryngeal muscles using
either supramaximal or functional fatigue offer controlled
ways of measuring muscle contraction. In contrast, behav-
ioral models offer less precise control over individual muscle
contractions but are more homologous to human vocal
training. The only behavioral animal model of vocal train-
ing currently used to investigate the laryngeal neuromuscu-
lar adaptations to vocal exercise is training rats to increase
their production of ultrasonic vocalizations (USVs). Despite
the different final acoustic output between human vocaliza-
tions and rat USVs, the laryngeal muscle activity during the
production and modulation of each type of vocalization is
quite similar. Laryngeal EMG in awake, vocalizing rats,
showed that both the thyroarytenoid and cricothyroid
muscles are active during USV frequency modulation, dem-
onstrating that both human and rat USVs require fine
motor control of the laryngeal musculature.46 An important
difference between human vocalizations and USVs is that
USVs appear to be produced via an edge-tone whistle mech-
anism created by an air jet through a narrowed glottis, not
vocal fold vibration.47 This mechanistic difference is actu-
ally an advantage of this model; training production of
USVs can increase activation of the intrinsic laryngeal
muscles regulating vocal fold adduction and elongation
without concern for inducing phonotrauma in the superfi-
cial vocal fold layers.
There are two studies using this model that have demon-
strated neuromuscular adaptations within the TA muscle of
7
both the young and old rat larynx in response to vocal train-
ing.48,49 After 8 weeks of daily vocal training with progres-
sively increasing the target number of USVs each week, age-
related changes in NMJ morphology were reduced. This was
the first evidence from a behavioral animal model that vocal
exercise could ameliorate age-related changes in laryngeal
neuromuscular mechanisms. In this study the behavioral
training target (number of USVs produced per session) was
the same across all animals, regardless of individual perfor-
mance or age. In the next study using this model, the training
goals were individualized for each animal, resulting in much
higher targets.49 Both the NMJ and muscle fiber size were
examined in the TA of young rats after 4 or 8 weeks of train-
ing. Similar to the first study, adaptations of NMJ morphol-
ogy were seen after only 8 weeks, but not 4 weeks. No muscle
hypertrophy was observed at either time point. It is likely that
the functional loads created by USV training are, therefore,
inadequate to induce hypertrophy, which is in contrast to the
maximal contractions induced by NMES. Further study of
behavioral USV training is required to understand the func-
tional consequences of the changes in NMJ morphology.
MODEL OF MUSCULAR ACTIVATION DURING
VOCALIZATION
In its broadest sense, the goal of vocal exercise is to improve
the coordination of the three vocal subsystems (respiration,
phonation, and resonance), whether the context is voice
therapy for dysphonic individuals or vocal training for vocal
athletes. As such, vocal exercise is ultimately fine motor skill
training. This hypothesis begs the question, are the concepts
of muscle strength or fatigue resistance relevant to vocal
training? That is, do any of the considerations outlined in
this exercise science tutorial actually matter when it comes
to training the voice? In typical day-to-day voice use, they
probably do not. Successful vocalization for typical speech
communication does not require greater than homeostatic
engagement of the respiratory, laryngeal, or articulatory/
resonatory muscles.
However, in a compromised system (eg, stroke, muscle
tension dysphonia) or during athletic voice use (eg, singing,
preaching, teaching), the muscles of voice production
require training and, therefore, the principles of exercise sci-
ence are relevant and critical to consider. Consider the
SAID principle and the theoretical construct presented in
Figure 1. Where does vocalization fall in the continuum of
endurance to strength training? Strength training focuses on
strengthening a specific muscle or groups of muscles. As dis-
cussed above, it is difficult to isolate the muscles of voice
production. Instead, vocalization can be thought of as a
coordinated, repetitive sequence of muscle activation and
deactivation, similar to a mixed athlete that requires both
endurance and ballistic components. Cyclists require endur-
ance for rides longer than 3 minutes and also require sudden
bursts of strength to make it up a hill. Vocalists may also
require both endurance and sudden changes in acceleration
to meet occupational vocal demands.
 8
ARTICLE IN PRESS
Journal of Voice, Vol. &&, No. &&, 2019
FIGURE 2. Model of neuromuscular coordination during vocalization of (A) a spoken utterance and (B) a sustained sung phrase.
 ARTICLE IN PRESS
Aaron M. Johnson and Mary J. Sandage Exercise Science and the Vocalist
Figure 2 presents a model of the cyclical coordination of
muscle activation in each vocal subsystem required to pro-
duce (A) a sentence commonly used in voice evaluation and
(B) a sustained sung phrase. Three phases of vocalization are
delineated: inhalation, prephonatory setup, and phonation.
The figure represents the sequence of the phases, whereas the
precise timing of the phases can vary greatly depending on
the communicative context and individual differences. For
example, the pre-phonatory setup phase is generally quite
short, but is presented in Figure 2 largely enough to ease
visual representation. Additionally, the figure is meant to be
an overview of the coordination of the vocal subsystems, not
a detailing of all muscles involved in speech and voice. For
example, for review of the complexity of passive and active
respiratory forces involved in speech and singing, please see
the seminal work by Hixon, Hoit and colleagues.50−52
To summarize the cycle: The muscles within and across
each subsystem must (1) coordinate to inhale a sufficient
amount of air for the planned utterance, (2) set the initial
laryngeal and articulatory position to begin the utterance,
(3) rapidly adjust throughout the utterance to meet the
respiratory, phonatory, and articulatory demands of each
phoneme while modulating the pitch and intensity of the
voice for the appropriate prosody of the intended message.
The cycle repeats with each new utterance, sometimes
immediately, such as in a lecture or performance situation,
or with a delay, as during turn-taking in a conversation.
This repetitive, low-load cycle during typical conversa-
tional speech does not tax the muscles to the point of
fatigue. If, however, the vocal load (intensity or duration) is
increased, the neuromuscular load also increases and neuro-
muscular fatigue may ensue. Additionally, if muscle
strength or endurance is comprised due to illness or disease,
the cycle may be disrupted or other muscles may engage in
an attempt to compensate, thus altering the cycle and possi-
bly disrupting communication. In either situation (increased
vocal load or comprised muscle function), vocal training
based on the principles of exercise science can be used to
restore or habilitate the desired vocal output.
FUTURE DIRECTIONS
To date, the application of exercise science physiology and
training principles to vocal function has been pursued with
great enthusiasm; however, many of our current beliefs
about voice function and vocal training lack evidence.
From this tutorial, it is clear that translation of the evidence
from limb skeletal muscle physiology is insufficient for our
understanding of the muscles used for vocal function. The
frameworks that are well developed in exercise science may
serve as a starting place to develop investigations targeting
both basic and applied aspects of voice physiology. Future
investigations should pursue a thorough understanding of
intrinsic laryngeal skeletal muscle fiber typing and metabo-
lism, neuromuscular responses to voice exercise within the
contexts of age and sex differences, and laryngeal muscle
response to extensive voice rest and reduced use. Identifying
9
the physiological, neurological, and psychological aspects
of vocal loading and voice fatigue in models that mimic
human vocalizations loads will provide the foundation
needed for applied research. Applied research will be benefi-
cial to create a framework from which voice habilitation
and rehabilitation programs may be developed and evalu-
ated for efficacy.
Acknowledgments
The authors would like to thank The Voice Foundation and
Nancy Solomon, Ph.D. for the invitation to submit this
work, based on the authors’ invited lectures on Exercise and
the Voice at The Voice Foundation’s 47th Annual Sympo-
sium: Care of the Professional Voice on June 1, 2018, in
Philadelphia, Pennsylvania.
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