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J Voice. Author manuscript; available in PMC 2022 May 01.
Published in final edited form as:
J Voice. 2021 May ; 35(3): 376–385. doi:10.1016/j.jvoice.2019.09.007.
Exercise Science and the Vocalist
Aaron M. Johnson1, Mary J. Sandage2
1New
York University Voice Center, Department of Otolaryngology – Head and Neck Surgery,
New York University School of Medicine, New York, New York
2Department
of Communication Disorders, Auburn University, Auburn, Alabama
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Abstract
The application of exercise science training knowledge has been of growing interest to voice
professionals. This tutorial, derived from the authors’ invited presentations from the “Exercise and
the Voice” Special Session 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 understanding 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.
Keywords
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voice physiology; exercise science; laryngeal muscles; vocal training
1. Introduction
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Individual athletes have unique aptitudes and training needs that depend on many
physiologic-based or performance-based variables.1 Physiologic variables are related to an
individual’s overall physical condition and include aspects such as age, sex, overall health,
genetic predisposition, and native muscle fiber type complement. Performance variables are
specific to the type of training and include the duration and intensity of the target exercise.
These individual differences between athletes are framed in established training paradigms
within which power, endurance, or mixed training programs are developed. Occupational
voice requirements differ widely between individuals, even within the same profession, e.g.,
teachers. Some teachers are required to instruct for shorter periods of time at a high sound
intensity level in large spaces with acoustic challenges that must be overcome by a
combination of voice technique and amplification. Other teachers may speak to smaller
Correspondence to Aaron M. Johnson, New York University Voice Center, New York University Langone Health, 345 E. 37th Street,
Suite 306, New York, NY 10016, aaron.johnson@nyulangone.org.
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Declarations of interest: The authors have no conflicts of interest to declare.
Johnson and Sandage
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groups in smaller spaces over an eight hour day. Contrasts may also be drawn within vocal
performers. The vocal dose and vocal calibration to the room acoustics can vary widely
between a recital performance and a lead role in an opera. Despite these individual
physiologic and performance differences, few, if any, voice habilitation and rehabilitation
programs have been tailored with these differences in mind.
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In the field of occupational voice use and training, most clinicians and teachers understand
the importance of the specificity of training for targeted skill acquisition that results in
excellent technique. Less considered aspects of vocal training are the upregulation of muscle
bioenergetics and the development of fatigue resistance to promote injury prevention and
more rapid performance recovery. In this tutorial, skill acquisition and upregulation of
physiological variables that support extensive muscle engagement will be described within a
theoretical framework for training. Frameworks for voice training that include these exercise
science constructs of upregulation of muscle cellular function, neuromuscular function, and
fatigue resistance, will guide and shape a trajectory for voice training and provide a structure
from which empirical studies of voice function can be assessed for strengths and limitations.
Evaluating what has been empirically studied to date is as important as identifying what is
not yet understood in the merger of exercise physiology and voice training disciplines.
2. Exercise Science Components
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Much of what is currently developed for voice training programs has been translated from
the evidence available for limb skeletal muscle and cardiorespiratory fitness. There are many
aspects of exercise science that play a foundational role in performance training for the end
goals of skill acquisition, fatigue management, and avoidance of injury. Knowledge of
muscle fiber types, bioenergetic profiles and fatigability of the muscle fiber types in the
context of tissue adaptability drives development of sport training programs.2 Skill
acquisition has been well addressed in voice training programs; however, a systemic lack of
knowledge and awareness of muscle fiber types, bioenergetics, neuromuscular development,
and tissue adaptability in the context of occupational voice use undermines our ability to
develop the most effective voice habilitation and rehabilitation programs.
2.1.
Muscle Fiber Types
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The two primary types of skeletal muscle fibers throughout the body are Type I and Type II,
differentiated by their contraction speed and fatigability. Type II muscle fibers are the
muscle fibers that contribute the most to force production and are more fatigable than Type I
muscle fibers. Except for the posterior cricoarytenoid muscle (PCA), the intrinsic laryngeal
muscles are generally understood to have more Type II muscle fibers than Type I muscle
fibers. The greater prevalence of Type II muscle fibers in the larynx is functionally important
for rapid closure of the larynx for airway protection, the primary biological role of the
larynx. Type I muscle fibers are endurance fibers, useful primarily for postural support and
activity that lasts for longer than 3 minutes. The PCA has a greater complement of Type I
muscle fibers than Type II muscle fibers which makes sense given the PCA’s role in
maintaining airway patency.
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The extent to which individuals vary with regard to muscle 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.
2.2.
Bioenergetic Profiles
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Muscle bioenergetics describes the mechanisms and manner by which muscles are supplied
with adenosine triphosphate (ATP), the primary fuel for muscle contraction and relaxation.
Metabolic pathways include two anaerobic pathways, the immediate energy system and
glycolysis, and one aerobic 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, making 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.
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After 2-3 minutes of exercise, the aerobic pathway, oxidative 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 pathway
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 synergistically, 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
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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 education 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 specific 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
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agents, it may be hypothesized that a mixed athlete profile (anaerobic + 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.
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The actual bioenergetic requirements for voice use is largely theoretical at the time of this
writing and the metabolic profile for the intrinsic laryngeal muscles is not well understood in
vivo. Tellis, et al.8 used visible light spectroscopy 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 measured. Without concurrent measurement of glucose utilization, it would
be impossible to determine if laryngeal metabolism was primarily anaerobic or aerobic.
Nanjundeswaran, et al.9 used well-established gas exchange analysis to determine oxygen
uptake during reading tasks and during recovery from reading in a between group design,
individuals describing vocal fatigue, vocally healthy sedentary individuals, 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 adaptations with exercise and detraining will be vital for
future evidenced-based development of voice habilitation and rehabilitation programs.
2.3.
Fatigability/Fatigue Resistance
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Fatigue is a complex construct which requires consideration of both psychological and
physiological perspectives. In some literature this is described as “central” versus
“peripheral” fatigue.10 In other more recent literature, fatigue is framed as “perceived”
versus “performance” fatigability.11 Both constructs require consideration of the feeling/
perception 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 different construct from having
bioenergetic depletion from extensive engagement of the laryngeal muscles. Quantification
of vocal fatigue is an ongoing research effort with voice-related scales such as the Vocal
Fatigue Index (VFI) and the Evaluation of the Ability to Sing Easily (EASE) scale now
available for use.12,13 Fatigue has generally been considered a negative condition and the
remedy has generally been cessation of voice use or voice rest.
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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, i.e., 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 non-muscular tissue strain; however, the evidence to
support this has been limited 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
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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 exercise construct with voice training
programs requires a skillful 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 differentiation 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.
3. Neuromuscular Training Adaptations
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3.1.
The SAID principle
The specific adaptation to imposed demand (SAID) principle is the foundational framework
from which any strength and conditioning exercise program is designed for both endurance
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.
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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 challenge may be in the form of increased
resistance loading, increased repetition, increased duration of the muscle activity, or a
combination of these factors.
The exercise principle of specificity, indicates that the muscle will adapt to the activity
trained. Specificity is realized 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 example, the
velopharyngeal closure differs between speech tasks and other non-speech tasks, such as
blowing, sucking, etc. Even within non-nasal consonant targets, the degree of
velopharyngeal closure differs, with more forceful and longer closure for the /s/ phoneme
than /p/.16
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A final concept to consider within the larger framework of the SAID principle is
reversibility. If the muscle is not regularly challenged at the same (maintenance) or greater
(overload) degree, then the trained adaptations will downregulate 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 risking injury. The type of demand imposed
should match the vocal requirements of the goal behavior. For example, preparation for a
recital should be different than training for work as a classroom teacher. Analysis of these
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two different scenarios has indicated that while the overall vocal dose may be similar in
distance, the dose is achieved over different time spans and using a different average sound
level.17
3.2.
Sex & Age Considerations
Muscle morphology and response to exercise will differ between most men and women.
Women realize measurable muscle strength gains through both neuromuscular mechanisms
and hypertrophy, with a greater reliance on the former. 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 al.18 provides a comprehensive review of the effects of sex hormones on laryngeal
muscle senescence.
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3.3.
Training Adaptations in the Muscles of Voice Production
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Exercises to increase strength and endurance of the limb muscles have been extensively
studied in the traditional exercise 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
neuromuscular 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 (e.g. 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
studied in isolation relative to specific neuromuscular deficits, giving some insight into the
capability for training to improve each individual subsystem.
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3.3.1. Respiratory Muscles—In typical voice production there is more than sufficient
strength and endurance of the respiratory muscles to produce voice. In voice therapy or
singing training, coordination of respiratory muscles with the phonatory system is often the
goal rather than muscle strengthening. The capacity for increasing respiratory muscle
strength has been demonstrated in respiratory muscle strength training (RMST) programs for
individuals who have compromised respiratory 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 during inspiration or exhalation. Direct measurement of the
strength of the respiratory muscles is not possible in vivo. Therefore, respiratory muscle
strength is indirectly quantified by measuring changes in pulmonary function parameters
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
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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, phonation 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 production for specific individuals with respiratory muscle weakness but may
not be a necessary component of voice habilitation or rehabilitation.22
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More relevant for voice production is improved respiratory muscle endurance to reduce
fatigue or improve vocal performance during extended periods of voicing, such as singing or
sustained speaking (e.g. teaching, lecturing). Respiratory muscle 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 (MVV), a pulmonary function task. MVV 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 (MPT) has been
used extensively as a surrogate measure of laryngeal aerodynamic efficiency, no specific
task targeting respiratory muscle endurance during voicing has been established.
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3.3.2. Muscles of the Vocal Tract—The muscles surrounding the vocal tract
contribute to resonance 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 quantified; however, tongue strength measurement during
swallowing, 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 correlate with
articulatory muscle weakness. In a study measuring 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 developing speech or a speech sound disorder.
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The rapid, fine motor muscular movements needed for articulation and resonance
adjustments are best trained (and treated when a deficit is present) by speech and voice
tasks, not by gross motor, nonspeech exercises.27 In contrast, 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 determines
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the size and shape of the vocal tract. It is also the primary 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 pressure generated by
pushing different portions of the tongue against a pressure transducer, such as the Iowa Oral
Performance 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.
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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 individual
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.
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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 different
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. Alternatively, 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 of general physical exercise and the muscles voice
production.
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3.3.3. 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 through auditory-perceptual or acoustic analysis. During this
task the laryngeal muscles adduct the vocal folds and maintain a constant longitudinal
tension. During more typical use, such as conversational speech, the intrinsic laryngeal
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.
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As with the muscles of respiration and the vocal tract, specifically targeting strength and
endurance of the laryngeal muscles is not typically a target of vocal training. However, lack
of laryngeal muscle strength and tonicity are relevant concepts in the context of
hypofunctional voice disorders. For example, laryngeal muscle atrophy (loss of size and
strength) is thought to be the primary cause of presbyphonia, a voice disorder related to
advanced age. The evidence 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 Silverman Voice Treatment.
34-36 Each of these three interventions incorporates one or more maximal vocal function task
(i.e. 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 non-vocal activities such as swallowing or the Valsalva
maneuver. However, these maximum vocal function tasks engage the laryngeal (and likely
respiratory) muscles at levels greater than that required for most voicing tasks, which may
result in improved function and neuromuscular adaptations 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.
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3.4.
Animal Models of Vocal Exercise
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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
mechanisms underlying vocal exercise.37 Additionally, animal models allow us to examine
neuromuscular training response in both diseased and normal, non-injured 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 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.
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Investigation of neuromuscular responses to training requires methodology to target the
specific muscle(s) of interest. This targeting has been accomplished in exercise models of
the animal vocal subsystems using three methods: resistance 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
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and require the animals be motivated for the reward. Examples of these approaches can be
found in each vocal subsystem.
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3.4.1. 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
contrast to human studies, in which airway resistance is introduced 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 tracheal cannula. This obstruction increases
the respiratory muscle engagement needed to maintain ventilation. Results using this model
demonstrated an interesting mix of adaptations 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 respiratory 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.
3.4.2. Animal models of tongue muscle exercise—NMES of the tongue muscles
via stimulation of the hypoglossal 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 relationship of the pre/post synaptic morphology in the neuromuscular
junctions (NMJ) of the genioglossus muscle changed with NMES, implicating possible
improved synaptic efficiency.41
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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 (i.e. greater intensity
than what is possible 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.
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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 protrusive tongue maneuver which is not a typical action in
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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 understand mechanisms underlying dysphagia treatments. Although,
relative to swallowing, the tongue muscles contract 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.
3.4.3. 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.
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In contrast, Karbiener et al.45 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 supramaximal 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 experimentally
determined the NMES parameters (intensity, duration, etc.) that resulted in muscle fatigue,
as measured by decreased adductory pressure over time. This combination, 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 skeletal muscles that occurs secondary
to shorter duration muscle efforts.3
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Using an NMES rat model, McMullen, et al.44 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. 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 forcing the muscles to
become more reliant on aerobic pathways. 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
NMES protocols for stimulating laryngeal muscles using either supramaximal or functional
fatigue offer controlled ways of measuring muscle contraction. In contrast, behavioral
models offer less precise control over individual muscle contractions but are more
homologous to human vocal training. The only behavioral animal model of vocal training
currently used to investigate the laryngeal neuromuscular adaptations to vocal exercise is
training rats to increase their production of ultrasonic vocalizations (USVs). Despite the
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different final acoustic output between human vocalizations 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, demonstrating 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 mechanism created by an air jet through a narrowed
glottis, not vocal fold vibration.47 This mechanistic difference is actually 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 superficial vocal fold layers.
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There are two studies using this model that have demonstrated neuromuscular adaptations
within the TA muscle of both the young and old rat larynx in response to vocal training.48,49
After 8 weeks of daily vocal training with progressively increasing the target number of
USVs each week, age-related changes in neuromuscular junction (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 performance 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 training. Similar to the first study, adaptations of NMJ morphology 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 functional
consequences of the changes in NMJ morphology.
4. Model of muscular activation during vocalization
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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 (e.g. stroke, muscle tension dysphonia) or during
athletic voice use (e.g. singing, preaching, teaching), the muscles of voice production require
training and, therefore, the principles of exercise science 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
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focuses on strengthening a specific muscle or groups of muscles. As discussed 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 endurance 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.
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Figure 2 presents a model of the cyclical coordination of muscle activation in each vocal
subsystem required to produce (A) a sentence commonly used in voice evaluation and (B) a
sustained sung phrase. Three phases of vocalization are delineated: inhalation, pre-phonatory
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
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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 conversational 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 neuromuscular 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 possibly 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.
5. Future Directions
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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
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pursue a thorough understanding of intrinsic laryngeal skeletal muscle fiber typing and
metabolism, 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 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 beneficial to create a framework from
which voice habilitation and rehabilitation programs may be developed and evaluated for
efficacy.
Acknowledgements
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
Symposium: Care of the Professional Voice on June 1, 2018, in Philadelphia, Pennsylvania.
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This work was partially supported by funding from The National Institute on Deafness and Other Communication
Disorders (NIDCD/NIH), grant K23DC014517 (Johnson, PI).
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Figure 1.
Exercise science theoretical framework.
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Figure 2.
Model of neuromuscular coordination during vocalization of (A) a spoken utterance and (B)
a sustained sung phrase.
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