JSLHR
Review Article
Muscle Bioenergetic Considerations for Intrinsic
Laryngeal Skeletal Muscle Physiology
Mary J. Sandagea and Audrey G. Smitha
Purpose: Intrinsic laryngeal skeletal muscle bioenergetics, the
means by which muscles produce fuel for muscle metabolism,
is an understudied aspect of laryngeal physiology with
direct implications for voice habilitation and rehabilitation.
The purpose of this review is to describe bioenergetic
pathways identified in limb skeletal muscle and introduce
bioenergetic physiology as a necessary parameter for
theoretical models of laryngeal skeletal muscle function.
Method: A comprehensive review of the human intrinsic
laryngeal skeletal muscle physiology literature was conducted.
Findings regarding intrinsic laryngeal muscle fiber complement
and muscle metabolism in human models are summarized
and exercise physiology methodology is applied to identify
probable bioenergetic pathways used for voice function.
T
here is a growing interest in the development
and application of targeted muscle training pro-
grams for voice and other disorders of respiration
and swallowing for habilitative and rehabilitative means
(Burkhead, Sapienza, & Rosenbek, 2007; Johnson, Ciucci,
& Connor, 2013; Pitts et al., 2009; Russell, Ciucci, Connor,
& Schallert, 2010). Foundational to an exercise program
of any type is an understanding of the muscle duration and
intensity requirements for the target activity, consideration
of the muscle fiber type and metabolic characteristics,
and a skillful application of muscle training principles to
achieve optimal outcome. Many aspects of intrinsic laryn-
geal skeletal muscle (ILSM) physiology—of which muscle
bioenergetics is one—are not well understood. Muscle fiber
type complement and the muscle bioenergetic (metabolic)
substrate that supports muscle fiber function are two key
physiological components required to understand basic
laryngeal physiology for targeted training programs. Basic
research is emerging in the area of ILSM muscle fiber typ-
ing, with ILSM metabolism as an area of particularly limited
a
Auburn University, Auburn, AL
Correspondence to Mary Sandage: sandamj@auburn.edu
Editor: Julie Liss
Associate Editor: Jack Jiang
Received May 11, 2016
Revision received September 23, 2016
Accepted October 27, 2016
https://doi.org/10.1044/2016_JSLHR-S-16-0192
1254 Journal of Speech, Language, and Hearing Research • Vol. 60 • 1254–1263 • May 2017 • Copyright © 2017 American Speech-Language-Hearing Association
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Results: Intrinsic laryngeal skeletal muscle fibers
described in human models support the fast, high-
intensity physiological requirements of these muscles
for biological functions of airway protection. Inclusion
of muscle bioenergetic constructs in theoretical modeling
of voice training, detraining, fatigue, and voice loading
have been limited.
Conclusions: Muscle bioenergetics, a key component for
muscle training, detraining, and fatigue models in exercise
science, is a little-considered aspect of intrinsic laryngeal
skeletal muscle physiology. Partnered with knowledge of
occupation-specific voice requirements, application of
bioenergetics may inform novel considerations for voice
habilitation and rehabilitation.
research. Fiber type and metabolism are requisite compo-
nents for theoretical modeling of laryngeal physiology, which
may include training models for sustainable occupation-
specific vocal dose. A holistic understanding of skeletal
muscle bioenergetic pathways applied to laryngeal muscle
function physiology is of particular importance for our
understanding of aspects of voice training that develop
fatigue resistance, given that bioenergetic fatigue is a pri-
mary component of muscle fatigue in general. Translation
of limb skeletal muscle bioenergetics is a place to start,
given the technical challenges for basic ILSM metabolic
research in vivo.
Muscle bioenergetics, the aspects of muscle fiber
manufacturing and utilization of adenosine triphosphate
(ATP) for muscle fuel, will first be described, followed by
a summary of ILSM fiber types to provide a functional
context for muscle metabolism as it is currently understood.
The bioenergetic pathways that support muscle metabo-
lism are dynamic and can be upregulated during times of
muscle training to establish fatigue resistance and down-
regulated in times of muscle disuse or detraining. The im-
plications of muscle fiber bioenergetic adaptations during
muscle training programs are important for researchers
to consider when developing theoretical models of voice
training and voice fatigue. Clinicians can also apply bio-
energetic constructs when developing training programs for
Disclosure: The authors have declared that no competing interests existed at the time
of publication.
 habilitation or rehabilitation of muscles used for optimal
voice use.
Muscle Metabolism
Bioenergetics refers to the production of energy sources
required for muscle contraction and relaxation (Hoffman,
2002). According to Brooks, Fahey, and Baldwin (2005), the
human body uses three bioenergetic pathways to produce
ATP, the primary muscle fuel required to power muscular
movements. ATP is required for muscle fiber processes that
promote both contraction and relaxation, described as
excitation–contraction coupling. ATP is locally available in
the muscle tissue in limited quantities for muscle contrac-
tion and must be replaced when depleted or when muscle
contraction requirements exceed its stored capacity. The
three primary energy systems for manufacturing ATP corre-
late with the demands imposed on the muscles of the body:
power (e.g., shot putting), speed (e.g., 100-m sprinting), and
endurance (e.g., distance running). Each of these activities
requires specific biochemical mechanisms that support ATP
production. In the human body, energy conversion occurs
within each cell in the presence of a substrate that can both
receive energy input from energy-yielding reactions and
yield energy to reactions requiring an energy input, usually
ATP. ATP is composed of a nitrogenous base (adenine),
a five-carbon sugar (ribose), and three phosphates. Remov-
ing the terminal phosphate from ATP results in adenosine
diphosphate, and removing two phosphates from ATP results
in adenosine monophosphate. This degradation of ATP by
cleaving a terminal phosphate supplies the chemical energy
required to power muscle contraction, regardless of which
energy system is providing the ATP.
In skeletal muscle, three primary bioenergetic path-
ways have been identified: the immediate energy system,
glycolysis, and oxidative phosphorylation (Brooks et al.,
2005). The immediate energy system uses creatine phosphate
(CP; also called phosphocreatine) as the fuel substrate for
production of ATP. Glycolysis utilizes circulating glucose
and stored glycogen for ATP substrate. Both of these bio-
energetic mechanisms are anaerobic pathways. Oxidative
phosphorylation, an aerobic pathway housed within the
mitochondria, relies on oxygen as the fuel substrate (Powers
& Howley, 2014).
Immediate energy sources are so named because they
are immediately available for muscle contraction (Brooks
et al., 2005). In physical efforts that require power, such
as throwing a shot put, muscle activity lasts for only a few
seconds and the muscle cells used rely primarily on the
immediate energy system. CP, the cellular source of imme-
diate energy, is a high-energy phosphorylated compound
existing at approximately five times greater concentrations
than ATP in resting muscle. CP acts as a reserve of phos-
phate energy to regenerate the ATP consumed during mus-
cle contraction. The enzyme creatine kinase catalyzes the
interaction of CP and adenosine diphosphate to result in
ATP. The concentration of stored ATP and the CP reserve
generally found in a cell cannot sustain muscle contraction
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for more than a few seconds; therefore, muscle contraction
lasting longer than a few seconds requires supplemental
energy sources.
Glycolytic, nonoxidative energy sources are consumed
when muscle activity lasts longer than a few seconds and
involves the breakdown of a simple sugar (glucose) and
stored carbohydrates (glycogen; McArdle, Katch, & Katch,
2010). For speed activities, that is, rapid and forceful ac-
tivities lasting from a few seconds to 1 min, such as the
100-m sprint, skeletal muscle relies primarily on nonoxida-
tive glycolytic energy sources as well as immediate energy
sources. Skeletal muscle tissue contains high concentrations
of glycolytic and glycogenolytic enzymes, so muscles spe-
cialized in these processes can rapidly break down glucose
and glycogen, yielding a lactate anion and a proton at
physiological pH. The number of facilitating enzymes for
glycolysis and gluconeogenesis, the means by which circu-
lating glucose is stored as glycogen in the liver, is extensive
(Nelson & Cox, 2008). Skeletal muscle contains low amounts
of free glucose. The glycogen reserves of energy found in
skeletal muscles are supplemented with glucose supplied
from the blood, glycogen stored in the liver, and fats and
amino acids that exist in the muscle. Glucose in the blood-
stream is consumed as needed by skeletal muscle as special
receptors move to the surface of the muscle cell during mus-
cle activity to offload circulating glucose. In glycolysis, one
molecule of glucose produces two molecules of ATP; fur-
thermore, the quantitative energy available from glycolytic
energy sources is greater than that available from immedi-
ate energy sources, but the combined energy provided by
glycolytic and immediate energy sources is a fraction of the
energy available from oxidative energy sources (Powers &
Howley, 2014).
Oxidative energy sources for muscles include carbo-
hydrates, fats, and certain amino acids (Brooks et al.,
2005). Oxidative mechanisms of energy production allow
more energy to be liberated from a glucose molecule than
from glycolytic energy production because the breakdown
of glucose is longer and more involved, which ultimately
yields more ATP: 36 molecules of ATP in oxidative phos-
phorylation versus two molecules of ATP in nonoxidative
energy production. For endurance activities in which skele-
tal muscles are engaged for longer than 2–3 min, such as
middle distance and marathon running, oxidative phos-
phorylation takes over for the primary bioenergetic path-
way to support muscle contraction. At the onset of muscle
activity, immediate energy systems are activated. If muscle
activity continues, it depletes the immediate energy sup-
ply and glycolysis predominates to power muscle activity,
and when muscle activity exceeds the capacity of glyco-
lytic energy, oxidative phosphorylation takes over as the
energy source (see Figure 1). Bioenergetic pathways also
work synergistically to meet the muscle activity require-
ments. For example, a distance runner relying primarily
on oxidative phosphorylation may engage the immediate
energy and glycolytic energy systems to provide energy to
muscle fibers that produce power in order to run up a steep
hill when more power is required.
1255
 Figure 1. Temporal characteristics of bioenergetic pathways. At the onset of exercise, all three energy systems are turned on. For exercise
that lasts about fifteen seconds, the immediate energy system is the primary fuel source. Exercise bouts lasting longer than this brief time
frame deplete the immediate energy system and require supplemental energy sources. The glycolytic energy system then becomes the
primary fuel source for exercise bouts lasting approximately forty-five seconds, after which the glycolytic system is depleted. Oxidative
phosphorylation is the primary fuel source for exercise bouts lasting longer than approximately two to three minutes, depending on the
upregulation of the individual’s metabolism. Adapted from Brooks et al. (2005).

All three energy systems are “turned on” at the onset
of physical activity. For exercise that lasts about fifteen
seconds, the immediate energy system is the primary fuel
source. Exercise bouts lasting longer than this brief time
frame deplete the immediate energy system and require
supplemental energy sources. The glycolytic energy system
then becomes the primary fuel source for exercise bouts
lasting approximately forty-five seconds, after which the
glycolytic system is greatly reduced or depleted. Oxidative
phosphorylation is the primary fuel source for exercise
bouts lasting longer than approximately two to three min-
utes, depending on the upregulation of the individual’s
metabolism. Highly trained individuals will transition to
oxidative phosphorylation faster. The temporal aspects of
bioenergetic substrate use are illustrated in Figure 1.
An aspect of substrate utilization after exercise has
ceased is the replenishment of locally available muscle fuel
stores and enzymes to catalyze ATP production. After ex-
ercise, oxygen is often consumed during a process referred
to as excess postexercise oxygen consumption (EPOC;
McArdle et al., 2010). During this process, oxygen uptake
remains elevated for a period of time during the recovery
process to return the body to homeostasis. EPOC occurs to
a greater degree following higher intensity muscle activity
and to a lesser extent for low-intensity activity. This process
can become more efficient with muscle training and less
efficient with detraining and disuse.
Limb Skeletal Muscle Fiber Types
Bioenergetic mechanisms used by skeletal muscle are
in part determined by the muscle fiber complement of the
muscles in use; therefore, a short review of skeletal muscle
fiber characteristics is required for metabolic context. Skel-
etal muscle consists of bundles of muscle cells called mus-
cle fibers (Hoffman, 2002). The number of muscle cells per
muscle varies, depending on the size of the muscle and
the type of work the muscle is required to do. The thyro-
arytenoid muscle, which is responsible for fine adjustments
in the tension of the vocal fold, has only a few hundred
muscle fibers when compared with the vastus lateralis, the
largest of the quadricep muscles, which contains hundreds
of thousands of muscle fibers (MacIntosh, Gardiner, &
McComas, 2006). It is understood that fiber type is deter-
mined by its neural innervation; however, with training,
detraining, or disuse, morphological and bioenergetic char-
acteristics of the fiber type can be influenced to operate
in ways that mirror other muscle fiber types (MacIntosh

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 et al., 2006; McArdle et al., 2010; Powers & Howley, 2014).
Some motor units are designed for aerobic metabolism,
which refers to energy-generating catabolic reactions when
oxygen is present, whereas other motor units are better
suited for anaerobic activity, during which oxygen is absent
(McArdle et al., 2010).
Two distinct muscle fiber types have been identified
according to their contractile and metabolic characteristics:
slow-twitch fibers (Type I) and fast-twitch fibers (Type II).
The contractile properties of skeletal muscle are determined,
in part, by the myosin heavy chain (MHC) isoforms, which
determine the maximum contraction speed of a muscle
fiber, a vital parameter for the functional characterization
of muscle fibers (Larsson & Moss, 1993; Shiotani, Westra,
& Flint, 1999). Type I fibers are fatigue-resistant fibers and
therefore are more suited for prolonged, low-to-moderate
intensity activity. Type I muscle fibers primarily produce
ATP through aerobic, oxidative pathways; therefore, Type I
fibers are highly fatigue resistant and well suited for pos-
tural requirements and prolonged aerobic exercise (McArdle
et al., 2010).
Type II fibers are better suited for shorter, higher
intensity activity and can be broken down into Type IIa
and Type IIx fibers (Hoffman, 2002; McArdle et al., 2010).
Type IIa fibers are referred to as fast, fatigue-resistant,
oxidative glycolytic fibers, which means they rely on both
oxidative phosphorylation and glycolysis for energy pro-
duction. They have the capacity for both aerobic and an-
aerobic metabolism. Type IIx fibers, or fast, fatigable
glycolytic fibers, have the greatest capacity for anaerobic
metabolism. Type IIa and IIx fibers are both anaerobic
fibers, but in different capacities. Type IIx fibers rely pri-
marily on anaerobic (glycolytic) metabolism to produce
energy. It should be noted that although biochemical and
contractile differences exist between muscle fiber types,
these fiber types do not generally function in isolation,
but rather form a continuum. In addition, whole muscles,
which are made up of many motor units, generally consist
of a combination or hybrid of muscle fiber types. Table 1
provides a summary of muscle fiber type characteristics.
The muscle fiber complement in limb skeletal muscle
is usually estimated at 50% Type I fibers and 50% Type II
fibers (Powers & Howley, 2014). Most people have a 50/50
distribution of muscle fiber type, but the literature suggests
Table 1. Characteristics of muscle fiber types found in the larynx.
Muscle fiber type Contractile property
Limb skeletal muscle
Type I Slow
Type IIa Fast
Type IIx Fast
Specialized muscle fiber types
Type IIL Superfast
Slow tonic Slow
Note. Muscle fiber types that have been found in the larynx are described according to their physiological
characteristics. Adapted from Brooks et al. (2005), Han et al. (1999), and Schiaffino and Reggiani (2011).
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that there are outliers who are genetically predisposed to a
greater percentage of one fiber type over another, such as
elite athletes (Brooks et al., 2005). The muscle fiber distri-
bution predisposes elite athletes to perform the athletic re-
quirements of their sport. For example, elite sprinters have
been found to have a higher proportion of fast glycolytic
muscle fibers (power fibers) whereas elite distance runners
have been found to have a higher proportion of slow-twitch
oxidative fibers (endurance fibers). Type I fibers are most
likely found in abundance in endurance athletes, such as
distance runners and cross country skiers (McArdle et al.,
2010). As we described previously, muscle training programs
may alter muscle fiber characteristics to better match the
work imposed on the muscle; however, extensive training of
a 50/50 distribution of muscle fiber type complement will
not match that of a trained individual with a genetically
optimal muscle fiber complement for the task (Powers &
Howley, 2014). If there are elite athletes who are outliers to
the typical muscle fiber type distribution, the potential of
vocal outliers with genetic predisposition to certain vocal
tasks over others should be considered and investigated.
During motor unit recruitment, muscle fibers are
recruited in a specific order, the magnitude of recruitment
being directly linked to the degree of force production re-
quired. This recruitment order is referred to as the size
principle (Sale, 1986). According to the size principle, mus-
cle fibers are recruited in the following order: Type I →
Type IIa → Type IIx. The degree to which these fibers are
recruited in succession is determined by the intensity of
the muscle effort. For lower intensity activities, Type IIx
may not be recruited because the degree of force required
may not necessitate the engagement of Type IIx fibers.
For maximal intensity exercise, all muscle fiber types will
be recruited in order to produce the higher degree of force
required, with more Type II fibers engaged than Type I
for greater force production. That being said, even during
a maximal voluntary contraction, not all muscle fibers
within a motor unit are typically engaged at the same time
(McArdle et al., 2010).
ILSM Muscle Fiber Types
There is abundant research about the muscle fiber
complement of limb skeletal muscle, but there has been
Fatigue resistance Metabolic properties
High Slow oxidative
Moderate Fast oxidative glycolytic
Low Fast glycolytic
Low Fast glycolytic
High Oxidative
1257
 limited research done to determine the fiber type profiles Figure 2. Intrasubject variability. The thyroarytenoid (TA), lateral
cricoarytenoid (LCA), interarytenoid (IA), posterior cricoarytenoid
of human ILSMs. Most of the basic ILSM muscle fiber (PCA), and cricothyorid (CT) were characterized by the ratio of
research has been based on animal models. The intrinsic percent of Type I fibers to Type II fibers in laryngeal muscles in three
laryngeal muscles include four paired muscles—the thyro- human cadavers. Data were adapted from Rosenfield et al. (1982).
arytenoid (TA), lateral cricoarytenoid (LCA), posterior
cricoarytenoid (PCA), and cricothyroid (CT)—and one un-
paired muscle, the interarytenoid (IA; Hoh, 2005). Limb
skeletal muscle is primarily responsible for postural sup-
port and locomotion, and intrinsic laryngeal muscles are
responsible for airway protection, respiration, and phona-
tion (Hoh, 2005). The larynx also serves a vital buffering
role between the ambient environment and the body’s core
homeostasis (Sandage, Connor, & Pascoe, 2014). Given
the differences in physiological requirements of the larynx
between species (e.g., articulation for humans and thermo-
regulation for panting species), comparison of animal
muscle fiber characterization with human ILSM physiol-
ogy should be done with care.
Human laryngeal muscles have been described to
express Type I, Type IIa, Type IIx, and Type IIL isoforms
similar to fiber types seen in limb skeletal muscle (Tellis,
Rosen, Thekdi, & Sciote, 2004). Few investigations have
been conducted to describe the specific muscle fiber com-
plement of the intrinsic laryngeal muscles in humans. In a
cadaver study, the total number of muscle fibers counted
from each muscle for each cadaver was similar; however,
variability in the distribution of Type I and Type II fibers
was found within and between cadavers (Rosenfield, Miller,
Sessions, & Patten, 1982). The intersubject variability of
the muscle fiber complements of the ILSMs between par-
ticipants is graphically represented in Figure 2. Figure 3
shows the intrasubject variability of the muscle fiber com-
plement of each of the ILSMs.
Shiotani et al. (1999) investigated the MHC com-
position of human cadaver intrinsic laryngeal muscles of
nine middle-aged and older adults. These authors used
sodium dodecyl sulfate polyacrylamide gel electrophoresis
(SDS-PAGE) and Western blot analysis to determine MHC
composition. They found that human laryngeal muscle
composition exhibited a predominance of fast-type MHC
in laryngeal adductor (closing) muscles and a mixed fast–
slow type in respiratory and phonatory muscles. In addi-
tion, an MHC band migrating between Type IIa and predominantly consist of Type I fibers. One explanation
Type I was found in all laryngeal muscles, which is similar for the incongruent findings of these studies could be re-
in position to Type IIL found in rats. This indicates the lated to the ages of the cadavers; during the aging process,
possible presence of superfast Type IIL muscle fibers in the there tends to be a change from Type I to Type II fibers
larynx. The TA muscle is made up of two muscular com- (MacIntosh et al., 2006). Because the ages of the cadavers
ponents: the thyromuscularis and the thyrovocalis, or simply in the Rosenfield et al. study were not reported, this cannot
vocalis (VOC; Stemple, Glaze, & Klaben, 2010). Shiotani be confirmed. Another difficulty in comparing the results
et al. (1999) reported MHC composition for the VOC spe- of these two studies lies in the nomenclature used and the
cifically and the TA muscles generally. The findings of method of reporting muscle fiber types. Rosenfield et al.
MHC composition in human intrinsic laryngeal muscles are reported muscle fiber types as either Type I or Type II,
reported in Figure 4. These authors found higher percent- whereas Shiotani et al. reported Type I, Type IIa, and
ages of Type IIa muscle fibers than Type IIb or Type I in Type IIb. This difference makes translation of data from one
each of the ILSMs. study to the other more difficult. Shiotani et al. reported
Overall, Shiotani et al. (1999) reported lower per- the findings in a table of means and standard deviations, so
centages of Type I fibers than Rosenfield et al. (1982), par- combining the Type II groups is not feasible without the
ticularly for the PCA, which were previously reported to raw data. It should also be noted that in humans, Type IIb

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 Figure 3. Intersubject variability in intrinsic laryngeal skeletal muscle fiber type. The same data from Figure 2
were reformatted to show variability among three human cadavers in the percent of Type I fibers to Type II
fibers in laryngeal muscles. The numbers 1, 2, and 3 correspond to the cadavers in the study. The PCA,
which is responsible for maintaining airway patency, had a high percentage of Type I fibers in all three cadavers.
TA = thyroarytenoid; PCA = posterior cricoarytenoid; LCA = lateral cricoarytenoid; IA = interarytenoid; and
CT = cricothyroid. Data were adapted from Rosenfield et al. (1982).

fibers are currently referred to as Type IIx fibers, which are studies indicated the presence of STFs in all nine cadaver
considered to be undifferentiated muscle fibers (Powers & TA muscles, predominantly in the region of the VOC
Howley, 2014). muscle. These authors proposed that STFs may contribute
Li, Lehar, Nakagawa, Hoh, and Flint (2004) compared to the TA’s function of pitch modulation and regulation
MHC isoforms found in abductor and adductor muscles in
five human cadavers ages 55–75 years using SDS-PAGE
and Western blot analysis. Although extraocular-specific Figure 4. Myosin heavy chain percent composition in human intrinsic
laryngeal muscles. The human laryngeal muscle composition of
MHC and fast Type IIb MHC isoforms have been found
six human cadavers was examined via sodium dodecyl sulfate
in the TA muscles of rats, they were not detected in this polyacrylamide gel electrophoresis (SDS-PAGE) and Western blot
study in the human cadaver ILSMs. These authors found analysis to determine myosin heavy chain composition. It should
that fast Type IIx MHC was expressed only in adductor be noted that Type IIb fibers are currently referred to as Type IIx
muscles, which are the TA, VOC, and LCA muscles, muscle fibers in the human body. TA = thyroarytenoid; LCA = lateral
cricoarytenoid; IA = interarytenoid; VOC = thyrovocalis; PCA =
whereas fast Type IIa MHC and slow MHC were expressed posterior cricoarytenoid; and CT = cricothyroid. The graph is adapted
in all ILSMs. They propose that fast Type IIx MHC expres- from the means and standard deviation (error bars) data reported by
sion may be associated with rapid glottic closure in order Shiotani et al. (1999).
to protect the airway because they are found only in the
adductor muscles in the larynx. Consistent with the find-
ings of Shiotani et al. (1999) and D’Antona et al. (2002),
the Li et al. study found a higher percentage of Type II
fibers than Type I fibers, with the exception of the PCA,
which contained the highest percentage of Type I fibers.
Han, Wang, Fischman, Biller, and Sanders (1999) in-
vestigated the presence of slow tonic muscle fibers (STFs)
in the TA muscle of nine human cadavers. STFs are unique
muscle fibers because they contract in slow, stable, pro-
longed contractions instead of with a twitch. The contrac-
tions of STFs are precisely controlled and fatigue resistant.
STFs are also found in the human extraocular muscles
(Bormioli, Torresan, Sartore, Moschini, & Schiaffino, 1979).
Immunofluorescence microscopy and immunoblotting

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 during phonation because they are found in human laryn-
ges and not in the larynges of other mammals.
In addition to the cadaver studies described here, a
smaller body of work described in vivo muscle fiber anal-
ysis. D’Antona et al. (2002) investigated the functional
properties and MHC isoforms in the TA, VOC, LCA, CT,
and PCA muscles of four adult men ages 55–67 years biop-
sied subsequent to laryngectomy. Biopsy samples were
analyzed using SDS-PAGE and densitometry. The presence
of MHC-1, MHC-2A, and MHC-2X isoforms were identi-
fied. An additional MHC isoform, provisionally labeled
MHC-L by these authors, was found in three of the four vo-
cal muscles, which was a migrating type between MHC-1
and MHC-2A. These authors also found that fast MHC iso-
forms, particularly MHC-2A, were predominant, which is
consistent with the findings of Verdolini Abbott et al. (2012).
It is interesting to note that one-third of the fibers were mixed
or hybrid, which is consistent with the observation that there
are likely innumerable mixed fiber types in the human body
(Powers & Howley, 2014). In another in vivo muscle fiber
study, Horton, Rosen, Close, and Sciote (2008) investigated
the presence of perinatal, extraocular, IIb, and cardiac
MHC isoforms in the TA and PCA muscles from 15 partic-
ipants ages 45–81 years who underwent total laryngectomy.
Real-time quantitative reverse-transcriptase polymerase
chain reaction was used to identify MHC genes expressed
in the TA and both portions of the PCA. Similar to the
findings of D’Antona et al. (2002), no extraocular-specific
MHC or MHC-IIb were detected in either of the ILSMs;
however, low amounts of perinatal and cardiac genes were
found in both the TA and the PCA.
ILSM Bioenergetics
Large gaps exist in the current understanding of
ILSM muscle fiber bioenergetics. Because of the highly
specialized functional demands of the ILSMs (e.g., ventila-
tion, swallowing, phonating, coughing, airway patency),
the ILSMs are made up of very small and fast fibers with
a high mitochondrial content, which is a unique muscle fi-
ber phenotype (McMullen & Andrade, 2006). Fast-twitch
muscle fibers found in the limbs typically rely more heavily
on anaerobic bioenergetic pathways with lower mitochon-
drial density than do Type I fibers. Schiaffino and Reggiani
(2011) have asserted that all laryngeal muscle fibers are
fatigue resistant, regardless of fiber type.
The empirical identification of bioenergetic pathways
in the ILSMs is challenging in vivo. Tellis et al. (2011) were
the first to evaluate the efficacy of visible light spectros-
copy in vivo to provide evidence of vocal fold muscle metab-
olism. Visible light spectroscopy measures reflected visible
light to monitor tissue oxygen (StO2) and relative total
hemoglobin in the TA–LCA muscle complex. Measure-
ments of StO2 and relative total hemoglobin levels were
continuous and direct before, during, and after a phonatory
task of production of ah for as loud as possible for a total
of 60 s. The participants were instructed phonate as long as
possible, take a quick breath as needed, and then resume
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phonation until the target of 60 s was achieved. Continuous
phonation was likely not achieved for 60 consecutive sec-
onds given the respiratory constraints for most individuals.
These measurements indicated a drop in StO2 levels during
the phonatory task, followed by overshoot of StO2 after the
phonatory task was completed, as compared with baseline.
The StO2 overshoot observed is consistent with what has
been described as EPOC (McArdle et al., 2010).
These findings were compared with those of Cannon,
White, Andriano, Kolkhorst, and Rossiter (2011) and de-
termined to be consistent; however, the parallels described
for rise and fall in StO2 levels may be an overestimation
given that a 60-s, noncontinuous voicing task was com-
pared with an 8-min maximal cycling ergometer task. The
bioenergetic pathways used for a brief vocalization are
likely reliant on the immediate energy system, which would
not be comparable to a steady-state cycling bout that relied
on oxidative phosphorylation as described in Figure 1.
This methodology may have identified oxygen use during
voicing as a substrate for energy production, which would
be unexpected given the short duration of the vocalization.
It may be that all metabolic mechanisms were turned on at
the start of the vocalization and oxygen was part of more
complex substrate utilization that also included CP and glu-
cose, the latter two of which were not measured. Given this
possibility, the extent to which oxygen was used relative
to total substrate utilization for the task is still unknown. It
remains unclear as to whether the bioenergetic pathways
within the ILSMs are unique. The results of this study are
valuable and pose excellent questions for future investiga-
tion into laryngeal muscle physiology, particularly if the
findings are indicative of novel bioenergetic pathways that
are not yet described.
Limb Skeletal Muscle Adaptation
Limb skeletal muscle adapts in conditions of muscle
use, disuse and, detraining. With limb skeletal muscle exer-
cise of sufficient intensity and frequency, muscle physiology
adapts via neurological, morphological, and bioenergetic
mechanisms (Powers & Howley, 2014). Upregulation of
muscle fiber bioenergetic substrate utilization occurs when
the demands placed on the muscle exceed typical demands,
described as the specific adaptations to imposed demand
principle (McArdle et al., 2010). Downregulation of muscle
metabolism occurs when the demands placed on the muscle
tissue fall below typical demands over a period of time
(McArdle et al., 2010).
With endurance training, significant adaptations
occur to the metabolic features of muscle fibers; these ad-
aptations are primarily expressed as an increase in mito-
chondrial proteins and glycolytic enzymes that matches
the increased demand on oxidative capacity (Brooks et al.,
2005). Metabolic and musculoskeletal adaptations that
occur during endurance training include increases in mito-
chondrial size and number, oxidative enzymes, capillary
density, and reliance on stored fat as an energy (Hoffman,
2002). Endurance training increases the body’s ability to
 produce ATP efficiently and offload oxygen to working
muscles faster (Hoffman, 2002). In addition, the efficiency
with which EPOC takes place is also influenced by training
and detraining. There are two primary types of athletic
endurance: muscular and cardiorespiratory. Muscular
endurance refers to the capability of a muscle or group of
muscles to engage in sustained, high-intensity, or static
activity, whereas cardiorespiratory endurance is the ability
to sustain long-duration exercise (Hoffman, 2002). For the
ILSMs, the focus would be primarily muscular endurance
for repeated, brief, submaximal engagement over variable
lengths of time.
The aim of anaerobic conditioning is to facilitate high-
intensity activity with rapid recovery between each bout of
exercise and to offset fatigue without experiencing a decrease
in performance (Hoffman, 2002). Physiological adaptations
that occur with anaerobic exercise include metabolic trans-
formation of Type I fibers to a more glycolytic subtype,
significant glycolytic enzyme elevation, an increase in toler-
ance to maximum blood lactate concentrations, a decrease
in lactate concentrations during submaximal exercise, and
increased lactate buffering capacity (Hoffman, 2002). Recov-
ery training for muscle efforts that rely on the immediate
energy system is evidenced by rapid resynthesis of ATP and
phosphocreatine following exercise depletion, with ATP
replenishing within 3–5 min and phosphocreatine replenish-
ing within 8–15 min (Stone, Stone, & Sands, 2009).
Strength training, from an exercise science perspec-
tive, relies on a multitude of principles including, but not
limited to, the principles of specificity, overload, and
fatigue management. Bioenergetic specificity (appropriate
exercise intensity, duration, rest intervals) and mechanic
specificity (movements should be specific to the athlete’s
sport) are essential components of athletic training (Stone
et al., 2009). In essence, this means the muscles should be
trained in a specific manner to achieve the target behavior,
upregulating the bioenergetic mechanisms specific for the
target behavior along the way. Overload focuses on pro-
viding the proper stimuli to elicit the desired physical,
physiological, and performance adaptations (upregulation)
by training beyond the current physical performance level.
Fatigue management describes aspects of muscle condi-
tioning that train the muscle to be more fatigue resistant
through both central and peripheral mechanisms. Although
central mechanisms of fatigue are not yet well described,
peripheral mechanisms include increased availability of
muscle fuel substrate, increased concentration of bioener-
getic enzymes, and motor learning to cycle through muscle
fibers within a motor unit (MacIntosh et al., 2006).
Aerobic training, or endurance training, aims to im-
prove efficiency of ATP production for exercise bouts of
longer durations by causing adaptations to skeletal muscle
mitochondria and respiratory capacity. Increases in the num-
ber of mitochondria and in complexity of the mitochondrial
reticulum allow for more ATP production, thus increasing
efficiency of the muscle.
When exercise conditioning intensity falls below the
level to which the muscles and cardiorespiratory system
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have been habituated, the metabolic mechanisms that have
been upregulated for muscle efficiency and fatigue resis-
tance will reverse course and a period of downregulation
will occur. Stores of locally available muscle fuels will no
longer be maintained, and the increased levels of bioener-
getic enzymes will diminish. It is easier to maintain muscle
efficiency for function than to take a break and return to
the prior level of function. Aspects of muscle training phys-
iology, including bioenergetic fatigue resistance, provide
evidence for use of muscle metabolic physiology in theoret-
ical models of muscle training, including voice training.
Intrinsic Laryngeal Skeletal Muscles
The ILSMs are rapidly engaging and disengaging
throughout the day to sustain biological functions such as
breathing, phonation, and swallowing. Because phonation
is sustained by and cannot be separated from respiration,
the duration of ILSM engagement is dependent upon
available respiratory volume and the contribution of the
respiratory muscles to management of subglottic pressure.
ILSM engagement is also directly related to the type of
voicing task, articulation, and phrasing (Titze, Hunter, &
Švec, 2007). For these reasons, the use of ILSMs is distinct
from limb skeletal muscles in the human body. In addition,
because phonation can be prolonged for a maximum of
approximately thirty seconds, including voice onset and
offset, steady-state oxidative phosphorylation, which occurs
after approximately two to three minutes of continuous
muscle activity, is likely not achieved. Therefore, given our
current understanding of the temporal constraints of commu-
nication and vegetative vocal behaviors in the development
of theoretical constructs of voice training and fatigue, it could
be hypothesized that the ILSM muscles, with the exception
of the PCA, may be primarily reliant on anaerobic energy
(i.e., immediate energy system and/or glycolysis) and use
oxidative phosphorylation to a far lesser extent. Although
there is emerging evidence of oxygen uptake during sustained
vocalization (Tellis, Carroll, Fierro, & Sciote, 2011), the de-
gree to which CP and glucose uptake occurs is unknown.
An important implication for translation of limb
skeletal muscle metabolism to the ILSMs is the degree of
force that is expected from the ILSMs for voicing tasks.
Typical voice use for conversation would be considered
submaximal muscle activity. Applying the size principle,
submaximal activity would indicate the likelihood that
Type I and Type IIa fibers are predominantly recruited.
Performing a theater role in a large performance space
without amplification might be considered a maximally
intensive vocal challenge. The size principle would also
indicate that a higher percentage of Type II fibers would
be recruited for higher intensity vocal tasks in order to
maintain higher sound level voice production against higher
subglottal pressures.
As described by Welham and Maclagan (2003), the
underlying physiological mechanisms for vocal fatigue,
including depletion of bioenergetic substrate, are largely
unknown. Applied research in the area of voice fatigue has
1261
 largely focused on voice function measures following what
are described as vocally fatiguing tasks (Boucher, Ahmarani,
& Ayad, 2006; Chang & Karnell, 2004; Milbrath & Solomon,
2003; Solomon & DiMattia, 2000; Solomon, Glaze, Arnold, &
van Mersbergen, 2003). Applying a muscle bioenergetic con-
struct to the Milbrath and Solomon (2003) investigation of
the influence of vocal warm-up on voice fatigue, it could
by hypothesized that the use of ILSMs for vocal warm-up
would be additive to the subsequent fatiguing task instead
of ameliorating the effects of the prolonged voicing task.
Bioenergetic mechanisms used during the vocal warm-up
may not have had time to recover prior to the extended
voicing task, resulting in a greater degree of muscle meta-
bolic depletion. In future studies of voice fatigue, the physi-
ological rationale for choice of task and interpretation of
outcomes would be enhanced with bioenergetic fatigue
included in the model. Working from a physiological model
that includes bioenergetic fatigue in company with mechan-
ical stress, voice building programs that are designed to
develop tolerance for vocally fatiguing tasks may be of
great occupational benefit.
Inclusion of bioenergetic fatigue in research and clini-
cal hypothesis development may provide a more holistic
approach to the understanding of voice function and the
development of voice disorder. For example, consider the
potential role of bioenergetic fatigue in the etiology of mus-
cle tension dysphonia. Bioenergetic fatigue could be impli-
cated in the increased reliance on compensatory muscle
efforts as seen in primary muscle tension dysphonia. Also
consider the impact of specific techniques in voice rehabili-
tation as having a direct impact on muscle bioenergetics. A
shift in muscle bioenergetic utilization may account for the
experience of less vocal effort and subsequent fatigue when
using resonant voice, whereby sound level gain is achieved
via a greater reliance on vocal tract tuning and reduced reli-
ance on higher vocal fold closure forces. Reduced vocal
fold closure forces, the physiological goal for pressed voice
and high closed quotient, may lower reliance on Type II
muscle fiber power and may realize reduced bioenergetic
fatigue from rapidly depleted immediate energy stores.
Given the fatigue-resistant profile of laryngeal mus-
cles asserted by Hoh (2005) that are described as predomi-
nantly composed of Type II fibers, fibers that are generally
considered more fatigable, it may be that the ILSMs func-
tion in a distinct manner compared with limb skeletal
muscle. Until the bioenergetic mechanisms of the ILSMs
can be determined in vivo in humans (technically challenging
given the location and small volume of the ILSMs), trans-
lation of limb skeletal muscle bioenergetics to laryngeal
function may serve as a useful theoretical framework in a
manner similar to the use of models of mechanical stress
used to account for molecular breakdown of vocal fold
tissue (Titze, Švec, & Popolo, 2003).
Conclusions
Muscle bioenergetics is a little-considered aspect of
voice physiology, despite its importance for understanding
1262 Journal of Speech, Language, and Hearing Research • Vol. 60 • 1254–1263 • May 2017
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mechanisms of muscle function, muscle training and detrain-
ing, and aspects of fatigue resistance. Further basic research
is needed for a more complete understanding of ILSM bio-
energetics. Evaluation of the length of time muscles are
engaged combined with determination of the force required
for the target muscle behavior are two primary means to
establish bioenergetic requirements indirectly. The former
is easier to establish than the latter, given that the current
state of voice science lacks a cohesive theoretical frame-
work for determination of vocal force or power. Applied
research in the area of voice dose or load is an important
first step to quantify functional occupation-specific voice
requirements (Cleveland, Sundberg, & Stone, 2001; Folland
& Williams, 2007; Stathopoulos & Felson, 2006). From the
vocal dose literature, muscle bioenergetic frameworks can
be applied to theoretical models for voice habilitation,
which should include fatigue resistance training. Future
directions to determine the bioenergetic aspects of the ILSMs
should include more basic research to identify metabolic
profiles of the ILSMs as well as applied studies of temporal
and force/power aspects of voice requirements. Discerning
these novel aspects of voice function will allow for the
development of functionally relevant voice assessment pro-
cedures and training approaches that will advance the study
of ILSM physiology to be in closer alignment with that of
limb skeletal muscle physiology.
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