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The Role of Fiber Types in
Muscle Hypertrophy:
Implications for Loading
Strategies
Dan Ogborn, MSc, CSCS and Brad J. Schoenfeld, MSc, CSCS, CSPS
2
AU1
2
Lehman CollegAU2 e, Bronx, New YorAU3 k
ABSTRACT
EMERGING EVIDENCE SUGGESTS
THAT TYPE I FIBERS DISPLAY A
SUBSTANTIAL PROPENSITY FOR
GROWTH IF THEY ARE SELEC-
TIVELY TARGETED VIA LOW-LOAD
TRAINING. THE PURPOSE OF THIS
ARTICLE WILL BE TO REVIEW THE
RESEARCH REGARDING FIBER
TYPE–SPECIFIC HYPERTROPHY
AND DRAW EVIDENCE-BASED
CONCLUSIONS AS TO THEIR
IMPLICATIONS FOR PROGRAM
DESIGN.
INTRODUCTION
Many individuals whAU5 oresistance
traindosowiththeprimary
goal of increasing muscular
size. Current theory suggests that
exercise-induced muscle hypertrophy is
regulated by a phenomenon called me-
chanotransduction, whereby mechanical
forces are converted into chemical signals
that mediate intracellular anabolic and
catabolic pathways, ultimately leading
to a shift in muscle protein balance that
favors synthesis over degradation (42).
The net effect is an accretion of myofi-
brillar contractile proteins that augments
the diameter of individual fibers and
thereby results in an increase in whole-
muscle cross-sectional area (CSA) (28).
Both endurance-oriented type I (slow
twitch) fibers and strength-oriented
type II (fast twitch) fibers have the abil-
ity to hypertrophy. However, research
shows that the growth capacity of fast-
twitch fibers is approximately 50%
greater than that of slow-twitch fibers
(3), although a high degree of interindi-
vidual variability is seen with respect to
the extent of hypertrophic adaptation
(20). Based on this information, it may
be assumed that recruitment of type II
fibers should be the main focus of exer-
cise program design for the accretion of
muscle mass, given the enhanced rate of
hypertrophy in these fibers as compared
with type I fibers.
Despite a logical rationale, emerging
evidence suggests that such an
approach may be simplistic and per-
haps misguided, at least if the goal is
to maximize muscle size. Therefore,
the purpose of this article will be to
review the research regarding fiber
type–specific hypertrophy and draw
evidence-based conclusions as to their
implications for program design.
HYPERTROPHY OF TYPE II FIBERS
WITH HIGH-INTENSITY STRENGTH
TRAINING
Type II muscle fibers have long dis-
played superior growth after high-
intensity strength training
(1,10,11,13,14,20,31,32). These experi-
mental results are often extrapolated to
represent a growth capacity exceeding
that of type I fibers; however, it is
important to note that these findings
are specific to the training intensities
at which the study is performed and
may not apply universally across the
repetition continuum. The superior
capacity for growth of this particular
fiber type may be more a consequence
of the models we study than an intrin-
sic property of the fiber itself. In sup-
port of this hypothesis, bodybuilders
display greater type I fiber hypertrophy
than powerlifters, presumably as a
result of routinely training with higher
repetition ranges (13).
Our previous understanding of the
relationship between training intensity
and the resultant fiber type–specific
hypertrophy is best summarized by
Fry’s (13) comprehensive review of
resistance training program variables.
Using a regression analysis to assess
the intensity-related percent change
in fiber growth across various studies,
it was determined that for the majority
of training intensities above 50% of 1
repetition maximum (1RM), type II
fiber growth exceeded that of the type
I fibers. In addition, the peak growth
rate of type I fibers was lower than for
type II, regardless of training intensity.
This work is limited by the fact that
research to date has been biased
KEY WORDS:
low-intensity exercise; slow-twitch
fibers; low-load training; strength-
endurance continuum
Copyright ÓNational Strength and Conditioning Association Strength and Conditioning Journal | www.nsca-scj.com 1
toward training intensities greater than
60% of 1RM, with a lack of lower-
intensity strength training studies in
the literature (13,38). Thus, the paucity
of low-intensity resistance training
research precludes equal weighting in
analysis, predisposing results toward
higher-intensity training. Furthermore,
regression merely shows the correla-
tion between 2 variables, in this case,
fiber type–specific hypertrophy and
training intensity; it does not imply
causation.
DIRECT COMPARISONS OF
TRAINING INTENSITIES AND FIBER
TYPE–SPECIFIC HYPERTROPHY
Strength training interventions using
intensities above 50% of 1RM abound
(38); however, direct comparisons,
including low-intensity training, that
address fiber type–specific hypertro-
phy are currently lacking, and those
that have been conducted are disparate
and contradictory in their findings.
Campos et al. (10) compared 3 differ-
ent repetition ranges against a seden-
tary control group and found that
groups who performed sets with either
a 3–5 RM or 9–11 RM load to failure
produced significant growth in both
fiber types as compared with training
with 20–28 RM, where the extent of
hypertrophy did not reach statistical
significance. In agreement, Schuenke
et al. (31) found that high-intensity
training (3 36–10 RM; ;80–85% of
1RM) to failure resulted in significant
growth of all fiber types as compared
with a lack of growth after lower-
intensity training (3 320–30 RM;
;40–60% of 1RM). Interestingly, train-
ing with low intensity at a slow speed
(10 seconds concentric and 4 seconds
eccentric) induced a greater hypertro-
phic response compared with training
with a comparable resistance at tradi-
tional speed, but adaptations were less
than that seen with high-intensity
loads.
Employing a quasi within-subject
design, Mitchell et al. (24) compared
training with 3 sets at 80% of 1RM
against one set at 80% of 1RM and
3 sets with 30% of 1RM over 10 weeks,
with all groups taking every set
to concentric failure. Whole-muscle
hypertrophy was equivalent among
all training groups at completion of
the study, and fiber type–specific hyper-
trophy indicated substantial hypertrophy
in all fiber types, with no significant dif-
ferences in fiber type–specific growth
indicated. It should be noted, however,
that the low-intensity condition resulted
in an ;23% increase in type I fiber area
compared with ;16% in the high-
intensity condition. Conversely, high-
intensity training resulted in an ;15%
increase in type II fiber area compared
with ;12% in the low-intensity condi-
tion. The study was likely underpow-
ered to detect significance, suggesting
that an increase type I fiber area sub-
stantially contributed to the hypertro-
phic effects of low-intensity training.
THE INFLUENCE OF TRAINING
INTENSITY ON WHOLE-MUSCLE
HYPERTROPHY
A number of studies have compared
whole-muscle hypertrophy in low-
intensity versus high-intensity training
protocols. Holm et al. (17) employed
a within-subject design, whereby sub-
jects performed 10 sets of unilateral leg
extensions, training one leg at 70% of
1RM and the contralateral leg at 15.5%
of 1RM in a randomized, counterbal-
anced fashion. After 12 weeks, magnetic
resonance imaging (MRI) showed an
approximately 3-fold greater increase
in quadriceps muscle CSA with
higher-intensity exercise compared
with low-intensity exercise. A limitation
of the study was that training at 15.5%
of 1RM was not carried out to concen-
tric muscular failure, which has been
shown to be necessary to maximize
a hypertrophic response in low-
intensity exercise (24).
Leger et al. (23) and Lamon et al. (22)
employed a similar protocol to that of
Campos et al. (10); neither study found
significant differences in muscle CSA
between low-intensity and high-
intensity groups. The discrepancy in
results between studies may be attrib-
utable to the fact that both Leger et al.
(23) and Lamon et al. (22) evaluated
middle-aged males, who conceivably
were detrained relative to the younger
males studied by Campos et al. (10).
Another important difference between
studies was the techniques used to
measure hypertrophy. Campos et al.
(10) employed muscle biopsies, whereas
Leger et al. (23) and Lamon et al. (22)
used computerized tomography (CT).
Because CT does not allow evaluation
of differential effects on fiber typing, it is
not clear whether differences in slow-
twitch versus fast-twitch fibers played
a role in explaining the discrepancies
in these findings. Moreover, noncon-
tractile increases in sarcoplasmic pro-
teins (i.e., mitochondria, fluid, etc.)
may have contributed to the results.
This is an important consideration as
mitochondrial protein synthesis is par-
ticularly sensitive to extended time
under tension (TUT) during strength
training and may increase dispropor-
tionately as TUT and total work are
higher with low-load training (8,9).
As such, it is important to consider
the possibility that even if whole-
muscle hypertrophy is equivalent in
response to various training intensities,
the increase in CSA may be mediated
by differing cellular adaptations (28),
and muscle strength and function
may vary accordingly. This is partially
supported by the observation that
strength is increased to a greater extent
with high-intensity training (10,31),
even when whole-muscle hypertrophy
is comparable (24), although adapta-
tions independent to muscle could also
explain such a response.
Recently, Ogasawara et al. (26) found
similar increases in CSA of the triceps
brachii and pectoralis major as deter-
mined by MRI in subjects performing
training at 75% of 1RM versus 30% of
1RM. The study employed a within-
subject design, whereby participants
performed the higher-intensity exer-
cise for 12 weeks initially and, after
a 12-month washout period of detrain-
ing, performed 12 weeks of the low-
intensity exercise in a nonrandomized
fashion. Although intriguing, these
findings must be viewed with caution
as “muscle memory” via both neural
mechanisms and satellite accretion
may have influenced the results (7,32).
Type I Fiber Hypertrophy
VOLUME 0 | NUMBER 0 | MONTH 2013
2
INTERACTIONS OF LOAD AND
MOTOR UNIT RECRUITMENT
The premise behind high-intensity
training is rooted firmly in Henne-
man’s Size principle that states the
orderly recruitment of motor units dur-
ing a given task (15,16). This principle
dictates that motor units are recruited
based on their size: smaller, low-
threshold slow motor units are recruited
initially, followed by progressively
larger, higher-threshold motor units as
the force demands of the task increases.
Training with heavy loads requires sub-
stantial force production and therefore
calls upon both low- and high-threshold
motor units to maximize force. As
load (training intensity) decreases, the
required force production from the
muscle is reduced, and fewer motor
units are required to complete the lift.
Given that fibers must be recruited in to
respond and adapt to resistance exercise
(21), it seems logical to conclude that
training at very high levels of intensity is
required to maximize recruitment and
therefore muscular development.
However, this argument discounts the
role of fatigue in the stimulation of
hypertrophy and its ability to influence
motor unit recruitment. During low-
load contractions, initial motor unit
recruitment is lower than under high-
load conditions. However, as fatigue
increases, the recruitment threshold
of higher-threshold motor units is pro-
gressively reduced (2). Conceivably,
this results in the gradual recruitment
of higher threshold, presumably fast
motor units as fatigue increases. This
recruitment process provides a mecha-
nism, whereby low-intensity strength
training can activate fast-twitch motor
units and ultimately stimulate the
growth of these fibers.
The exact mechanisms, whereby
fatigue enhances high-threshold motor
unit recruitment, are not well under-
stood. It has been speculated that
results are mediated by metabolic
stress associated with exercise relying
primarily on the fast glycolytic energy
system (29). The accumulation of
hydrogen ions, increased muscle hyp-
oxia, and free radical generation all
have been implicated as playing a role
in the process (29). Regardless of the
mechanism, the fatigue-induced activa-
tion of F AU6
T fibers is believed to be an
attempt to maintain necessary levels of
force generation so that work output is
maintained (2).
Although intuitively it would seem that
a given threshold of intensity is required
to achieve recruitment of the full spec-
trum of fibers, studies to date have
failed to establish a specific percentage
of RM at which this occurs. Surface
electromyography (EMG), which pro-
vides a global measure of motor unit
activity of a given muscle, has been
used to provide an indirect measure of
motor unit recruitment during resis-
tance exercise. Cook et al. (12) recently
demonstrated that EMG amplitude of
the quadriceps femoris during knee
extension exercise to failure was signif-
icantly greater at a high intensity (70%
of 1RM) than at low intensity (20% of
1RM). This suggests that the threshold
for optimal motor unit recruitment
exceeds 20% of 1RM. In contrast,
Wernbom et al. (39) reported that peak
EMG activity was similar among 3 sets
of low-intensity (30% of 1RM) unilateral
knee extensions. In attempting to justify
the discrepancies between the studies of
Cook et al. (12) and Wernbom et al.
(39), one could infer that 30% of 1RM
represents a lower threshold for type II
recruitment. However, Suga et al. (33)
found that fiber recruitment during
blood flow–restricted training at 30%
of 1RM did not reach levels achieved
with traditional high-intensity resis-
tance exercise, as determined by
inorganic phosphate splitting via
31
P-magnetic resonance spectroscopy.
Only when blood flow–restricted
exercise was carried out at an intensity
of 40% of 1RM did P
i
peaks equate
to those associated with the high-
intensity training. Given the conflict-
ing results, it is difficult to draw any firm
conclusions as to a minimum intensity
threshold for recruiting the full spec-
trum of muscle fibers, although evi-
dence indicates that intensity below
30% of 1RM is suboptimal for inducing
substantial recruitmentofhigh-threshold
motor units.
UNDERSTANDING THE
RELATIONSHIP BETWEEN LOAD
AND TIME UNDER TENSION
The hypothesis that we have underes-
timated both the growth potential of
type I fibers and the ability of low-
intensity training to stimulate hyper-
trophy relies on 2 basic premises: (a)
that hypertrophy requires a minimum
TUT that varies with training intensity
and (b) that this TUT is greater for
type I than type II fibers. To address
this relationship, Burd et al. (9) com-
pared the protein synthetic response
after 4 sets at 3 training intensity con-
ditions: 90% of 1RM lifted to failure,
30% of 1RM to failure, and 30% of
1RM lifted such that the total work
was matched to the 90% of 1RM con-
dition. The protein synthetic response,
although of differing time course, was
similar when either 90% of 1RM or
30% of 1RM was lifted to concentric
failure; however, the low-load work-
matched condition did not stimulate
mixed, myofibrillar, and sarcoplasmic
protein synthesis to a similar extent
as the other conditions. Although the
protein synthetic response to an acute
bout of resistance exercise is not nec-
essarily indicative of long-term hyper-
trophic adaptations (3), there is some
evidence, albeit conflicting, that low-
intensity exercise can produce compa-
rable hypertrophy with higher-intensity
exercise provided sets are taken to fail-
ure (24,26).
Methodology may at least partially
explain the divergent findings regard-
ing the effects of training intensity on
fiber type–specific and whole-muscle
hypertrophy. The studies that do not
equate total intrasession work tend to
show similar growth between high-
and low-intensity exercises (24,26),
with the exception of Schuenke et al.
(31) who displayed greater hypertro-
phy when training at a high intensity.
Conversely, studies that do equate
work show a hypertrophic advantage
for high-intensity exercise (10,17). It is
also important to consider the contri-
bution of muscular failure to these
Strength and Conditioning Journal | www.nsca-scj.com 3
experimental findings. Whereas the
majority of studies identify concentric
failure as the end point for the set
(10,24,31), Holm et al. (17) did not,
and only the low-intensity condition
trained to failure in Ogasawara et al.
(26). Although fatigue may contribute
to the hypertrophic response (29,30), it
is currently unknown how the relation-
ship between training intensity and
hypertrophy compare when exercise
is fatiguing but terminated before the
point of concentric failure.
Nevertheless, given that low-intensity
resistance exercise seems to preferen-
tially increase hypertrophy of type I
fibers (24), it is logical to conclude that
an increased TUT is necessary to fully
stimulate these fibers. This would be
consistent with the endurance-oriented
nature of slow-twitch fibers that renders
them resistant to fatigue.
DO TYPE I FIBERS HAVE A LIMITED
GROWTH CAPACITY?
It remains questionable as to whether
type I fibers have the ultimate hyper-
trophic potential of type II fibers.
There is evidence that they do not.
Studies evaluating the relationship
between CSA and mitochondrial den-
sity suggest that the growth of a given
muscle fiber is achieved at the expense
of its endurance capacity (36). This
implies that the smaller size of highly
oxidative slow-twitch fibers is an evo-
lutionary design constraint, limiting
their inherent ability to hypertrophy
in comparison with fast-twitch fibers
with a low oxidative capacity (36).
One way that type I fiber hypertrophy
may be self-limiting is via competition
between anabolic and catabolic intra-
cellular signaling pathways. Expression
of muscle ring finger and muscle atro-
phy F-box—ubiquitin ligases that mediate
protein degradation—is approximately
2-fold higher in oxidative versus nonox-
idative fibers (36). Moreover, there is evi-
dence that type I fibers have a reduced
ability to increase phosphorylation of
ribosomal protein kinase S6 (p70S6K)
after resistance exercise compared with
type II fibers, which in turn blunts their
protein translational capacity (19).
p70S6K is a downstream effector in
the mTOR pathway, and its activation
via mechanical stimuli has been deemed
critical to the hypertrophic response
(41). These events are consistent with
the “AMPK-PK AU7
B switch” hypothesis,
whereby signaling is switched to either
a catabolic AMPK/PGC-1a–oran
anabolic PKB-TSC2-mTOR–dominated
state depending on whether the imposed
demand is endurance or resistance based
(5). Although signaling interactions are
unquestionably more complex than
asimpleswitchmechanism, especially
given the stimulation of AMPK with tra-
ditional resistance exercise (19), research
does suggest that the endurance-
oriented nature of type I fibers provides
a greater inclination to turnover rates
that favor proteins involved in metabo-
lism (i.e., mitochondrial proteins) over
structural muscle protein (i.e., myofibril-
lar proteins) (36).
Another potential limiting factor in
type I growth is their ability to increase
satellite cell proliferation. Satellite cells
are muscle stem cells that reside
between the basal lamina and the sar-
colemma, which remain dormant in
the resting state. When stimulated by
mechanical stress, however, satellite
cells generate precursor cells (myo-
blasts) that proliferate and ultimately
fuse to existing cells, providing the
necessary agents for remodeling of
muscle tissue (35,40). In addition, sat-
ellite cells are able to donate their
nuclei to the existing muscle fibers,
enhancing their capacity for protein
synthesis (6,25). In young, untrained
subjects, satellite cell number is approx-
imately equal between slow- and fast-
twitch fiber types (18). However, there
is evidence tha AU8
tmixedmodesofexer-
cise training, even of an endurance-
oriented nature, results in a greater
increase of the satellite cell pool in
type II fibers (37), indicating a greater
long-term growth potential for these
fiber types. The heightened exercise-
induced expression of the protein
MyoD in type II fibers (4), which is pre-
dominantly responsible for upregulating
satellite proliferation and thus facilitates
the formation of new myoblasts, could
be a potential mechanism to explain
their enhanced satellite cell response.
This suggests that over time, fast-
twitch fibers may have a favorable pre-
disposition to growth because of an
enhanced capacity to synthesize new
contractile proteins.
Considering the aforementioned fac-
tors, evidence suggests that although
type I fibers possess significant growth
potential, they may have a lower ceil-
ing for hypertrophy in comparison
with type II fibers. Unfortunately, no
study to date has directly examined
this hypothesis. Furthermore, as the
study documenting enhanced phos-
phorylation of p70S6K only relied on
higher training intensities, it remains to
be determined whether low-intensity
strength training can augment protein
synthetic signaling pathways (24) in
type I fibers specifically to a greater
extent than high-intensity training in
type II fibers (19). This topic should
be explored in future research.
PRACTICAL APPLICATIONS
Based on the current body of research,
there is emerging evidence indicating
that type I fibers can substantially
contribute to overall muscle CSA.
Research also suggests that low-load
resistance exercise may help to maxi-
mize type I fiber hypertrophy, pro-
vided that training is carried out to
concentric muscular failure (24). From
a practical perspective, the following
recommendations can be made.
If one’s goal is simply to maximize
overall muscle mass, exercise prescrip-
tions should include training across
a wide spectrum of repetition ranges.
Higher-intensity exercise seems neces-
sary to fully stimulate fast-twitch fiber
growth (13), whereas lower-intensity
exercise preferentially enhances hyper-
trophy in slow-twitch fibers (24). A
periodized approach combining high-
and low-intensity training may help
ensure an optimal hypertrophic response
in the full continuum of fiber types. Both
linear and nonlinear models are viable
approaches here, as neither has been
showntobesuperiortotheotherinthis
regard. Thus, intensities can be varied
Type I Fiber Hypertrophy
VOLUME 0 | NUMBER 0 | MONTH 2013
4
within and/or across multiple training
sessions or by alternating target repeti-
tion zones every few microcycles. Train-
ing loads can easily be manipulated
based on the characteristics of the exer-
cises within a training session, favoring
high-load training on multi-joint exer-
cises like the squat and deadlift, saving
higher repetition ranges for single-joint,
isolation type exercises that may be bet-
ter suited to lighter training loads.
Although training percentages or
repetition ranges can be varied in
a periodized manner, advanced train-
ing techniques may provide additional
hypertrophic benefit. Drop sets, where
training load is progressively decreased
on subsequent sets with little to no rest
once the point of fatigue or technical
failure is achieved at each training
load, may provide the best of both
worlds (27). Training load can be max-
imized initially to capitalize on type II
fiber activation; however, as fatigue sets
in, training loads can be progressively
decreased to increase the TUT to max-
imally stimulate the type I fibers. In
addition, rest-pause training, where a
set with a given training load is extended
beyond the point of fatigue by taking
small rests within the set, may provide
a similar benefit by increasing the dura-
tion of loading. Care must be taken
when using these techniques to balance
the need for increased muscle recruit-
ment and TUT to promote optimal
hypertrophy against the potential for ele-
vated levels of fatigue and overuse (27).
On the other hand, if hypertrophy
is a means to maximize strength,
then higher-intensity loads should be
favored over lighter loads, as gains in
strength are greater with high-load
training as compared with low-load
training (10) even when a comparable
hypertrophic response occurs (24). If
strength is to be maximized in specific
exercises, as in sports such as power-
lifting, higher-intensity training is
essential because of the specificity of
strength (13) and the fact that exercise
technique can differ across the training
intensity continuum (34). Fiber-type
specificity plays a role in this process.
Fast-twitch fibers are innervated by
larger motor neurons compared with
their slow-twitch counterparts, allowing
for enhanced high force production.
Because of the smaller size of the neu-
rons associated with type I fibers, they
simply cannot cycle fast enough to carry
out tasks involving high levels of force.
Hence, the major focus here should be
on high-load training (greater than
;75% of 1RM).
Conflicts of Interest and Source of Funding:
The authors report no conflicts of interest
and no source of fundin AU4g.
Dan Ogborn is
currently com-
pleting a postdoc-
toral fellowship
and physiother-
apy degree at
McMaster
University.
Brad
Schoenfeld is
a lecturer in exer-
cise science at
CUNY AU9Lehman
College and is
director of their
human perfor-
mance laborator AU10y.
REFERENCES
1. Aagaard P, Andersen JL, Dyhre-Poulsen P,
Leffers AM, Wagner A, Magnusson SP,
Halkjaer-Kristensen J, and Simonsen EB.
A mechanism for increased contractile
strength of human pennate muscle in
response to strength training: Changes in
muscle architecture. J Physiol (Lond) 534:
613–623, 2001.
2. Adam A and De Luca CJ. Recruitment
order of motor units in human vastus
lateralis muscle is maintained during
fatiguing contractions. J Neurophysiol 90:
2919–2927, 2003.
3. Adams GR and Bamman MM.
Characterization and regulation of
mechanical loading induced compensatory
muscle hypertrophy. Compr Physiol.AU11
4. Aguiar AF, Vechetti-Ju
´nior IJ, Alves de
Souza RW, Castan EP, Milanezi-Aguiar RC,
Padovani CR, Carvalho RF, and Silva MDP.
Myogenin, MyoD and IGF-I regulate muscle
mass but not fiber-type conversion during
resistance training in rats. Int J Sports Med
34: 293–301, 201 3.
5. Atherton PJ, Babraj J, Smith K, Singh J,
Rennie MJ, and Wackerhage H. Selective
activation of AMPK-PGC-1alpha or PKB-
TSC2-mTOR signaling can explain specific
adaptive responses to endurance or
resistance training-like electrical muscle
stimulation. FASEB J 19: 786–788, 2005.
6. Barton-Davis ER, Shoturma DI, and
Sweeney HL. Contribution of satellite cells
to IGF-I induced hypertrophy of skeletal
muscle. Acta Physiol Scand 167: 301–
305, 1999.
7. Bruusgaard JC, Johansen IB, Egner IM,
Rana ZA, and Gundersen K. Myonuclei
acquired by overload exercise precede
hypertrophy and are not lost on detraining.
Proc Natl Acad Sci U S A 107: 15111–
15116, 2010.
8. BurdNA,AndrewsRJ,WestDWD,
Little JP, Cochran AJR, Hector AJ,
Cashaback JGA, Gibala MJ, Potvin JR,
Baker SK, and Phillips SM. Muscle time
under tension during resistance exercise
stimulates differential muscle protein
sub-fractional synthetic responses in
men. J Physiol (Lond) 590: 351–362,
2012.
9. Burd NA, West DWD, Staples AW,
Atherton PJ, Baker JM, Moore DR,
Holwerda AM, Parise G, Rennie MJ,
Baker SK, and Phillips SM. Low-load
high volume resistance exercise
stimulates muscle protein synthesis
more than high-load low volume
resistance exercise in young men.
PLoS One 5: e12033, 2010.
10. Campos GER, Luecke TJ, Wendeln HK,
Toma K, Hagerman FC, Murray TF,
Ragg KE, Ratamess NA, Kraemer WJ, and
Staron RS. Muscular adaptations in
response to three different resistance-
training regimens: Specificity of repetition
maximum training zones. Eur J Appl Physiol
88: 50–60, 2002.
11. Charette SL, McEvoy L, Pyka G,
Snow-Harter C, Guido D, Wiswell RA, and
Marcus R. Muscle hypertrophy response to
resistance training in older women. J Appl
Physiol 70: 1912–1916, 1991.
12. Cook SB, Murphy BG, and Labarbera KE.
Neuromuscular function after a bout of
low-load blood flow-restricted exercise.
Med Sci Sports Exerc 45: 67–74, 2013.
13. Fry AC. The role of resistance exercise
intensity on muscle fibre adaptations.
Sports Med 34: 663–679, 2004.
Strength and Conditioning Journal | www.nsca-scj.com 5
14. Harber MP, Fry AC, Rubin MR, Smith JC,
and Weiss LW. Skeletal muscle and
hormonal adaptations to circuit weight
training in untrained men. Scand J Med Sci
Sports 14: 176–185, 2004.
15. Henneman E, Somjen G, and
Carpenter DO. Excitability and inhibitability
of motoneurons of different sizes.
J Neurophysiol 28: 599–620, 1965.
16. Henneman E, Somjen G, and
Carpenter DO. Functional significance of
cell size in spinal motoneurons.
J Neurophysiol 28: 560–580, 1965.
17. Holm L, Reitelseder S, Pedersen TG,
Doessing S, Petersen SG, Flyvbjerg A,
Andersen JL, Aagaard P, and Kjaer M.
ChangesinmusclesizeandMHC
composition in response to resistance
exercise with heavy and light loading intensity.
J Appl Physiol 105: 1454–1461, 2008.
18. Kadi F, Charifi N, and Henriksson J. The
number of satellite cells in slow and fast
fibres from human vastus lateralis muscle.
Histochem Cell Biol 126: 83–87, 2006.
19. Koopman R, Zorenc AHG, Gransier RJJ,
Cameron-Smith D, and van Loon LJC.
Increase in S6K1 phosphorylation in
human skeletal muscle following resistance
exercise occurs mainly in type II muscle
fibers. Am J Physiol Endocrinol Metab
290: E1245–E1252, 2006.
20. Kosek DJ, Kim J-S, Petrella JK, Cross JM,
and Bamman MM. Efficacy of 3 days/wk
resistance training on myofiber hypertrophy
and myogenic mechanisms in young vs. older
adults. J Appl Physiol 101: 531–544, 2006.
21. Kraemer WJ and Ratamess NA.
Fundamentals of resistance training:
Progression and exercise prescription.
Med Sci Sports Exerc 36: 674–688, 2004.
22. Lamon S, Wallace MA, Le
´ger B, and
Russell AP. Regulation of STARS and its
downstream targets suggest a novel
pathway involved in human skeletal muscle
hypertrophy and atrophy. J Physiol (Lond)
587: 1795–1803, 2009.
23. Le
´ger B, Cartoni R, Praz M, Lamon S,
De
´riaz O, Crettenand A, Gobelet C,
Rohmer P, Konzelmann M, Luthi F, and
Russell AP. Akt signaling through GSK-
3beta, mTOR and Foxo1 is involved in
human skeletal muscle hypertrophy and
atrophy. J Physiol (Lond) 576: 923–933,
2006.
24. Mitchell CJ, Churchward-Venne TA,
West DWD, Burd NA, Breen L, Baker SK,
and Phillips SM. Resistance exercise load
does not determine training-mediated
hypertrophic gains in young men. J Appl
Physiol 113: 71–77, 2012.
25. Moss FP and Leblond CP. Satellite cells as
the source of nuclei in muscles of growing
rats. Anat Rec 170: 421–435, 1971.
26. Ogasawara R, Loenneke JP, Thiebaud RS,
and Abe T. Low-load bench press training
to fatigue results in muscle hypertrophy
similar to high-load bench press training.
Int J Clin Med 4: 114–121, 2013.
27. Schoenfeld B. The use of specialized
training techniques to maximize muscle
hypertrophy. Strength Cond J 33: 60–65,
2011.
28. Schoenfeld BJ. The mechanisms of muscle
hypertrophy and their application to
resistance training. J Strength Cond Res
24: 2857–2872, 2010.
29. Schoenfeld BJ. Potential mechanisms for
a role of metabolic stress in hypertrophic
adaptations to resistance training. Sports
Med 2013 doi: 10.1007/s40279-013-
0017-1.
30. Schott J, McCully K, and Rutherford OM.
The role of metabolites in strength training.
II. Short versus long isometric contractions.
Eur J Appl Physiol Occup Physiol 71:
337–341, 1995.
31. Schuenke MD, Herman JR, Gliders RM,
Hagerman FC, Hikida RS, Rana SR,
Ragg KE, and Staron RS. Early-phase
muscular adaptations in response to slow-
speed versus traditional resistance-training
regimens. Eur J Appl Physiol 112: 3585–
3595, 2012.
32. Staron RS, Leonardi MJ, Karapondo DL,
Malicky ES, Falkel JE, Hagerman FC, and
Hikida RS. Strength and skeletal muscle
adaptations in heavy-resistance-trained
women after detraining and retraining.
J Appl Physiol 70: 631–640, 1991.
33. Suga T, Okita K, Morita N, Yokota T,
Hirabayashi K, Horiuchi M, Takada S,
Omokawa M, Kinugawa S, and Tsutsui H.
Dose effect on intramuscular metabolic
stress during low-intensity resistance
exercise with blood flow restriction. J Appl
Physiol 108: 1563–1567, 2010.
34. Swinton PA, Swinton PA, Stewart A,
Stewart A, Agouris I, Agouris I, Keogh JW,
Keogh JW, Lloyd R, and Lloyd RA
Biomechanical analysis of straight and
hexagonal barbell deadlifts using
submaximal loads. J Strength Cond Res
25: 2000–2009, 2011.
35. Toigo M and Boutellier U. New
fundamental resistance exercise
determinants of molecular and cellular
muscle adaptations. Eur J Appl Physiol 97:
643–663, 2006.
36. van Wessel T, de Haan A, van der
Laarse WJ, and Jaspers RT. The muscle
fiber type-fiber size paradox: Hypertrophy
or oxidative metabolism? Eur J Appl
Physiol 110: 665–694, 2010.
37. Verney J, Kadi F, Charifi N, Fe
´asson L,
Saafi MA, Castells J, Piehl-Aulin K, and
Denis C. Effects of combined lower body
endurance and upper body resistance
training on the satellite cell pool in elderly
subjects. Muscle Nerve 38: 1147–1154,
2008.
38. Wernbom M, Augustsson J, and Thomee
´R.
The influence of frequency, intensity,
volume and mode of strength training on
whole muscle cross-sectional area in
humans. Sports Med 37: 225–264, 2007.
39. Wernbom M, Ja
¨rrebring R, Andreasson MA,
and Augustsson J. Acute effects of blood
flow restriction on muscle activity and
endurance during fatiguing dynamic knee
extensions at low load. JStrengthCondRes
23: 2389–2395, 2 009.
40. Zammit PS. All muscle satellite cells are
equal, but are some more equal than
others? J Cell Sci 121: 2975–2982,
2008.
41. Zanchi NE and Lancha AH. Mechanical
stimuli of skeletal muscle: Implications on
mTOR/p70s6k and protein synthesis. Eur J
Appl Physiol 102: 253–263, 2008.
42. Zou K, Meador BM, Johnson B,
Huntsman HD, Mahmassani Z, Valero MC,
Huey KA, and Boppart MD. The
a₇b₁-integrin increases muscle
hypertrophy following multiple bouts of
eccentric exercise. J Appl Physiol 111:
1134–1141, 2011.
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