J Appl Physiol 126: 278–285, 2019.
First published November 1, 2018; doi:10.1152/japplphysiol.00601.2018.
RESEARCH ARTICLE
Cardiovascular responses during isometric exercise following lengthening and
shortening contractions
Jeremy D. Seed,1 Benjamin St. Peters,1 Geoffrey A. Power,1 and X Philip J. Millar1,2
1
Department of Human Health and Nutritional Sciences, University of Guelph, Guelph, Ontario, Canada; and 2Toronto
General Research Institute, Toronto General Hospital, Toronto, Ontario, Canada
Submitted 5 July 2018; accepted in final form 29 October 2018
Seed JD, St. Peters B, Power GA, Millar PJ. Cardiovascular
responses during isometric exercise following lengthening and short-
ening contractions. J Appl Physiol 126: 278 –285, 2019. First pub-
lished November 1, 2018; doi:10.1152/japplphysiol.00601.2018.—
The present study investigated the effects of prior lengthening or
shortening contractions on cardiovascular responses during isometric
exercise. We utilized the history dependence of skeletal muscle,
where active 2-s lengthening or shortening before an isometric con-
traction can increase [residual force enhancement (RFE)] or decrease
[force depression (FD)] force production. Matching torque output
between RFE and FD conditions yields lower and higher electro-
myography (EMG) values, respectively. In study 1, heart rate and
perceived exertion (PE; Borg10) were measured in 20 participants
during 20-s isometric plantar flexion contractions at low (16 ⫾ 4%
MVC)-, moderate (50 ⫾ 5% MVC)-, and high (88 ⫾ 7% MVC)-
intensity. In study 2, heart rate and blood pressure were measured in
14 participants during 2-min isometric plantar flexion contractions
(40% MVC). In both studies, torque output was held constant between
FD and RFE conditions resulting in differences in soleus EMG
activity (P ⬍ 0.05). In study 1, PE was lower during the RFE
condition (P ⬍ 0.01), while increases in heart rate were similar
between FD and RFE at low (⌬2 ⫾ 8 vs. 3 ⫾ 6 beats/min, P ⬎ 0.99)
and moderate (⌬14 ⫾ 9 vs. 14 ⫾ 9 beats/min, P ⬎ 0.99) intensity but
smaller during RFE at high intensity (⌬35 ⫾ 13 vs. 29 ⫾ 13 beats/
min, P ⫽ 0.004). In study 2, heart rate responses were smaller in the
RFE condition following the initial 20-s period; diastolic blood
pressure responses were smaller during the last 80 s. A 2-s active
change in muscle length before an isometric contraction can influence
heart rate and blood pressure responses; however, these differences
appear to be modulated by both intensity and duration of the contrac-
tion.
NEW & NOTEWORTHY Using the history dependence of isomet-
ric force to alter maximal torque production and motor unit activation
between residual force enhancement and force depression conditions,
we observed that heart rate responses were different between condi-
tions during a subsequent 20-s high-, but not low- or moderate-,
intensity isometric contraction. A 2-min moderate-intensity contrac-
tion revealed time-dependent effects on heart rate and diastolic blood
pressure. Active 2-s shortening and lengthening before an isometric
contraction can influence the cardiovascular responses.
blood pressure; exercise; heart rate; history dependence of force;
isometric
Address for reprint requests and other correspondence: P. J. Millar,
ANNU 348A, 50 Stone Rd. East, Guelph, ON, Canada, N1G2W1 (e-mail:
pmillar@uoguelph.ca).
278 8750-7587/19 Copyright © 2019 the American Physiological Society
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INTRODUCTION
The relative intensity of a muscle contraction is considered
to be the primary determinant for the magnitude of the cardio-
vascular response to isometric exercise (16). The influence of
maximal torque production (absolute intensity) (24, 25) and the
influence of muscle mass or limb differences (23, 24, 31) have
also been shown to be secondary factors. One factor that has
not been considered is the influence of prior lengthening or
shortening of the muscle before the contraction. The history
dependence of force phenomenon describes the capacity to
increase [termed residual force enhancement (RFE)] or de-
crease [termed force depression (FD)] torque production im-
mediately following active, brief (e.g., 2 s) lengthening or
shortening, respectively, as compared with a purely isometric
contraction at the same muscle length and level of activation
(9). Whether these acute (and temporary) changes in torque
production can modulate the cardiovascular response to exer-
cise is unknown.
The history dependence of force occurs independent of
contraction intensity, and when torque output is matched be-
tween an isometric contraction and the RFE or FD states,
differences in electromyographic (EMG) activity are observed
(13, 28). The mechanisms responsible for the acute changes in
contractile strength are not fully established. The RFE state
demonstrates a greater contribution of passive torque to overall
torque production, which has been suggested to involve Ca2⫹-
dependent stiffening of the giant protein titin (10). As a result,
less active torque is required to produce similar torque levels to
those of a purely isometric contraction, ultimately contributing
to less motor unit activation (13, 28). In contrast, it has been
proposed that the FD state is associated with a stress-induced
inhibition of cross bridges in the newly formed actin-myosin
overlap zone following shortening (18), requiring higher levels
of descending drive and/or motor unit activation to achieve
similar isometric torque production (13, 28).
The purpose of this study was to investigate the effects of the
history dependence of force phenomenon on the control of
heart rate and blood pressure during exercise. To investigate,
we conducted two separate studies. Study 1 examined the
intensity-dependent contributions of RFE and FD states on the
control of heart rate and perceived exertion (PE) during 20-s
isometric plantar flexion contractions at low [16 ⫾ 4% maxi-
mal voluntary contraction (MVC)], moderate (50 ⫾ 5%
MVC), and high (88 ⫾ 7% MVC) intensity. Study 2 examined
the temporal contributions of RFE and FD states on the control
of heart rate and blood pressure during a 2-min isometric
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 CARDIOVASCULAR EFFECTS OF PRIOR LENGTHENING AND SHORTENING
plantar flexion contraction at 40% MVC. Based on prior data
that the cardiovascular response to isometric exercise is influ-
enced by the relative contraction intensity (16), we hypothe-
sized that the RFE state (increased torque production condi-
tion) would be associated with smaller increases in heart rate
and/or blood pressure when compared with the FD state across
all intensities and time points.
METHODS
Participants
We recruited 27 healthy young men and women through advertise-
ments on campus, five of which completed both studies. All women
self-reported being in the early follicular phase of their menstrual
cycle. Females using oral contraceptives (n ⫽ 7) were studied within
the first 5 days of their placebo pill phase. All participants were free
of cardiovascular, metabolic, or neuromuscular diseases, nonmedi-
cated, nonsmoking, in sinus rhythm, and without recent injury to the
right lower limb used to complete the exercise. All participants
abstained from caffeine 12 h, and strenuous exercise and alcohol
consumption 24 h, before experimental testing. The study was ap-
proved by the University of Guelph Research Ethics Board, and all
participants provided informed written consent before participation.
Experimental Protocol
Both studies were completed in the same light- and temperature-
controlled laboratory. In study 1 and study 2, participants entered the
laboratory and anthropometrics were collected. Next, they were seated
with their right foot attached to a dynamometer footplate (Humac
NORM; Computer Sports Medicine Solutions, Stoughton, MA). The
participant sat upright and was held stable with both torso and hip
restraining straps. The knee was immobilized by strapping the distal
thigh to a cushioned support fixed to the dynamometer. The restraints
were tightened to minimize extraneous movements and limit the need
for coactivation of other muscles to maintain their position. Par-
ticipants were instructed to keep their upper body and other limb
completely relaxed. The right foot was secured to a dorsiflexor/
plantarflexor adaptor with an inelastic Velcro strap over the distal
metatarsals and a ratcheting binding placed over the ankle in line
with the malleoli. The maximum range of motion at the ankle was
from 80 to 140° (90°, neutral ankle angle). Torque, angular
position, and stimulus trigger data were sampled at 1,000 Hz using
a 12-bit analog-to- digital converter (PowerLab System 16/35;
ADInstruments, Bella Vista, Australia).
EMG. In both studies, raw EMG data were recorded at 2,000 Hz,
and 10-Hz high-pass and 1,000-Hz low-pass filtered (ADInstruments).
To measure plantar flexor muscle activity, one EMG electrode was
placed ~2 cm inferior to the lateral border of gastrocnemius on the
soleus and a reference electrode on the calcaneal tendon. Dorsiflexor
muscle antagonist activity was measured by placing one EMG elec-
trode ~2 cm lateral and 7 cm inferior to the tibial tuberosity on the
tiblialis anterior and a reference electrode on the tendon of tibialis
anterior at the distal tibia. A fifth ground electrode was placed on the
center of the patella. All EMG electrode sites were prepared by
shaving and cleaning the skin with alcohol wipes.
All voluntary EMG was normalized by stimulating the deep fibular
and tibial nerves with a bar electrode to produce maximal compound
action potentials. Briefly, the deep fibular nerve was located by
palpating posteriorly from the head of the fibula. The tibial nerve was
identified by locating the distal tendon of the semitendinosus muscle
and moving laterally while palpating deep into the popliteal fossa. A
single pulse from a constant current high-voltage stimulator (model
DS7AH; Digitimer, Welwyn Garden City, Hertfordshire, UK) was
used for peripheral nerve stimulation. The voltage was set at 400 V
with a pulse width of 200 ␮s. The current was gradually increased
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279
until max M-wave amplitude (M-max) was achieved to ensure the
activation of all motor units.
Participants performed two to three MVCs. During each MVC, the
participants were instructed to perform plantar flexion as fast and as
hard as possible, with visual feedback provided as a torque trace on a
computer monitor. During all MVCs, strong verbal encouragement
was also provided. To examine the level of voluntary activation (VA)
during plantar flexion MVCs, the interpolated twitch technique was
used (21). Participants were instructed to contract as fast and as hard
possible and received stimulations before the start of contraction,
during the plateau phase of contraction, and 1–2 s after complete
relaxation. Torque produced by tibial nerve stimulation during the
plateau phase of the contraction was compared with the torque
following stimulation at rest 1–2 s postcontraction. The current used
for the interpolated twitch technique was the same current that
produced M-max. A torque tracing was visible to participants, and
they were all verbally encouraged during the contraction. A minimum
of 95% activation was required for participants to be included in both
studies. The level of VA was assessed as follows: %VA ⫽ [1–
(superimposed twitch torque/reference twitch torque)] ⫻ 100. A min-
imum of a 5-min rest was provided before continuing with the
experimental protocol.
Study 1
Twenty participants (23 ⫾ 3 yr, 13 males and 7 females) were
recruited. After participants were seated and attached to the dyna-
mometer footplate, EMG was instrumented as described above. Next,
participants were familiarized with the Borg CR10 scale and in-
structed to think about how strenuous the upcoming maximal volun-
tary contraction would feel and to consider this to represent a 10 on
the scale. Participants were instructed to perform a 10-s maximal
isometric plantar flexion contraction. Verbal encouragement was
given throughout the MVC. The average torque produced between 7.5
and 8 s of the MVC was set as the high-intensity condition for the
trials that followed. Peak torque was not used for the high-intensity
condition as participants were unable to maintain this level for 20 s
during pilot testing. At the end of the MVC, subjects were reminded
that the contraction they performed was a 10 on the Borg CR10 scale.
Participants underwent instrumentation to collect continuous beat-
to-beat heart rate using single-lead electrocardiography (Lead II;
1,000 Hz; ADInstruments). Following a 10-min period of quiet seated
rest, each participant performed three types of plantar flexion contrac-
tions: FD, isometric, and RFE, in that order, over three different
exercise intensities. This protocol follows standard in vitro history
dependence of force experimental designs (15, 28), such that if there
was an effect of fatigue, it would negatively bias against our hypoth-
esis, leading to increased EMG activity during RFE relative to FD.
The lengthening/shortening contractions were divided into three dis-
tinct yet continuous phases; a 2-s preactivation, a 2-s lengthening/
shortening, and a 16-s steady-state isometric. The shortening contrac-
tions (FD) were initiated at an ankle angle of 80° for 2 s and shortened
at 15°/s over 2 s into the 110° isometric steady-state for 16 s. The
lengthening contractions (RFE) were initiated at an ankle angle of
140° for 2 s and lengthened at 15°/s over 2 s into the 110° isometric
steady state for 16 s (Fig. 1). The three exercise intensities were low
(20% of high intensity), moderate (60% of high intensity), and high
(in relation to the MVC). The order of the exercise intensities was
randomized.
A torque guideline was visible on the screen as well as a torque
trace, but participants were blinded to the intensity since the torque
values on the monitor were covered and the scale was adjusted so
the distance between the baseline torque and guideline was the
same between trials. Participants were given 5-min rest between
each contraction. The foot was strapped into place 1 min before
starting the baseline period (the 3-min mark of the rest period) to
avoid any perturbations during the baseline. At the 4-min mark, the
280 CARDIOVASCULAR EFFECTS OF PRIOR LENGTHENING AND SHORTENING

Fig. 1. Representative figure of the torque, joint

angle, and right soleus muscle activation (EMG)
produced during passive movement (column A), pre-
activation, and active muscle lengthening residual
force enhancement (RFE) condition] or shortening
[force depressed (FD) condition] (column B), and a
16 s isometric plantar flexion contraction (column C).
Of note, participants were required to hold the iso-
metric contraction for an additional 1–2 s to ensure
constant torque production throughout the exercise
period.

1-min baseline recording commenced, and after the baseline, a 20-s
contraction was performed. Torque, EMG, and ECG were collected
during each 20-s contraction. Immediately following a contraction,
participants were given a copy of the Borg CR10 scale and asked to
rate how strenuous and difficult the contraction felt. If a contraction
felt more strenuous or difficult than the initial MVC, subjects were
instructed that values ⬎10 were acceptable.
Data and statistical analysis. The change in heart rate was calcu-
lated in each contraction by subtracting the average of the 1-min
baseline from the average heart rate in the last 10 s of each contrac-
tion. Raw EMG was analyzed over the same 10-s period as the heart
rate and the root-mean-square EMG (EMGRMS) was calculated.
EMGRMS in FD and RFE was expressed as a percentage of the
M-max. All statistical analyses were performed on GraphPad Prism
(GraphPad Software). Two-way repeated measures ANOVAs were
performed to detect the presence of an interaction between intensity
and the contraction condition (RFE or FD) on heart rate, PE, and
EMGRMS. Significant effects were probed using Bonferroni post hoc
procedures with correction for multiple comparisons. A paired t-test
was performed to examine resting heart rate between RFE and FD
baseline periods, as well as, to examine potential heart rate changes
throughout the baseline periods in anticipation of the exercise (i.e.,
first vs. last 20-s epochs). Significance was considered to be P ⬍ 0.05,
and data are presented as means ⫾ SD, unless otherwise specified.
Study 2
Fifteen participants (23 ⫾ 2 yr, 14 men and 1 women) were
recruited. After participants were seated and attached to the dyna-
mometer footplate, EMG was instrumented as described above. Par-
ticipants were instructed to perform two 5-s maximal plantar flexion
isometric contractions. Verbal encouragement was given throughout

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 CARDIOVASCULAR EFFECTS OF PRIOR LENGTHENING AND SHORTENING
the MVC and the max torque produced between the two contractions
was used to determine 40% MVC for the trials.
Following the MVC protocol, participants were instrumented to
measure continuous heart rate (lead II electrocardiography) and beat-
to-beat blood pressure (Finometer MIDI; Finapres). The latter col-
lected using photoelectric plethysmography on the left middle finger.
Both signals were recorded at a sampling frequency of 1,000 Hz
(Powerlab, ADInstruments, Colorado Springs, CO). Participants were
given a 5-min period of quiet rest before the start of the baseline
period for the FD plantar flexion contraction and muscle metaboreflex
test. All continuous variables were measured for the entirety of the
test, which consisted of a 2-min baseline period and a 2-min plantar
flexion contraction with the right leg at 40% MVC. For the FD
contraction, there was a 2-s isometric phase at an ankle angle of 80°,
a 2-s shortening phase to 110°, and a 116-s isometric phase. After a
15-min rest, participants performed the RFE plantar flexion contrac-
tion. For the RFE trials, a 2-s isometric phase at an ankle angle of 140°
was followed by a 2-s lengthening phase to 110°, and a 116-s
isometric phase. Upon completing the tests, and following a 5-min
rest, participants performed another MVC to ensure they were not
fatigued. Based on the results of study 1, we did not complete a purely
isometric contraction in this study to further reduce the risk of fatigue.
Data and statistical analysis. The changes in heart rate and blood
pressure were analyzed in 20-s segments as this was the duration of
the contraction in study 1; the change was calculated by subtracting
the 2-min baseline average from the average of the 20-s segments
during the contraction. EMG was analyzed as EMGRMS and expressed
as a percentage of the M-max. All statistical analyses were performed
using GraphPad Prism (GraphPad Software). Two-way repeated mea-
sures ANOVAs were used to detect an interaction between time and
the contraction condition on blood pressure and heart rate. A paired
t-test was performed to determine a difference in activation between
contraction conditions. Significant effects were probed using Bonfer-
roni post hoc procedures with correction for multiple comparisons. A
paired t-test was performed to determine a difference in heart rate and
blood pressure between RFE and FD baseline periods. Significance
was considered to be P ⬍ 0.05, and data are presented as
means ⫾ SD, unless otherwise specified.
RESULTS
Study 1
Participants were normotensive (110/73 ⫾ 8/6 mmHg), had
a body-mass index below 30 kg/m2 (24.1 ⫾ 3.4 kg/m2 [range:
19.4 –29.5 kg/m2]), and had an average peak MVC of
62.5 ⫾ 24.4 N·m. The low-, moderate-, and high-intensity
contractions were completed at 16 ⫾ 4, 50 ⫾ 5, and 88 ⫾ 7%
of the peak MVC torque, respectively. Torque production was
not statistically different (all P ⬎ 0.05) between RFE and FD
conditions during the low (10.0 ⫾ 4.2 vs. 9.9 ⫾ 4.2 N·m-),
moderate (30.9 ⫾ 12.2 vs. 31.2 ⫾ 12.0 N·m)-, and high
(48.5 ⫾ 17.3 vs. 47.4 ⫾ 16.8 N·m)-intensity contractions.
Baseline heart rates were also similar (All P ⬎ 0.05) between
RFE and FD conditions during the low (70 ⫾ 11 vs.
71 ⫾ beats/min)-, moderate (69 ⫾ 9 vs. 70 ⫾ 10 beats/min)-,
and high (69 ⫾ 9 vs. 69 ⫾ 9 beats/min)-intensity bouts. Fur-
thermore, heart rate did not differ (P ⬎ 0.05) between the first
and last 20 s epochs at any baseline time point (i.e., no
anticipatory effects).
A significant interaction was observed in EMGRMS (P ⬍
0.001; Fig. 2), with less activation during the RFE vs. FD
condition at the moderate (P ⬍ 0.0001)- and high (P ⬍
0.0001)- intensity contraction but not during the low-intensity
contraction (P ⫽ 0.08). The percent difference in EMGRMS
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281
Fig. 2. Right soleus muscle activation (EMGRMS) as a percentage of the
maximum M-wave amplitude (M-max), indicating maximal motor unit acti-
vation, between residual force enhancement (RFE) and force depressed (FD)
conditions at low-, moderate-, and high-intensity isometric plantar flexion
contractions. The low-, moderate-, and high-intensity contractions were com-
pleted at 16 ⫾ 4, 50 ⫾ 5, and 88 ⫾ 7% of maximal voluntary contraction
(MVC), respectively. Data were obtained in 20 participants and are expressed
as means ⫾ SE.
between RFE and FD was 21, 19, and 15% at the low-,
moderate-, and high-intensity contraction, respectively. PE
demonstrated a condition effect being higher in FD than RFE
contractions (P ⫽ 0.007; Fig. 3A). As expected an effect
of-intensity was also observed with PE increasing as intensity
increased (P ⬍ 0.0001; Fig. 3A). The increases in heart rate
(Fig. 3B) were higher during the FD compared with RFE
conditions at the high-intensity contraction (35 ⫾ 13 vs.
29 ⫾ 13 beats/min, P ⫽ 0.004) but not different at the low- or
moderate-intensity contraction (both P ⬎ 0.99).
Study 2
Participants were normotensive (110/71 ⫾ 8/7 mmHg), had
an average body-mass index below 30 kg/m2 (25.0 ⫾ 3.7
kg/m2 [range: 19.9 –32.2 kg/m2]), and had an average peak
MVC of 70.3 ⫾ 18.5 N·m. Torque production was not statis-
tically different (P ⬎ 0.05) between RFE and FD conditions
(26.3 ⫾ 7.2 vs. 26.0 ⫾ 7.2 N·m). Baseline heart rate (P ⫽ 0.7)
did not differ between RFE and FD conditions (65 ⫾ 9 vs.
65 ⫾ 8 beats/min), but systolic pressure (132 ⫾ 11 vs.
136 ⫾ 11 mmHg, P ⫽ 0.05) and diastolic pressure (73 ⫾ 10
vs. 76 ⫾ 9 mmHg, P ⫽ 0.03) were slightly higher during the
RFE baseline. There was no difference (P ⬎ 0.05) in heart rate
between the first and last 20 s of the baseline period for both
FD and RFE conditions (i.e., no anticipation effects).
As observed in study 1, there was a significant difference in
EMGRMS between RFE and FD during 2 min of plantar flexion
(P ⫽ 0.01). There were significant interactions observed for the
changes in heart rate (P ⫽ 0.02; Fig. 4A) and systolic (P ⫽
0.02; Fig. 4B) and diastolic (P ⫽ 0.03; Fig. 4C) blood pressure.
Heart rate was lower with RFE at 40, 60, 100, and 120 s of
contraction (All P ⬍ 0.05) compared with FD, without a
difference at 80 s (P ⫽ 0.06). Systolic blood pressure was
lower with RFE only at the 80-s time point (P ⬍ 0.05), while
diastolic blood pressure was lower during RFE at 60, 80, 100,
and 120 s of contraction (All P ⬍ 0.05).
282 CARDIOVASCULAR EFFECTS OF PRIOR LENGTHENING AND SHORTENING

Similarly, diastolic blood pressure responses were larger with

the FD versus RFE condition, primarily in the last 80-s of the
contraction. The current findings demonstrate that brief 2-s
active lengthening and shortening can produce both intensity
(study 1)- and time (study 2)-dependent effects on cardiovas-
cular responses during subsequent isometric contractions.
History Dependence of Isometric Force
The history dependence of isometric force describes the
capacity for brief active lengthening or shortening to influence
subsequent isometric torque production. This phenomenon has

Fig. 3. Perceived exertion (PE; A) and the change in heart rate (B) between
residual force enhancement (RFE) and force depressed (FD) conditions at
low-, moderate-, and high-intensity isometric plantar flexion contractions. The
low, moderate, and high intensity contractions were completed at 16 ⫾ 4,
50 ⫾ 5, and 88 ⫾ 7% of maximal voluntary contraction (MVC), respectively.
Data were obtained in 20 participants and are expressed as means ⫾ SE. AU,
arbitrary units.

DISCUSSION

The present study examined the influence of 2-s active

lengthening or shortening contractions on the cardiovascular
responses to subsequent isometric exercise. In agreement with
prior work using the history dependence of force paradigm (13,
28), EMG was lower in the RFE state compared with the FD
state in both studies; highlighting consistent differences in
motor unit pool activation and descending central motor drive
across each-intensity and contraction duration. In accordance,
PE was lower in the RFE state paralleling the difference in
electrical muscle activation. Interestingly, the changes in heart
rate were similar between the RFE and FD states during low
(16 ⫾ 4% MVC)- and moderate (50 ⫾ 5% MVC)-intensity
contractions but differed by 6 beats/min during the high-
intensity (88 ⫾ 7% MVC) contraction. To determine whether
these results were impacted by the short duration of the
isometric exercise, we completed a second study using a 2-min
isometric plantar flexion contraction at 40% MVC. These
Fig. 4. The change in heart rate (A), systolic (B), and diastolic (C) blood
results replicated the observation that heart rate was not dif- pressure during 2-min of 40% plantar flexion isometric contraction in the
ferent between the RFE and FD conditions during the initial 20 residual force enhancement (RFE) and force depressed (FD) conditions. Data
s of exercise onset but found consistent differences thereafter. were obtained in 14 participants and are expressed as means ⫾ SE.

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 CARDIOVASCULAR EFFECTS OF PRIOR LENGTHENING AND SHORTENING
been described in both single-fiber and intact whole muscle,
but the implications are not well understood and need to be
reconciled with the currently accepted paradigm of cross-
bridge theory (13). One common observation is that when
matched for torque production in the RFE and FD states,
parallel alterations in EMG are observed (13, 28), which are
considered to be the result of differences in central drive (13).
We observed consistent differences in electrical muscle activ-
ity between the RFE and FD states in all of our conditions
supporting the alteration in torque production with our model.
Perceived Exertion
In line with our hypothesis, we observed that PE was
reduced across the RFE condition. The mechanisms responsi-
ble for altering a participant’s perception of effort remain
debated (27), although our parallel reduction in EMG is con-
sistent with the model that PE is mediated by corollary dis-
charge, in which descending motor drive simultaneously stim-
ulates regions in the sensory cortex (17, 27). Such a model does
not preclude an indirect role of muscle afferent feedback in
adjusting motor output but states that afferent mechanisms are
not responsible directly for the feelings of effort (27). Studies
blocking skeletal muscle group III/IV afferent feedback
through the administration of intrathecal fentanyl have pro-
duced inconsistent results, not impacting PE during moderate-
intensity isometric handgrip or cycling exercise (3), while
decreasing PE during high-intensity dynamic exercise (1). Our
model did not block afferent feedback from exercising muscle
per se but instead sought to maintain a consistent level by
controlling muscle force production. Therefore, the differences
in PE between conditions at all intensities were likely due to
the differences in descending drive observed in EMG.
Cardiovascular Responses to Isometric Contractions
The understanding that relative intensity of an isometric
contraction is responsible for the magnitude of the cardiovas-
cular response (16) led us to hypothesize that heart rate and
blood pressure responses would be lower in the RFE than FD
conditions. Interestingly, despite differences in EMG and PE
across each of the exercise intensities in study 1, heart rate was
only altered between the RFE and FD conditions at the highest
intensity (88 ⫾ 7% MVC). This suggests an intensity-depen-
dent threshold for the contributions of active lengthening and
shortening on the control of heart rate during exercise, which
could relate to the degree of afferent feedback, motor drive, or
PE. To examine the temporal effects of RFE and FD conditions
on the cardiovascular responses, we also examined heart rate
and blood pressure responses over a 2-min moderate-intensity
isometric contraction. Here, it was found that the increases in
heart rate were greater in the FD condition after the initial 20-s
epoch at exercise onset (i.e., a time-dependent interaction).
Similarly, small but consistent differences in diastolic blood
pressure also demonstrated a time-dependent change.
The autonomic nervous system plays an important role in the
regulation of heart rate and blood pressure during exercise (6).
More specifically, modulation of sympathetic and parasympa-
thetic outflow occurs through a combination of afferent feed-
back from peripheral chemoreceptors (32), arterial and cardio-
pulmonary baroreceptors (5), mechanically- and metabolically
sensitive group III/IV afferents in skeletal muscle (20, 22), and
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283
feedforward control from higher brain regions, termed central
command (8). The present use of the history dependence of
isometric force to alter EMG while maintaining torque produc-
tion mirrors a number of experimental models designed to
isolate the influence of central command (7, 30). For example,
Goodwin et al. (8) applied vibration to agonist or antagonist
muscles to evoke reflex excitation or inhibition of motor
neurons during an isometric bicep or tricep contraction. When
constant torque production was maintained, it was found that
antagonist muscle activation (presumed increase in central
command) resulted in larger blood pressure, heart rate, and
ventilation responses during low-intensity contractions (~15–
35% MVC). However, this study had a number of potential
confounders, 1) only the minute-to-minute changes in cardio-
respiratory measures were examined; 2) EMG responses be-
tween the conditions were not reported; and 3) participants
reported that the vibration-assisted contraction (presumed de-
crease in central command) was not subjectively easier. Fur-
thermore, this experimental model can be technically challeng-
ing (26) and assumes no cardiovascular effects of external
muscle vibration, which we have shown can acutely influence
muscle sympathetic nerve activity at rest (33). Transcutaneous
electrical stimulation of group I and II afferent feedback can
also modulate muscle sympathetic and blood pressure re-
sponses to static handgrip exercise (11).
Prior work comparing cardiovascular responses during con-
stant-force versus constant-EMG static knee extension, another
model proposed to study the contributions of central command,
has also demonstrated delayed (time-dependent) differences in
heart rate and blood pressure during exercise (7, 30). However,
these, and the present, findings are at odds with data demon-
strating that central command is involved in a near instanta-
neous contribution to the heart rate response during exercise
(34). Given the knowledge that central command can influence
heart rate in anticipation of exercise (4), we considered that
differences across the baseline period used to calculate the
change score may have influenced our results. In contrast, we
observed that heart rate was not altered over any of the RFE
and FD baseline periods (i.e., no anticipation effects). One
important consideration that may influence the early cardio-
vascular responses in both study 1 and 2 is that participants
were only provided ~5 s notice of when each contraction was
going to commence. Motor intention before execution has been
suggested to have an role in mediating early cardiovascular
responses as heart rate increases more rapidly following arbi-
trary (self-selected) versus cued one-legged cycling (12). As a
result, we speculate that the initial 20 s of exercise onset served
as the first involvement of central mechanisms, and given the
small changes in EMG between conditions, adjustments were
made thereafter based on peripheral afferent feedback from
group III/IV skeletal muscle afferents shown to alter central
command (1, 2).
Although muscle torque production was held constant be-
tween FD and RFE contractions, similar to the tendon vibration
model (8, 26), we cannot rule out a role of peripheral skeletal
muscle afferents in mediating the differences in cardiovascular
responses. The specific relationships between muscle force or
activation on stimulating group III (primarily mechanically
sensitive) and group IV (primarily chemically sensitive) skel-
etal muscle afferents have not been established, nor has the
impact of a prior lengthening or shortening contraction on
284 CARDIOVASCULAR EFFECTS OF PRIOR LENGTHENING AND SHORTENING
mechanically sensitive afferent sensitivity or responsiveness.
Additionally, it is unclear whether the history dependence of
force phenomenon is coupled with an underlying metabolic
alteration. Single fibers isolated from rabbit psoas muscle and
activated by high Ca2⫹ demonstrate that a FD contraction has
similar ATPase activity per unit of force compared with a
purely isometric contraction of identical fiber length and acti-
vation (14), although, in a similar set-up, a 40-s RFE contrac-
tion may have less ATPase activity per unit of force (15).
However, at the whole muscle level in humans, a 30% MVC
contraction of the gastrocnemius medialis exhibits similar
muscle oxygen consumption, as assessed via near-infrared
spectroscopy between RFE and isometric states (29). Classi-
cally, the muscle metaboreflex is considered to be the primary
contributor to the progress rise in blood pressure (and muscle
sympathetic outflow) during an isometric contraction (19).
However, in study 2, the differences in heart rate and diastolic
blood pressure between RFE and FD contractions were con-
sistent and did not increase over time, arguing against a role of
the muscle metaboreflex in mediating the observed differences
between the RFE and FD conditions.
Methodological Considerations
We acknowledge several limitations. First, although partic-
ipants were instructed to avoid contraction of other muscle
groups, it is possible participants were contracting knee and or
hip extensors during the experimental trials; however, it is
likely that any coactivation was similar between contractions at
a given intensity and prior work has shown that the muscle
contracting at the higher relative intensity determines the
hemodynamic response (16). Second, we purposefully did not
randomize the order of FD and RFE within each intensity due
to the inherent confounder of potential fatigue. For example,
although we provided 5 min of rest between contractions in
study 1, and 15 min of rest between contractions in study 2, if
the FD state was performed last it would have been difficult to
discern whether the changes in EMG were related to the history
dependence of force phenomenon or fatigue. With the RFE
state being completed last in each trial, if fatigue were present
it would reduce the magnitude difference in EMG between the
states and bias against the present differences. Third, we did
not collect respiratory variables that may contribute to the
hemodynamic differences during exercise. Finally, it is impor-
tant to consider that the present model produced ~10 –20%
differences in EMG activity, and thus large magnitude differ-
ences in cardiovascular measures were not expected.
Conclusion
In conclusion, we used the history dependence of isometric
force as a novel paradigm to acutely modulate muscle torque
production. Matching torque output during a subsequent iso-
metric contraction demonstrated that a brief 2-s lengthening or
shortening contraction could alter EMG, PE, and cardiovascu-
lar responses. Our results demonstrate a difference in heart rate
responses between the RFE and FD conditions during a brief
20-s high-, but not low- or moderate-, intensity isometric
contraction. However, during a 2-min contraction at a moder-
ate intensity, with a sustained difference in EMG, a persistent
difference in heart rate was observed following the initial 20-s
period of exercise onset. Whether these observations reflect
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alterations in central command or peripheral afferent feedback
is unclear and warrants further study.
GRANTS
This research was supported by Natural Science and Engineering Research
Council of Canada Discovery Grant (to P. J. Millar and G. A. Power), Canada
Foundation for Innovation Grant 34379 (to P. J. Millar), and Ontario Ministry
of Research, Innovation, and Science Grant 34379 (to P. J. Millar).
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the authors.
AUTHOR CONTRIBUTIONS
J.D.S., G.A.P., and P.J.M. conceived and designed research; J.D.S., B.S.P.,
G.A.P., and P.J.M. performed experiments; J.D.S., and B.S.P. analyzed data;
J.D.S., B.S.P., G.A.P., and P.J.M. interpreted results; J.D.S., G.A.P., and
P.J.M. prepared figures; G.A.P., and P.J.M. drafted manuscript; J.D.S., G.A.P.,
and P.J.M. edited and revised manuscript; J.D.S., B.S.P., G.A.P., and P.J.M.
approved final version of manuscript.
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