- Autonomic Neuroscience

Autonomic Neuroscience: Basic and Clinical 162 (2011) 35–41
Contents lists available at ScienceDirect
Autonomic Neuroscience: Basic and Clinical
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / a u t n e u
Comparison of the effects of aerobic and resistance training on cardiac autonomic
adaptations in ovariectomized rats
Larissa C.R. Silveira, Geisa C.S.V. Tezini, Débora S. Schujmann, Jaqueline M. Porto,
Bruno R.O. Rossi, Hugo C.D. Souza ⁎
Exercise Physiology Laboratory of the Department of Biomechanics, Medicine and Rehabilitation, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil
a r t i c l e
i n f o
Article history:
Received 28 September 2010
Received in revised form 14 January 2011
Accepted 16 February 2011
Keywords:
Physical training
Ovariectomy
Cardiac autonomic control
a b s t r a c t
We have compared the effects of two types of physical training on the cardiac autonomic control in
ovariectomized and sham-operated rats according to different approaches: double autonomic blockade (DAB)
with methylatropine and propranolol; baroreflex sensibility (BRS) and spectral analysis of heart rate
variability (HRV).
Wistar female rats (± 250 g) were divided into two groups: sham-operated and ovariectomized. Each group
was subdivided into three subgroups: sedentary rats, rats submitted to aerobic trained and rats submitted to
resistance training.
Ovariectomy did not change arterial pressure, basal heart rate (HR), DAB and BRS responses, but interfered
with HRV by reducing the low-frequency oscillations (LF = 0.20–0.75 Hz) in relation to sedentary shamoperated rats. The DAB showed that both types of training promoted an increase in the predominance of vagal
tonus in sham-operated rats, but HR variations due to methylatropine were decreased in the resistance
trained rats compared to sedentary rats. Evaluation of BRS showed that resistance training for sham-operated
and ovariectomized rats reduced the tachycardic responses in relation to aerobic training. Evaluation of HRV
in trained rats showed that aerobic training reduced LF oscillations in sham-operated rats, whereas resistance
training had a contrary effect. In the ovariectomized rats, aerobic training increased high frequency
oscillations (HF = 0.75–2.5 Hz), whereas resistance training produced no effect.
In sham-operated rats, both types of training increased the vagal autonomic tonus, but resistance training
reduced HF oscillations and BRS as well. In turn, both types of training had similar results in ovariectomized
rats, except for HRV, as aerobic training promoted an increase in HF oscillations.
© 2011 Elsevier B.V. All rights reserved.
1. Introduction
Epidemiological studies have shown that aerobic physical training
has beneficial effects on morbidity and mortality resulting from
cardiovascular diseases (Tsatsoulis and Fountoulakis, 2006; Warburton
et al., 2006). In women, the regular practice of physical exercises is
especially favourable, mainly after menopause (Bonaiuti et al., 2002),
when estrogen reduction contributes to an increase in the incidence of
such diseases (Gutkowska et al., 2007).
Part of these beneficial effects is the result of important cardiovascular adaptations. Such adaptations are characterized by decrease in
basal heart rate (HR) and intrinsic heart rate (IHR) of cardiac pacemaker
(De Angelis et al., 2004; Tezini et al., 2009), left ventricle eccentric
hypertrophy (Garciarena et al., 2009), increase in ejection volume,
increase in cardiac debt during exercise (Fenning et al., 2003),
⁎ Corresponding author at: Department of Biomechanics and Rehabilitation, School
of Medicine of Ribeirão Preto, University of São Paulo, 14049-900, Ribeirão Preto, SP,
Brazil. Tel.: +55 16 3602 4416; fax: +55 16 3602 4413.
E-mail address: [email protected] (H.C.D. Souza).
1566-0702/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.autneu.2011.02.003
improvement in baroreflex sensibility (Souza et al., 2007), and mainly,
adaptations in the cardiac autonomic control, which are characterized
by both decreased sympathetic autonomic influence and increased
vagal influence on the heart (Carter et al., 2003; Souza et al., 2009; Tezini
et al., 2009).
On the other hand, little is known about the cardiovascular
benefits of resistance training. The literature shows that this type of
exercise has been used as anti-hypertensive therapy as well as for
control of other chronic–degenerative diseases of metabolic origin
such as obesity (Ibañez et al., 2005; Warner et al., 2010) and diabetes
mellitus (Svacinová et al., 2008), yielding very promising results.
However, evidence showing the action of this type of exercise on
cardiovascular autonomic control is still poor. The few studies existing
in the literature have reported very contradictory results as they had
addressed different physiological conditions and applied different
protocols, thus not allowing a proper comparison of the results
obtained (Selig et al., 2004; Collier et al., 2009; Hu et al., 2009).
In this sense, because of the lack of solid evidence regarding the
effects of resistance training on the cardiovascular autonomic control
also apply to estrogen deficiency, our objective was to investigate and
36
L.C.R. Silveira et al. / Autonomic Neuroscience: Basic and Clinical 162 (2011) 35–41
compare the effects of aerobic and resistance physical training on the
cardiovascular autonomic adaptations in ovariectomized rats by using
different approaches; evaluation of autonomic tonic control by means
of pharmacological blockade; baroreflex sensitivity; and evaluation of
cardiovascular autonomic modulation by analyzing both heart rate
variability and systolic arterial pressure.
through the animal's back. Twenty-four hours after the surgical
procedures, AP was measured in conscious rats kept in a quiet
environment. AP was recorded with a pressure transducer (MLT0380;
ADInstruments), and the amplified signal (ML110; ADInstruments)
was fed to a computer acquisition system (PowerLab 8/30; ADInstruments). Mean AP (MAP) and heart rate (HR) were calculated from
arterial pulse pressure.
2. Methods
2.5. Sympathovagal tonus and intrinsic rate of the cardiac pacemaker
All experimental procedures involved in this study were reviewed
and approved by the Animal Care and Use Committee.
The experiments were performed using female Wistar rats (240–
260 g) that were housed in a room at 21 °C with a 12 h light/dark
cycles and allowed free access to tap water and standard rat chow. The
rats were divided into six experimental groups: sedentary shamoperated rats (n = 12), trained sham-operated rats with aerobic
exercise by swimming (n = 12), trained sham-operated rats with
resistance exercise (n = 12), sedentary ovariectomized rats (n = 12),
ovariectomized trained rats with aerobic exercise by swimming
(n = 12) and ovariectomized trained rats with resistance exercise
(n = 12).
Assessment of the influence of autonomic tonus, sympathetic and
parasympathetic, in the HR determination was investigated by
administrating propranolol (5 mg/kg) and methylatropine (4 mg/kg),
respectively. After recording the basal HR for 30 min, methylatropine
was injected in half of the rats of each group, and HR was recorded
during the next 15 min to assess the effect of vagal blockade on HR.
Propranolol was then injected in the same rats, and HR was recorded for
another 15 min to determine the intrinsic HR (IHR). In the other half of
the rats, the methylatropine–propranolol sequence was reversed to
propranolol–methylatropine, following the same recording procedure
(15 min each) for each drug as in the previous sequence used to
determine the IHR. Data from the methylatropine–propranolol and
propranolol–methylatropine sequences were pooled to provide basal
HR (before any drugs) and IHR.
2.2. Ovariectomy
2.6. Baroreflex sensitivity
At 10 weeks of age, rats were anaesthetized (250 mg/kg,i.p.
tribromoethanol) and a small abdominal incision was made. The
ovaries were then located and a silk thread was tightly tied around the
oviduct, including the ovarian blood vessels. The oviduct was
sectioned and the ovary removed. The skin and muscle wall were
then sutured with silk thread. After surgery, the rats received an
injection of antibiotics (40,000 U/kg penicillin G procaine IM). Sham
rats were submitted to simulated ovariectomy according to the same
procedures described for ovariectomized rats, except for oviduct
section and ovary removal. The rats remained in individual cages for
post-surgical recovery during a period of 14 days.
Changes in MAP were elicited by alternating bolus injections of
phenylephrine (0.1 to 16.0 μg/kg) promoting bradycardic reflex
responses and sodium nitroprusside (0.4 to 64.0 μg/kg) promoting
tachycardic reflex responses. MAP and HR were measured before and
immediately after injection of phenylephrine (or sodium nitroprusside) when the AP achieved a new steady-state level. The two
parameters were then allowed to return to baseline, after which the
next injection was given. A total of at least five increases and five
decreases in MAP of different degrees were elicited in each rat.
Changes in MAP and HR were plotted and analyzed by means of linear
regression analysis, which calculated the slope (gain) of the
regression line obtained by the best-fit points relating changes in
MAP and HR.
2.1. Animals
2.3. Aerobic exercise
The program of physical training consisted of swimming exercises
conducted in a glass aquarium (100 cm long, 80 cm wide, and 80 cm
high) containing heated water (30 °C). The program was divided into
two phases: the first phase consisted of a 2-week adaptation,
beginning with a 10-minute swimming session that was gradually
increased to 45 min for 6 days per week. The second phase consisted
of a 10-week swimming training program in which the rats had 1hour training for 6 days per week.
2.4. Resistance training
The physical resistance training was applied according to protocol
already described (Hornberger and Farrar, 2004), with gradual load
increase during the 10-week period of training. Prior to the resistance
training itself, the rats were submitted to a 2-week adaptation
program. After this adaptation period, the training was performed
3 days a week on an alternate-day basis, with the rats executing
climbing procedures 6–7 times a day with 2-minute intervals
between each repetition.
2.4.1. Experimental protocol
On the sixth day of the last week, under tribromoethanol
anesthesia (250 mg/kg intraperitoneal), femoral venous and arterial
catheters (PE-50 soldered to PE-10) filled with heparinized saline
(500 IU/mL) were inserted into the animals and were exteriorized
2.7. Spectral analysis
The baseline AP and HR recorded during a 40-minute period were
processed by customized computer software that applies an algorithm to detect cycle-to-cycle inflection points in the pulsatile AP
signal, thus determining beat-by-beat values of systolic and diastolic
pressures. Beat-by-beat pulse interval (PI) series from the pulsatile AP
signal were also generated by measuring the length of time between
adjacent systolic waves. From the baseline 40-minute recording
period, the time series of PI and systolic AP (SAP) were divided into
contiguous segments of 300 beats, overlapping by half. After calculating the mean value and the variance of each segment, these were
submitted to a model-based autoregressive spectral analysis as
described elsewhere (Malliani et al., 1991; Rubini et al., 1993; Task
Force, 1996). Briefly, a modeling of the oscillatory components
presented in stationary segments of a beat-by-beat time series of
SAP and PI was calculated based on Levinson–Durbin recursion, with
the model order chosen according to Akaike's criterion (Malliani et al.,
1991). This procedure allows an automatic quantification of the centre
frequency and power of each relevant oscillatory component present
in the time series. The oscillatory components were labeled as having
very low (0.01–0.19 Hz), low (LF; 0.20–0.75 Hz), or high (HF; 0.75–
2.50 Hz) frequency. The power of the HF component of heart rate
variability (HRV) was expressed in absolute units, whereas the LF
component of HRV was expressed in normalized units, obtained by
L.C.R. Silveira et al. / Autonomic Neuroscience: Basic and Clinical 162 (2011) 35–41
calculating the percentage of the LF and HF variability with respect to
the total power after subtracting the power of the very-low-frequency
component (frequencies b 0.20 Hz). The ratio between LF and HF was
calculated to obtain the index of autonomic modulation balance for
determining the cardiac variability.
2.8. Statistical analysis
Data are reported as mean ± SEM. The results of hemodynamic
values, pharmacological blockade with methylatropine and propranolol, baroreflex sensitivity and spectral analysis were assessed by twoway ANOVA followed by Tukey's post hoc test. Significant differences
were considered at p b 0.05.
3. Results
Table 1 and Fig. 1 (A,B,C) show the basal values for AP and HR as
well as absolute and percentage HR values following pharmacological
blockade with propranolol and methylatropine. Fig. 1A shows that the
groups of sedentary, sham-operated and ovariectomized rats, had
similar values for basal HR, cardiac autonomic tonus balance and IHR
following double blockade. Fig. 1B shows that sham-operated rats
submitted to different physical trainings presented decrease in their
basal HR and IHR, in association with an increase in the percentage of
vagal autonomic tonus compared to sedentary rats. However, when
both types of training were compared, the groups of resistance
training exhibited higher values for HR. In turn, Fig. 1C shows that
ovariectomized rats, submitted to different types of training, also had
a decrease in basal HR and IHR compared to sedentary rats, but no
change in the cardiac autonomic tonus balance was observed.
Table 1 also lists the gains for baroreflex sensibility to bradycardiac
and tachycardic responses following administration of phenylephrine
and sodium nitroprussiate, respectively. The results showed that
sedentary ovariectomized rats exhibited no change in the baroreflex
sensibility compared to the sham-operated sedentary ones. Aerobic
physical training, either in sham-operated or ovariectomized rats, has
also promoted no such alteration. On the other hand, the resistance
physical training reduced the gain in baroreflex sensibility to
tachycardic responses in sham-operated rats compared to sedentary
and aerobic trained ones. In turn, ovariectomized rats submitted to
resistance training had a decreased baroreflex sensibility gain only in
relation to aerobic trained rats.
37
Table 2 and Fig. 2 (A,B,C) show the spectral analysis mean values
for HRV (pulse interval) in all groups studied. In sedentary rats,
ovariectomy changed neither total variance (Fig. 2A) nor HF
oscillations (Fig. 2C), but LF oscillations were found to be decreased
(Fig. 2B). Fig. 2A also shows that both types of training reduced total
variance in sham-operated rats, although in ovariectomized rats
aerobic training promoted an increase. Fig. 2B shows that aerobic
physical training promoted reduction in LF oscillations in shamoperated rats, whereas resistance training promoted an increase
instead. It was also shown that ovariectomized rats had no alteration.
Fig. 2C shows that resistance physical training promoted reduction in
HF oscillations only in sham-operated rats, whereas aerobic physical
training promoted increase only in ovariectomized rats. Analysis of
LF/HF ratio showed that sham-operated rats submitted to aerobic
training had reduced values, while in rats submitted to resistance
training showed values increased compared to sedentary rats. No
difference was observed in ovariectomized rats in relation to LF/HF
ratio.
Table 2 also lists the results of the analysis of SAP variability,
showing that no difference was found between the groups studies
according to the parameters evaluated.
4. Discussion
Our study has shown that ovariectomy influenced neither tonic
cardiac autonomic control nor baroreflex sensibility but promoted
changes in heart rate variability, which was evidenced by decrease in LF
oscillations. In sham-operated rats, the aerobic physical training
promoted relevant cardiac autonomic adaptations characterized by
greater predominance of vagal tonic component in the determination of
basal HR, associated with decrease in LF oscillations. In turn, resistance
physical training did not promote the same effects of the aerobic
training in sham-operated rats, and under some approaches evaluated
the results were worrying, as the reduction in baroreflex sensibility and
imbalance in HRV modulation. On the other hand, ovariectomized rats
had very different results following either aerobic or resistance physical
training, exhibiting neither sympathovagal balance nor baroreflex
sensitivity. Nevertheless, it was observed significant increase in HF
oscillations following aerobic physical training.
Ovariectomy has neither caused alterations in the basal values of
AP and HR nor promoted modifications in the tonic cardiac autonomic
control, thus corroborating results of previous studies (Liang et al.,
1997; Nickenig et al., 1998; Reckelhoff et al., 2000.; Sáinz et al., 2004;
Table 1
HR, MAP, autonomic pharmacological blockade and baroreflex sensitivity in sham-operated and ovariectomized rats divided into three groups: sedentary; aerobic trained; and
resistance trained.
Sham
Sedentary
Values
HR, bpm
MAP, mm Hg
Tonic autonomic control
HR after methylatropine, bpm
ΔHR after methylatropine, bpm
% HR after methylatropine
HR after propranolol, bpm
ΔHR after propranolol, bpm
% HR after propranolol, bpm
IHR, bpm
Baroreflex sensitivity
Bradycardic gain, bpm/mm Hg
Tachycardic gain, bpm/mm Hg
Ovariectomized
Aerobic
Resistance
371 ± 3
95 ± 3
329 ± 4a
96 ± 2
349 ± 1a,
99 ± 3
443 ± 6
72 ± 7
67 ± 1
330 ± 7
−41 ± 7
36 ± 3
366 ± 2
396 ± 6a
67 ± 12
86 ± 3a
319 ± 5
−10 ± 4a
14 ± 2a
339 ± 3a
397 ± 3a
48 ± 5a
82 ± 1a
338 ± 2b
−11 ± 2a
18 ± 1a
344 ± 3a
−1.43 ± 0.17
2.85 ± 0.02
−1.30 ± 0.14
3.29 ± 0.32
Sedentary
b
−1.51 ± 0.26
2.03 ± 0.15a, b
All values are expressed as mean ± SEM. HR, heart rate; MAP, mean arterial pressure; IHR, intrinsic heart rate.
a
P b 0.05 vs. Sham Sedentary Rats.
b
P b 0.05 vs. Sham Aerobic Trained Rats.
c
P b 0.05 vs. Ovariectomized Sedentary Rats.
d
P b 0.05 vs. Ovariectomized Aerobic Trained Rats.
Aerobic
Resistance
361 ± 4
97 ± 2
325 ± 4c
99 ± 2
328 ± 3c
93 ± 1
431 ± 10
70 ± 11
65 ± 2
323 ± 4
−38 ± 14
35 ± 2
359 ± 5
396 ± 10c
71 ± 16
71 ± 3
295 ± 4c
−30 ± 5
29 ± 1.5
328 ± 4c
400 ± 9c
72 ± 16
70 ± 4
298 ± 5c
−30 ± 7
30 ± 3
337 ± 4c
−1.71 ± 0.16
2.73 ± 0.28
−1.34 ± 0.12
3.21 ± 0.14
−1.43 ± 0.11
2.57 ± 0.1d
38
L.C.R. Silveira et al. / Autonomic Neuroscience: Basic and Clinical 162 (2011) 35–41
Fig. 1. Graphic representation of basal heart rate (HR; black line), intrinsic heart rate (IHR; dashed line) and respective percentage variations of HR after parasympathetic blockade
with methylatropine (M; upper boundary of the white rectangle) and sympathetic blockade with propranolol (P; lower boundary of the dark gray rectangle) in sham-operated and
ovariectomized sedentary rats (A); sham-operated rats divided into sedentary, aerobic trained, and resistance trained groups (B); and ovariectomized rats divided into sedentary,
aerobic trained, and resistance trained groups (C). aP b 0.05 vs. Sham Sedentary Rats; bP b 0.05 vs. Sham Aerobic Trained Rats; cP b 0.05 vs. Ovariectomized Sedentary Rats.
Tezini et al., 2009). However, some authors demonstrated that
ovariectomy might promote an increase in the arterial pressure
(Dantas et al., 1999; Hernández et al., 2000; Chappell et al., 2003;
Irigoyen et al., 2005; Souza et al., 2007; Sanches et al., 2009). This
discrepant outcome needs to be further investigated, but it is possible
that methodological procedures are involved such as time elapsed
between ovariectomy and experimental physical training (Flues et al.,
2010). Another interesting finding is that no change in baroreflex
Table 2
Spectral parameters of PI and SAP calculated from time series using autoregressive spectral analysis in sham-operated and ovariectomized rats divided into three groups: sedentary;
aerobic trained; and resistance trained.
Sham
Baseline values
PI, ms
SAP, mm Hg
Spectral parameters: PI
Variance, ms2
LF, nu
HF, ms2
LF–HF ratio
Spectral parameters: SAP
Variance, mm Hg2
LF, mm Hg2
HF, mm Hg2
Ovariectomized
Sedentary
Aerobic
Resistance
Sedentary
Aerobic
Resistance
0.161 ± 0.002
115 ± 2
0.182 ± 0.003a
113 ± 3
0.172 ± 0.002a, b
112 ± 2
0.166 ± 0.003
120 ± 4
0.184 ± 0.003c
111 ± 2
0.182 ± 0.002c
116 ± 4
13.3 ± 1.7
33 ± 4
5.9 ± 0.8
0.58 ± 0.11
7.2 ± 0.9a
9 ± 2a
4.1 ± 0.5
0.12 ± 0.02a
6.9 ± 1.2a
53 ± 6a, b
2.1 ± 0.2a, b
1.38 ± 0.26a, b
11.4 ± 1.7
23 ± 3a
5.6 ± 0.9
0.34 ± 0.08
18.1 ± 2.4c
26 ± 3
8.9 ± 1.2c
0.39 ± 0.05
8.2 ± 1.3d
33 ± 5
3.8 ± 0.6d
0.64 ± 0.16
15 ± 1.6
10.9 ± 1.3
2.1 ± 0.3
12.8 ± 1.5
9.4 ± 1.2
1.8 ± 0.3
10.6 ± 1.3
7.7 ± 1.3
1.5 ± 0.2
11 ± 0.9
7.9 ± 0.7
1.6 ± 0.1
12.6 ± 1.1
9.0 ± 0.9
1.8 ± 0.2
10.1 ± 1.8
6.8 ± 1.5
1.8 ± 0.3
All values are expressed as mean ± SEM. PI, pulse internal; SAP, systolic arterial pressure; LF, low frequency; HF, high frequency; nu, normalized units.
a
P b 0.05 vs. Sham Sedentary Rats.
b
P b 0.05 vs. Sham Aerobic Trained Rats.
c
P b 0.05 vs. Ovariectomized Sedentary Rats.
d
P b 0.05 vs. Ovariectomized Aerobic Trained Rats.
L.C.R. Silveira et al. / Autonomic Neuroscience: Basic and Clinical 162 (2011) 35–41
39
Fig. 2. (A) Total variance of pulse interval. (B) Spectral power density of pulse interval in the LF bands in normalized units (nu). (C) Spectral power density of pulse interval in high
frequency (HF) bands in absolute units in sham-operated and ovariectomized rats divided into three subgroups: sedentary; aerobic trained; and resistance trained. aP b 0.05 vs. Sham
Sedentary Rats; bP b 0.05 vs. Sham Aerobic Trained Rats; cP b 0.05 vs. Ovariectomized Sedentary Rats; dP b 0.05 vs. Ovariectomized Aerobic Trained Rats.
sensibility was observed in the ovariectomized rats, which was
pointed out elsewhere (Flues et al., 2010; Dias-Silva et al., 2009).
Nevertheless, these same studies have also reported that a decrease in
the baroreflex sensibility was accompanied by AP increase in
ovariectomized rats, an event that might be the key cause of
imbalance in the reflex control of heart rate observed by these
studies. On the other hand, ovariectomy promoted changes in the HRV
modulation in sedentary rats, which was characterized by the
reduction on LF oscillations. A previous study using single blockade
of cardiac autonomic components in ovariectomized rats showed that
LF oscillations were little affected by methylatropine but very reduced
following administration of propranolol (Tezini et al., 2009), thus
suggesting involvement of the sympathetic autonomic component as
well.
Another interesting observation in the present study is that two
types of physical training, aerobic and resistance ones, have promoted
reductions in the basal values of HR and IHR in both sham-operated
and ovariectomized rats. In sham-operated rats, however, aerobic
physical training promoted greater reductions in basal HR values
compared to resistance training, whereas no difference was found in
ovariectomized rats. The cause for such a finding is uncertain and
deserves further investigation.
Indeed, the mechanisms accounting for the basal HR reduction
after physical training has not yet been fully elucidated, but some
hypotheses have been raised though. Among the most accepted
hypotheses, one can cite the increase in the cardiac vagal tonic
influence (Smith et al., 1989; Hassan, 1991; Souza et al., 2007), as well
as automaticity adaptations and conduction in sinus nodes impulse,
thus resulting in decreased IHR (Negrão et al., 1992; Stein et al., 2002;
Danson and Paterson, 2003; Tezini et al., 2009). In our study, we have
observed that although ovariectomized rats presented no change in
their cardiac autonomic tonic balance (Fig. 1C), they had reductions in
basal HR values similar to those of sham-operated rats (Fig. 1B). This
finding strongly suggests the importance of IHR in reducing the basal
HR.
By comparing the effects of different types of physical exercises on
the autonomic control of sham-operated rats, we have observed that
aerobic training did not interfere with baroreflex sensibility but had
an influence on the cardiac autonomic tonic balance, thus establishing
an increase in the predominance of vagal autonomic component.
Adaptations in the modulation of HRV were characterized by
decreased LF oscillations. The results observed in autonomic tonus
and HRV modulation suggest a reduction in the sympathetic influence
and increase in vagal influence regarding the HR control, a finding
already reported elsewhere (Tezini et al., 2009; Souza et al., 2009). On
the other hand, resistance physical training did not promote the same
effects of aerobic training. The rats undergoing this type of training
showed reduction in HF oscillations and increase in LF oscillations. In
fact, these results show that resistance training impairs the cardiac
autonomic control by affecting mainly the parasympathetic autonomic component, thus reducing the cardiac autonomic modulation.
With regard to autonomic tonus, the results observed in shamoperated rats submitted to resistance training even indicated an
increase in the predominance of vagal autonomic component in the
determination of HR, in percentage values. However, we observed a
small increase in absolute values of HR following administration of
methylatropine in relation to sedentary group, a finding possibly
indicating an imbalance in either heart itself or cardiac autonomic
control. The causes for such adverse results between aerobic and
resistance exercises are unknown, but it is possible that the workload
imposed on the latter is a determining factor. In our study, the
workload was continuously incremented and had as reference the
animal's maximum movement capacity, which ensured that the
exercise being performed was characterized as a high-intensity
resistance training (Hornberger and Farrar, 2004). Therefore, this
study provides results that can contribute to other investigations
using protocols with milder workloads in order to assess at which
point the workload being imposed on the resistance training can be
harmful to the cardiovascular autonomic control.
The effects of aerobic physical training on the cardiac autonomic
control in ovariectomized rats were different from those observed in
sham-operated rats. In this case, changes occurred only in HRV, which
were characterized by an increase in HF oscillations. However,
resistance training did no promote any adaptation in ovariectomized
rats, including the HRV. These results point to the importance of
estrogen in the autonomic adaptations induced by physical exercises.
In fact, the role played by estrogen in the autonomic control is not
fully understood. However, several studies have demonstrated that
40
L.C.R. Silveira et al. / Autonomic Neuroscience: Basic and Clinical 162 (2011) 35–41
menopause is frequently associated with impairment in the cardiac
autonomic control under various aspects, including the modulation of
HRV (Virtanen et al., 2000; Zhang et al., 2000; Neves et al., 2007). The
causes of such impairment are still unknown, but it seems to involve
adaptations at central sites in the cardiovascular control resulting from
estrogen deficiency (Zhang and Kosaka, 2002; Rahimian et al., 2004). This
effect is supported by identifying estrogen receptors within the nucleus of
central nervous system (CNS) involved in the cardiac autonomic control
(Pelletier et al., 1988; Simonian and Herbison, 1997). However, either
blockade or activation of such receptors at specific sites seems to produce
different responses in the cardiovascular autonomic control (Saleh and
Connel, 2003; Saleh et al., 2005), which has impeded more specific
studies until now. Therefore, further studies are needed not only to
investigate the influence of estrogen on the cardiac autonomic control,
but also to identify its role as a possible coadjuvant in physical traininginduced adaptations in female rats.
With regard to SAP variability, ovariectomy and physical training
promoted alteration in neither total variance nor LF and HF
oscillations. In fact, these results were corroborated by a recent
study in which no differences in SAP variability were also found in
ovariectomized Wistar–Kyoto female rats (Dias-Silva et al., 2009),
thus suggesting that estrogen seems not to influence autonomic
modulation of arterial pressure. However, the relationship between
the role played by estrogenic receptors (estrogen receptor-α and
estrogen receptor-β) present at vascular endothelium (Kim-Schulze
et al., 1996; Grohé et al., 1997) and autonomic modulation of arterial
pressure needs further investigation.
In conclusion, the aerobic physical training in sham-operated
female rats promotes benefic adaptation in their cardiac autonomic
control, mainly regarding the cardiac autonomic modulation. On the
other hand, resistance trained rats exhibited preoccupying cardiac
autonomic alterations, with some cases showing even opposite results
compared to those from aerobic training. Additionally, ovariectomy
seems to interfere with the effects of physical training, thus
suggesting that estrogen plays a key role in the autonomic adaptations
resulting from physical training, although the mechanisms involved
are not fully understood and thereby need to be investigated.
References
Bonaiuti, D., Shea, B., Iovine, R., Negrini, S., Robinson, V., Kemper, H.C., Wells, G.,
Tugwell, P., Cranney, A., 2002. Exercise for preventing and treating osteoporosis in
postmenopausal women. Cochrane Database Syst. Rev. 3, CD000333.
Carter, J.B., Banister, E.W., Blaber, A.P., 2003. Effect of endurance exercise on autonomic
control of heart rate. Sports Med. 33 (1), 33–46.
Chappell, M.C., Gallagher, P.E., Averill, D.B., Ferrario, C.M., Brosnihan, K.B., 2003.
Estrogen or the AT1 antagonist olmesartan reverses the development of profound
hypertension in the congenic mRen2.Lewis rat. Hypertension 42, 781–786.
Collier, S.R., Kanaley, J.A., Carhart Jr., R., Frechette, V., Tobin, M.M., Bennet, N.,
Luckenbaugh, A.N., Fernhall, B., 2009. Cardiac autonomic function and baroreflex
changes following 4 weeks of resistance versus aerobic training in individuals with
pre-hypertension. Acta Physiol. 195, 339–348.
Danson, E.J., Paterson, D.J., 2003. Enhanced neuronal nitric oxide synthase expression is
central to cardiac vagal phenotype in exercise-trained mice. J. Physiol. 546, 225–232.
Dantas, A.P., Scivoletto, R., Fortes, Z.B., Nigro, D., Carvalho, M.H., 1999. Influence of female
sex hormones on endothelium-derived vasoconstrictor prostanoid generation in
microvessels of spontaneously hypertensive rats. Hypertension 34, 914–919.
De Angelis, K., Wichi, R.B., Jesus, W.R., Moreira, E.D., Morris, M., Krieger, E.M., Irigoyen,
M.C., 2004. Exercise training changes autonomic cardiovascular balance in mice.
J. Appl. Physiol. 96 (6), 2174–2178.
Dias-Silva, V.J., Miranda, R., Oliveira, L., Rodrigues Alves, C.H., Van Gils, G.H., Porta, A.,
Montano, N., 2009. Heart rate and arterial pressure variability and baroreflex sensitivity
in ovariectomized spontaneously hypertensive rats. Life Sci. 22 (84), 719–724.
Fenning, A., Harrison, G., Dwyer, D., Rose'Meyer, R., Brown, L., 2003. Cardiac adaptation
to endurance exercise in rats. Mol. Cell. Biochem. 251 (1–2), 51–59.
Flues, K., Paulini, J., Brito, S., Sanches, I.C., Consolim-Colombo, F., Irigoyen, M.C., De Angelis,
K., 2010. Exercise training associated with estrogen therapy induced cardiovascular
benefits after ovarian hormones deprivation. Maturitas 65, 267–271.
Garciarena, C.D., Pinilla, O.A., Nolly, M.B., Laguens, R.P., Escudero, E.M., Cingolani, H.E.,
Ennis, I.L., 2009. Endurance training in the spontaneously hypertensive rat: conversion
of pathological into physiological cardiac hypertrophy. Hypertension 53 (4), 708–714.
Grohé, C., Kahlert, S., Lobbert, K., et al., 1997. Cardiac myocytes and fibroblasts contain
functional estrogen receptors. FEBS Lett. 416, 107–112.
Gutkowska, J., Paquette, A., Wang, D., Lavoie, J.M., Jankowski, M., 2007. Effect of exercise
training on cardiac oxytocin and natriuretic peptide systems in ovariectomized
rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R267–R275.
Hassan, M.O., 1991. The role of the autonomic nervous system in exercise bradycardia
in rats. East Afr. Med. J. 68 (2), 130–133.
Hernández, I., Delgado, J.L., Díaz, J., Quesada, T., Teruel, M.J., Llanos, M.C., Carbonell, L.F.,
2000. 17β-Estradiol prevents oxidative stress and decreases blood pressure in
ovariectomized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R1599–R1605.
Hornberger Jr., T.A., Farrar, R.P., 2004. Physiological hypertrophy of the FHL muscle
following 8 weeks of progressive resistance exercise in the rat. Can. J. Appl. Physiol.
29 (1), 16–31.
Hu, M., Finni, T., Zou, L., Perhonen, M., Sedliak, M., Alen, M., Cheng, S., 2009. Effects of
strength training on work capacity and parasympathetic heart rate modulation
during exercise in physically inactive men. Int. J. Sports Med. 30 (10), 719–724.
Ibañez, J., Izquierdo, M., Argüelles, I., Forga, L., Larrión, J.L., García-Unciti, M., Idoate, F.,
Gorostiaga, E.M., 2005. Twice-weekly progressive resistance training decreases
abdominal fat and improves insulin sensitivity in older men with type 2 diabetes.
Diab. Care 28, 662–667.
Irigoyen, M.C., Paulini, J., Flores, L.J.F., Flues, K., Bertagnolli, M., Moreira, E.D., ConsolimColombo, F., Belló-Klein, A., De Angelis, K., 2005. Exercise training improves
baroreflex sensitivity associated with oxidative stress reduction in ovariectomized
rats. Hypertension 46, 998–1003.
Kim-Schulze, S., Mcgowan, K.A., Hubchak, S.C., et al., 1996. Expression of an estrogen
receptor by human coronary artery and umbilical vein endothelial cells. Circulation
94, 1402–1407.
Liang, H., Ma, Y., Pun, S., Stimpel, M., Jee, W.S., 1997. Aging- and ovariectomy-related
skeletal changes in spontaneously hypertensive rats. Anat. Rec. 249, 173–180.
Malliani, A., Pagani, M., Lombardi, F., Cerutti, S., 1991. Cardiovascular neural regulation
explored in the frequency domain. Circulation 84, 482–492.
Negrão, C.E., Moreira, E.D., Santos, M.C., Farah, V.M., Krieger, E.M., 1992. Vagal function
impairment after exercise training. J. Appl. Physiol. 72 (5), 1749–1753.
Neves, V.F., Silva de Sá, M.F., Gallo Jr., L., Catai, A.M., Martins, L.E., Crescêncio, J.C., Perpétuo,
N.M., Silva, E., 2007. Autonomic modulation of heart rate of young and postmenopausal women undergoing estrogen therapy. Braz. J. Med. Biol. Res. 40 (4), 491–499.
Nickenig, G., Bäumer, A.T., Grohè, C., Kahlert, S., Strehlow, K., Rosenkranz, S., Stäblein, A.,
Beckers, F., Smits, J.F., Daemen, M.J., Vetter, H., Böhm, M., 1998. Estrogen modulates
AT1 receptor gene expression in vitro and in vivo. Circulation 97 (22), 2197–2201.
Pelletier, G., Liao, N., Follea, N., Govindan, M.V., 1988. Mapping of estrogen receptorproducing cells in the rat brain by in situ hybridization. Neurosci. Lett. 94, 23–28.
Rahimian, R., Chan, L., Goel, A., Poburko, D., Van Breemen, C., 2004. Estrogen modulation
of endothelium-derived relaxing factors by human endothelial cells. Biochem.
Biophys. Res. Commun. 322, 373–379.
Reckelhoff, J.F., Zhang, H., Srivastava, K., 2000. Gender differences in development of
hypertension in spontaneously hypertensive rats: role of the renin–angiotensin
system. Hypertension 35, 480–483.
Rubini, R., Porta, A., Baselli, G., Cerutti, S., Paro, M., 1993. Power spectrum analysis of
cardiovascular variability monitored by telemetry in conscious unrestrained rats.
J. Auton. Nerv. Syst. 45, 181–190.
Sáinz, J., Osuna, A., Wangensteen, R., de Dios Luna, J., Rodríguez-Gómez, I., Duarte, J., Moreno,
J.M., Vargas, F., 2004. Role of sex, gonadectomy and sex hormones in the development of
nitric oxide inhibition-induced hypertension. Exp. Physiol. 89, 155–162.
Saleh, T.M., Connel, B.J., 2003. Estrogen-induced autonomic effects are mediated by
NMDA and GABAA receptors in the parabrachial nucleus. Brain Res. 973, 161–170.
Saleh, T.M., Connel, B.J., Cribb, A.E., 2005. Symphatoexcitatory effects of estrogen in the
insular cortex are mediated by GABA. Brain Res. 1037, 114–122.
Sanches, I.C., Sartori, M., Jorge, L., Irigoyen, M.C., De Angelis, K., 2009. Tonic and reflex
cardiovascular autonomic control in trained-female rats. Braz. J. Med. Biol. Res. 42 (10),
942–948.
Selig, S.E., Carey, M.F., Menzies, D.G., Patterson, J., Geerling, R.H., Williams, A.D.,
Bamroongsuk, V., Toia, D., Krum, H., Hare, D.L., 2004. Moderate-intensity resistance
exercise training in patients with chronic heart failure improves strength,
endurance, heart rate variability, and forearm blood flow. J. Card. Fail. 10, 21–30.
Simonian, S.X., Herbison, A.E., 1997. Differential expression of estrogen receptor and
neuropeptide Y by brainstem A1 and A2 noradrenaline neurons. Neuroscience 76,
517–529.
Smith, M.L., Hudson, D.L., Graitzer, H.M., Raven, P.B., 1989. Exercise training
bradycardia: the role of autonomic balance. Med. Sci. Sports Exerc. 21 (1), 40–44.
Souza, S.B., Flues, K., Paulini, J., Mostarda, C., Rodrigues, B., Souza, L.E., Irigoyen, M.C., De
Angelis, K., 2007. Role of exercise training in cardiovascular autonomic dysfunction
and mortality in diabetic ovariectomized rats. Hypertension 50 (4), 786–791.
Souza, H.C., De Araújo, J.E., Martins-Pinge, M.C., Cozza, I.C., Martins-Dias, D.P., 2009.
Nitric oxide synthesis blockade reduced the baroreflex sensitivity in trained rats.
Auton. Neurosci. 150 (1–2), 38–44.
Stein, R., Medeiros, C.M., Rosito, G.A., Zimenman, L.I., Ribeiro, J.P., 2002. Intrinsic sinus
and atrioventricular node electrophysiologic adaptations in endurance athletes.
J. Am. Coll. Cardiol. 39 (6), 1033–1038.
Svacinová, H., Nováková, M., Placheta, Z., Kohzuki, M., Nagasaka, M., Minami, N.,
Dobsák, P., Siegelová, J., 2008. Benefit of combined cardiac rehabilitation on
exercise capacity and cardiovascular parameters in patients with type 2 diabetes.
Tohoku J. Exp. Med. 215 (1), 103–111.
Task Force of the European Society of Cardiology and the North American Society of
Pacing and Electrophysiology., 1996. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93, 1043–1065.
Tezini, G.C.S.V., Silveira, L.C.R., Villa-Clé, P.G., Jacinto, C.P., Di Sacco, T.H.R., Souza, H.C.D.,
2009. The effect of aerobic physical training on cardiac autonomic control of rats
submitted to ovariectomy. Menopause 16 (1), 110–116.
L.C.R. Silveira et al. / Autonomic Neuroscience: Basic and Clinical 162 (2011) 35–41
Tsatsoulis, A., Fountoulakis, S., 2006. The protective role of exercise on stress system
dysregulation and comorbidities. Ann. NY Acad. Sci. 1083, 196–213.
Virtanen, I., Polo, O., Polo-Kantola, P., Kuusela, T., Ekholm, E., 2000. The effect of estrogen
replacement therapy on cardiac autonomic regulation. Maturitas 37 (1), 45–51.
Warburton, D.E., Nicol, C.W., Bredin, S.S., 2006. Health benefits of physical activity: the
evidence. CMAJ 174 (6), 801–809.
Warner, S.O., Linden, M.A., Liu, Y., Harvey, B.R., Thyfault, J.P., Whaley-Connell, A.T.,
Chockalingam, A., Hinton, P.S., Dellsperger, K.C., Thomas, T.R., 2010. The effects of
41
resistance training on metabolic health with weight regain. J. Clin. Hypertens.
(Greenwich) 12 (1), 64–72.
Zhang, L., Kosaka, H., 2002. Sex-specific acute effect of estrogen on endothelium-derived
contracting factor in the renal artery of hypertensive Dahl rats. J. Hypertens. 20,
237–246.
Zhang, H., Bai, W., Guo, J., Zheng, S., Zhao, J., 2000. Effect of hormone replacement
therapy on heart rate variability in postmenopausal women. Chin. Med. J. (Engl)
113 (7), 592–594.