(Circulation. 1999;100:27-32.)
© 1999 American Heart Association, Inc.
Clinical Investigation and Reports |
Muscle Metaboreflex Contribution to Sinus Node Regulation During Static Exercise
Insights From Spectral Analysis of Heart Rate Variability
From the Dipartimento di Medicina Interna (F.I., M.M., G.R., G.P., J.M.L.), Università di Roma "Tor Vergata," Rome, Italy, and Ospedale S. Gerardo (P.P.), Monza, Italy.
Correspondence to Dr Ferdinando Iellamo, Dipartimento Medicina Interna, Università di Roma "Tor Vergata," Via O. Raimondo, 8, 00173 Roma, Italy. E-mail iellamo{at}med.uniroma2.it
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Background—It is currently assumed that during static exercise, central command increases heart rate (HR) through a decrease in parasympathetic activity, whereas the muscle metaboreflex raises blood pressure (BP) only through an increase in sympathetic outflow to blood vessels, because when the metaboreflex activation is maintained during postexercise muscle ischemia, BP remains elevated while HR recovers. We tested the hypotheses that the muscle metaboreflex contributes to HR regulation during static exercise via sympathetic activation and that the arterial baroreflex is involved in the HR recovery of postexercise muscle ischemia.
Methods and Results—Eleven healthy male volunteers performed 4-minute static leg extension (SLE) at 30% of maximal voluntary contraction, followed by 4-minute arrested leg circulation (ALC). Autonomic regulation of HR was investigated by spectral analysis of HR variability (HRV), and baroreflex control of heart period was assessed by the spontaneous baroreflex method. SLE resulted in a significant increase in the low-frequency component of HRV that remained elevated during ALC. The normalized high-frequency component of HRV was reduced during SLE and returned to control levels during ALC. Baroreflex sensitivity was significantly reduced during SLE and returned to control levels during ALC when BP was kept elevated above the resting level while HR recovered.
Conclusions—The muscle metaboreflex contributes to HR regulation during static exercise via a sympathetic activation. The bradycardia that occurs during postexercise muscle ischemia despite the maintained sympathetic stimulus may be explained by a baroreflex-mediated increase in parasympathetic outflow to the sinoatrial node that overpowers the metaboreflex-induced cardiac sympathetic activation.
Key Words: exercise • muscles • heart rate • nervous system, autonomic • baroreceptors
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Static exercise is characterized by increases in arterial pressure (AP) and heart rate (HR). Two neural mechanisms have been implicated in these responses.1 One mechanism activates central neuronal circuits that control somatomotor and cardiovascular systems, establishing changes in parasympathetic and sympathetic efferent activity that determine the cardiovascular responses ("central command"). In the other mechanism, the changes in autonomic efferent activity are caused reflexly by stimulation of somatic afferents sensitive to metabolites produced within the contracting muscles ("exercise pressor reflex" or "muscle metaboreflex").
The current thinking is that during static exercise, the rise in AP occurs mainly via an increase in sympathetic activity to blood vessels due to muscle metaboreflex activation, whereas the increase in HR occurs mainly through a decrease in parasympathetic activity to the sinus node due to central command.2 This general view came from the observation that during postexercise circulatory occlusion, a maneuver that maintains muscle metaboreflex activation while removing the central command, the increases in AP, vascular resistance, and sympathetic nerve activity to resting muscles are kept elevated above resting levels, whereas HR fully recovers.3 4 5
However, Maciel et al6 and Martin et al7 reported a reduced HR response to static exercise after administration of ß-adrenergic blocking drugs, suggesting an involvement of the sympathetic nervous system in HR regulation, although the mechanism underlying the sympathetic contribution (ie, central versus reflex) has not been determined. More recently, O'Leary8 provided evidence that sympathetic activation originating from the muscle metaboreflex contributes substantially to the HR increase during exercise in the conscious dog, inasmuch as parasympathetic blockade with atropine did not affect the increase in AP and HR that occurred during exercise but did prevent the fall in HR during postexercise circulatory occlusion. The hypothesis advanced8 was that the fall in HR during postexercise muscle ischemia despite a maintained increase in sympathetic outflow was caused by a sudden rise of parasympathetic activity at the cessation of exercise, due to the loss of central command or to arterial baroreflex mechanisms, which overpowered the sympathetic activation. Whether these data can be extrapolated to humans is unknown, because neural control of circulation at rest and during exercise may differ between dogs and humans owing to differences in baseline autonomic tone, pumping capacity, and oxidative capacity of muscles.2
The present study was undertaken to test the hypotheses that in humans, the muscle metaboreflex contributes to HR regulation during static exercise via sympathetic activation and that the arterial baroreflex could be involved in HR recovery during postexercise circulatory occlusion. Autonomic regulation of HR has been investigated by means of power spectral analysis of HR variability, a technique currently used to derive noninvasive indexes of the different neural components regulating the sinoatrial node.9 Arterial baroreflex control of HR has been assessed by analysis of the relationship between beat-by-beat spontaneous fluctuations in arterial blood pressure and RR interval.10
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Subjects
Eleven healthy male volunteers, aged 26.0±2.4 years, participated in this study. All participants gave written informed consent. None were taking medications, and all were nonsmokers and not involved in regular physical activity. The protocol was approved by the Ethics Committee of the Department of Internal Medicine of our university.
General Procedure
Static exercise consisted of 1 leg-knee extension (SLE)
performed in the seated position with the trunk supported by the chair
back of a computer-based dynamometer apparatus (REV 9000,
Technogym). The inferior third of the leg was attached to
the distal end of the moveable lever arm of the dynamometer. A
pneumatic cuff was placed as high as possible on the thigh to allow
experiments with arrested circulation to the leg.
SLE was performed at 30% of maximal voluntary contraction, previously determined as the highest force developed by the subjects in 3 trials. A visual feedback5 allowed subjects to hold constant the muscle tension during static contractions. Subjects were instructed to avoid Valsalva maneuver and to relax all of the muscle not involved in contraction.
Experimental Protocol
The experiments were performed in the morning in a laboratory at
ambient temperature (22°C to 24°C). Subjects were required not to
eat or to drink coffee for 
2 hours. Each subject performed in random
order the exercise or no-exercise protocol. The exercise protocol
consisted of 5 minutes' rest followed by 4 minutes of SLE. Eight
seconds before cessation of SLE, the pneumatic cuff on the exercising
leg was rapidly inflated to suprasystolic levels (250
mm Hg), and arrested leg circulation (ALC) was maintained for 4
minutes in the postexercise period. The no-exercise protocol consisted
of 5 minutes' rest followed by 4 minutes of thigh circulatory
occlusion. A 20- to 30-minute rest period separated the exercise and
no-exercise protocols.
Recorded Variables
Subjects were connected to a defibrillator supplied with an
oscillographic screen (Hewlett-Packard [HP] 43120A); a chest
lead provided the ECG signal. Arterial pressure was
continuously and noninvasively measured from the third finger of the
nondominant hand by Finapres (Ohmeda, model 2300). This device provided
accurate estimates of changes of intra-arterial pressure
during laboratory tests, including exercise tests.11 The
arm with the instrumented finger was held extended at the heart level
by means of a pulley arrangement.5 12 Respiration was
assessed by a pneumotachograph-(Fleisch No. 3) pressure transducer set
(HP 47304A) connected to a face mask worn by the subjects. The 3 analog
signals were sampled at 300 Hz per channel by an analog/digital board
(Data Translation 2831) inserted into a personal computer and stored
for subsequent analyses.
Power Spectral Analysis
A derivative-threshold algorithm provided continuous series of
RR interval (tachogram) from the ECG signal. Stationary sections of
tachograms of appropriate length were selected according to guidelines
on standards of measurements for HR variability.9 The
variance of RR interval was evaluated. The harmonic components of
RR-interval variability were evaluated by the autoregressive method, in
which the autoregressive coefficients are estimated by the Yule-Walker
method.13 We checked the validity of the model by testing
the whiteness of the prediction error, and we chose the optimal model
order by applying the Akaike information criterion.14 The
center frequency and associated power of each relevant oscillatory
component were automatically calculated by the residue method. Two main
components were considered: that in the frequency band from 0.04 to
0.15 Hz (low frequency; LF) and that in the range 0.15 to 0.4 Hz (high
frequency; HF), which is synchronous with respiration. The
very-low-frequency component (<0.03 Hz) was not addressed and was
considered as a DC component.9 We calculated the power
density of each spectral component in absolute values
(ms2) and normalized units, which we obtained by
dividing the absolute power of each spectral component by total power
after having subtracted from it the power of the DC component, if
present, and multiplying this value by 100. The normalization
procedure is particularly helpful in allowing comparisons between
subjects or experimental conditions characterized by large differences
in total power or DC noise.9 15 Spectral analysis
of the respiratory signal was performed on the signal sampled once for
every cardiac cycle by a procedure similar to that described for RR
interval. These spectra were used to assess the main respiratory
frequency and to locate the respiratory component of the power spectral
analysis of RR-interval variability.
Spontaneous Baroreflex Analysis
Details of this analysis have been described
previously.5 12 Briefly, the beat-by-beat time series of
systolic AP (SAP) and RR interval are scanned by a computer to
identify sequences of 3 consecutive beats in which SAP and RR
interval of the following beat change in the same direction (either
increasing or decreasing). A linear regression is applied to each
individual sequence, and the mean slope of the SAP/RR interval
relationship, obtained by averaging all slopes computed within a given
test period, is calculated and taken as a measure of the spontaneous
baroreflex sensitivity (BRS) for that period. This technique provided
reproducible results during many laboratory tests, including static
exercise.16
Statistical Analysis
The significance of differences in the reported variables
among the different experimental periods was evaluated by ANOVA for
repeated measures with Bonferroni adjustment for multiple comparisons.
Values are presented as mean±SE. Differences were considered
statistically significant when P was <0.05.
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
SLE produced a significant increase in AP and a significant decrease in RR interval. During ALC, AP remained significantly increased above resting levels, whereas RR interval returned to control. On release of occlusion, AP also returned to control (Table 1
and Figure 1).
|
|
The RR-interval variance was not significantly different from that at
seated rest during both SLE and ALC. Spectral analysis of
RR-interval variability demonstrated the presence of 2 clearly
separated major oscillatory components in an LF and HF band in all
experimental periods (Figure 2).
|
The LF component significantly increased above rest during SLE and
remained elevated during ALC, both in absolute values and normalized
units. It returned to baseline during recovery (Table 1
). The
power of the HF component was markedly decreased during SLE compared
with rest, although the decrease did not reach statistical
significance. However, after the normalization procedure, the decrease
in the HF component was significant (Table 1). During ALC and
recovery, the HF component did not significantly differ from rest.
The center frequency of both the LF and HF components did not change
significantly during either SLE or ALC. The HF center frequency in the
RR-interval variability spectrum was close to that in the respiratory
variability signal (Table 1). During exercise, respiratory rate
did not change significantly from the resting value of 0.28±0.02
Hz.
BRS was significantly decreased from rest during exercise and returned
to control values during ALC (14.8±3.1, 9.1±1.9, and 13.4±3.1
ms/mm Hg during rest, SLE, and ALC, respectively; F=10.43;
P<0.001). Relating SAP to HR instead of RR interval did not
substantially modify the above results (-1.30±0.21, -1.10±0.18, and
-1.24±0.20 beats · min-1 ·
mm Hg-1 during rest, SLE, and ALC,
respectively; F=3.84; P<0.05). An example of spontaneous
baroreflex from 1 subject during rest, SLE, and ALC is shown in
Figure 3. No significant differences were
found between +RR/+SAPand -RR/-SAP sequences either at rest
(14.9±2.7 versus 13.8±3.2 ms/mm Hg) or during SLE (9.0±2.1 versus
8.8±1.7 ms/mm Hg). None of the considered variables were
significantly affected by circulatory occlusion of the thigh without
exercise (Table 2).
|
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The main findings of this study are 2-fold. The first is that in humans, the muscle metaboreflex contributes to HR regulation during static exercise through a sympathetic stimulation. The second new finding is that the arterial baroreflex may be involved in the recovery of HR during postexercise muscle ischemia despite the maintenance of sympathetic activation.
Muscle Metaboreflex Regulation of HR
In the present investigation, the contribution of the muscle
metaboreflex to HR regulation was assessed by power spectrum
analysis of RR-interval variability. In the power
spectrum analysis of short-term fluctuations of RR
interval, 2 main components can be identified, in LF and HF bands,
which are predominantly linked to a relative increase in sympathetic
and parasympathetic activity, respectively.9 15 17 18 19 20 21
By applying this methodology, we observed a decrease in the HF component of the RR-interval spectra during SLE, in agreement with the results of Taylor et al22 during static handgrip. This would reflect the well-known decrease in parasympathetic outflow to sinus node occurring during exercise. Concomitantly with the decrease in HF oscillations, there was an increase in the lower-frequency oscillations of HR that, by reflecting an increased sympathetic modulation to the sinoatrial node, would indicate a significant contribution of this autonomic division to HR regulation during static exercise. The relevance of the sympathetic nervous system in regulating HR is further stressed by the fact that the increase in the LF component did occur despite the HF component that was present in sympathetic discharge variability,23 which could have restrained LF enhancement, because vagal outflow decreases during exercise. Interestingly, the increase in the LF component was significant both in absolute values and normalized units. In this context, it is of note that total RR-interval variance was not significantly changed from rest during exercise, probably because HR values attained during SLE were not so dramatic. Thus, in our study, extremes of stimulation of the sinus node did not occur, allowing us to emphasize the strengths of the spectral analysis technique24 rather than their limitations, at variance with other studies25 26 that used various protocols of dynamic exercise that drastically reduced HR variability. Obviously, large interindividual differences in total power or in DC noise present at rest may persist during exercise, making it necessary to use normalized units to better assess the distribution of power in defined spectral components.15 19 20 This aspect is exemplified by our results with the HF component. During postexercise circulatory occlusion, the RR interval returned to control, whereas AP remained significantly elevated above rest, indicating a maintained activation of the muscle metaboreflex. During ALC, the HF component returned to rest, whereas the LF component remained significantly elevated. After release of circulatory occlusion, the HF component did not feature significant changes from rest and ALC, whereas the LF component returned to control, indicating the muscle metaboreflex as the effective stimulus in maintaining elevation of the LF component during postexercise muscle ischemia. Overall, these results strongly suggest that the muscle metaboreflex contributes to HR regulation during static exercise via a sympathetic excitation, this latter being maintained during postexercise ischemia, similar to what occurs for the vasculature3 5 despite the return of HR to control levels.
The present study is the first to provide experimental indication that the muscle metaboreflex contributes to HR regulation during static exercise in humans and might contribute to the theory that muscle metaboreflex may even be able to increase muscle blood flow by increasing cardiac output in addition to increasing blood pressure by vasoconstriction.
Baroreflex Control of HR
We found that during exercise, BRS was significantly reduced, but
it was restored during ALC. The restoration of BRS to the resting level
during postexercise ischemia, at the same time as AP was kept
elevated and close to the exercise level by the muscle metaboreflex,
could indicate that a vagally mediated baroreflex mechanism was
responsible for the return of HR toward resting levels despite the
maintained sympathetic activation. In this setting, the increased
parasympathetic outflow induced by the arterial baroreflex
would overpower the metaboreflex-induced cardiac sympathetic
excitation, because muscle metaboreflex exerts few direct influences on
parasympathetic outflow.2
The possibility that the loss of central command at the cessation of exercise could contribute to HR recovery cannot be excluded. However, the results of Bull et al27 concerning HR recovery, with a maintained pressor response, during muscle ischemia after electrically induced static contractions support the concept in the present study that removal of central command is not invariably the cause of HR recovery during postexercise circulatory occlusion.
During exercise, the decrease in arterial baroreflex gain was associated with an increase in the LF component of the RR-interval spectra. This observation is in line with a recent study by Cooley et al,21 which showed that LF oscillations in RR interval can be generated in the absence of vagally mediated baroreflex input. These findings support the concept of a central origin of the LF component in RR-interval variability and favor the notion that the LF component is mainly linked to sympathetic activity.18 19 20 21
Our findings confirm and extend those obtained by O'Leary8 in dogs under the influence of autonomic blocking drugs during exercise. We did not use pharmacological manipulations of the autonomic nervous system for several reasons. For example, atropine would alter both baseline vagal tone28 and HR response to static exercise.29 Furthermore, atropine virtually eliminates spontaneous baroreflex slopes,30 whereas ß-blockade enhances baroreflex sensitivity.31 32 Finally, results obtained after selective autonomic blockade must be viewed with caution, because interference with the activity of one division of the autonomic nervous system might lead to compensatory changes in the other that could obscure the relative contribution of each of the 2 components. This could lead to ambiguous results, particularly when multiple (redundant) control mechanisms are integrated in producing the net responses, as during exercise.1 Therefore, our experimental approach allowed a distinctive insight into the autonomic regulation of HR during static exercise by having used nonperturbational techniques, without artificially isolating the influence of the different neural pathways.
Study Limitations
We considered the possibility that our results could have been
influenced by respiratory adjustments to exercise, because the HF
RR-interval spectral power declines as breathing frequency
increases.33 However, in the present study, the
increase in respiratory rate was very small, amounting to 
2
breaths/min. This small change in breathing frequency should have
minimally affected the decrease in the HF component observed during
exercise.33 Moreover, the possibility that changes in
parasympathetic activity at the cessation of exercise could have
contributed to some extent to the maintained increase in the LF
component during ALC cannot be absolutely excluded.18 23
However, the finding of no significant differences in HF spectral power
(and in BRS as well) between ALC and recovery when, on the contrary, LF
returned to control would argue against a substantial contribution of
vagal mechanisms to LF spectra during ALC.
Finally, the spontaneous baroreflex method reflects responses to rapid, transient changes in AP that are vagally mediated, whereas it does not enable us to investigate the slower sympathetic component of the baroreflex. This could be important during exercise when, in contrast to during rest, a substantial baroreflex bradycardia has been reported to occur via sympathetic inhibition, whereas the remaining parasympathetic component in the baroreflex response appears to be reduced.34 However, this problem should have a greater effect on the baroreflex control of sinus node during exercise intensities greater than those used in the present investigation.34
In conclusion, the results of this study suggest that the muscle metaboreflex contributes to HR regulation during static exercise via a sympathetic activation that is maintained during postexercise muscle ischemia. The bradycardia that occurs during postexercise circulatory occlusion despite the maintained sympathetic stimulus may be explained by an arterial baroreflex-mediated increase in parasympathetic outflow to the sinus node that overpowers the metaboreflex-induced cardiac sympathetic activation.
Received November 18, 1998; revision received April 9, 1999; accepted April 15, 1999.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
1. Mitchell JH. Neural control of the circulation during exercise. Med Sci Sport Exerc. 1990;22:141–154.[Medline] [Order article via Infotrieve]
2.
Rowell LB, O'Leary DS. Reflex control of the
circulation during exercise: chemoreflexes and mechanoreflexes.
J Appl Physiol. 1990;69:407–418.
3.
Mark AL, Victor RG, Nerhed C, Wallin BG.
Microneurographic studies of the mechanisms of sympathetic nerve
responses to static exercise in humans. Circ Res. 1985;57:461–469.
4.
Mitchell JH, Reeves DR, Rogers HB, Secher NH, Victor
RG. Autonomic blockade and cardiovascular responses to
static exercise in partially curarized man. J Physiol
(Lond). 1989;413:433–445.
5.
Iellamo F, Hughson RL, Castrucci F, Legramante JM,
Raimondi G, Peruzzi G, Tallarida G. Evaluation of spontaneous
baroreflex modulation of sinus node during isometric exercise in
healthy humans. Am J Physiol. 1994;267:H994–H1001.
6. Maciel BC, Gallo L Jr, Marin Neto JA, Martins LEB. Autonomic nervous control of the heart rate during isometric exercise in normal man. Pflugers Arch. 1987;408:173–177.[Medline] [Order article via Infotrieve]
7. Martin CE, Shaver JA, Leon DF, Thompson ME, Reddy PS, Leonard JJ. Autonomic mechanisms in hemodynamic responses to isometric exercise. J Clin Invest. 1974;54:104–115.
8.
O'Leary DS. Autonomic mechanisms of muscle
metaboreflex control of heart rate. J Appl Physiol. 1993;74:1748–1754.
9.
Task Force of the European Society of
Cardiology and the North American Society of Pacing and
Electrophysiology. Heart rate variability: standards and measurements,
physiological interpretation, and clinical use.
Circulation. 1996;93:1043–1065.
10.
Bertinieri G, Di Rienzo M, Cavallazzi A, Ferrari AV,
Pedotti A, Mancia G. Evaluation of baroreceptor reflex by blood
pressure monitoring in unanesthetized cats. Am J
Physiol. 1988;254:H377–H383.
11.
Parati G, Casadei R, Groppelli A, Di Rienzo M, Mancia
G. Comparisons of finger and intra-arterial blood pressure
monitoring at rest and during laboratory testing.
Hypertension. 1989;13:647–655.
12.
Iellamo F, Legramante JM, Raimondi G, Peruzzi G.
Baroreflex control of sinus node during dynamic exercise in humans:
effects of central command and muscle reflexes. Am J
Physiol. 1997;272:H1157–H1164.
13. Kay SM, Marple SL. Spectrum analysis: a modern perspective. Proc IEEE. 1981;69:1380–1419.
14. Akaike H. Statistical predictor identification. Ann Int Stat Math. 1970;22:203–217.
15.
Pagani M, Lombardi F, Guzzetti S, Rimoldi O, Furlan R,
Pizzinelli P, Sandrone G, Malfatto G, Dell'Orto S, Piccaluga E, Turiel
M, Baselli G, Cerutti S, Malliani A. Power spectral analysis of
heart rate and arterial pressure variabilities as a marker
of sympathovagal interaction in man and conscious dog. Circ
Res. 1986;59:178–193.
16. Iellamo F, Legramante JM, Raimondi G, Castrucci F, Massaro M, Peruzzi G. Evaluation of reproducibility of spontaneous baroreflex sensitivity at rest and during laboratory tests. J Hypertens. 1996;14:1099–1104.[Medline] [Order article via Infotrieve]
17.
Pomeranz M, Macaulay RJB, Caudill MA, Kutz I, Adam D,
Gordon D, Kilborn KM, Barger AC, Shannon DC, Cohen RJ, Benson M.
Assessment of autonomic function in humans by heart rate spectral
analysis. Am J Physiol. 1985;248:H151–H153.
18.
Malliani A, Pagani M, Lombardi F, Cerutti S.
Cardiovascular neural regulation explored in the
frequency domain. Circulation. 1991;84:482–492.
19.
Pagani M, Montano N, Porta A, Malliani A, Abboud FM,
Birkett C, Somers VK. Relationship between spectral components of
cardiovascular variabilities and direct measures of
muscle sympathetic nerve activity in humans. Circulation. 1997;95:1441–1448.
20.
Montano N, Cogliati C, Porta A, Pagani M, Malliani A,
Narkiewicz K, Abboud FM, Birkett C, Somers VK. Central vagotonic
effects of atropine modulate spectral oscillations of
sympathetic nerve activity. Circulation. 1998;98:1394–1399.
21.
Cooley RL, Montano N, Cogliati C, van de Borne P,
Richenbacher W, Oren R, Somers VK. Evidence for a central origin of the
low-frequency oscillation in RR-interval variability.
Circulation. 1998;98:556–561.
22.
Taylor JA, Hayano J, Seals DR. Lesser vagal withdrawal
during isometric exercise with age. J Appl Physiol. 1995;79:805–811.
23. Montano N, Lombardi F, Gnecchi-Ruscone T, Contini M, Finocchiaro ML, Baselli G, Porta A, Cerutti S, Malliani A. Spectral analysis of sympathetic discharge, R-R interval and systolic arterial pressure in decerebrate cats. J Auton Nerv Syst. 1992;40:21–31.[Medline] [Order article via Infotrieve]
24. Malik M, Camm AJ. Components of heart rate variability: what they really mean and what we really measure. Am J Cardiol. 1993;72:821–822.[Medline] [Order article via Infotrieve]
25. Perini R, Orizio C, Baselli G, Cerutti S, Veicstenas A. The influence of exercise intensity on the power spectrum of heart rate variability. Eur J Appl Physiol. 1990;61:143–148.
26. Casadei B, Cochrane S, Johnston J, Conway J, Sleight P. Pitfalls in the interpretation of spectral analysis of the heart rate variability during exercise in humans. Acta Physiol Scand. 1995;153:125–131.[Medline] [Order article via Infotrieve]
27.
Bull RK, Davies CTM, Lind AR, White MJ. The human
pressor response during and following voluntary and evoked isometric
contraction with occluded blood supply. J Physiol. 1989;411:63–70.
28. Dauchot P, Gravenstein JS. Effects of atropine on the electrocardiogram in different age groups. Clin Pharmacol Ther. 1970;12:274–280.
29.
Freyschuss U. Elicitation of heart rate and blood
pressure increase on muscle contraction. J Appl
Physiol. 1970;28:758–761.
30.
Parlow J, Viale JP, Annat A, Hughson RL, Quintin L.
Spontaneous cardiac baroreflex in humans: comparison with drug-induced
responses. Hypertension. 1995;25:1058–1068.
31. Lucini D, Pagani M, Mela GS, Malliani A. Sympathetic restraint of baroreflex control of heart period in normotensive and hypertensive subjects. Clin Sci. 1994;86:547–556.[Medline] [Order article via Infotrieve]
32.
Legramante JM, Raimondi G, Massaro M, Cassarino S,
Peruzzi G, Iellamo F. Investigating feed-forward neural regulation of
circulation from analysis of spontaneous arterial
pressure and heart rate fluctuations. Circulation. 1999;99:1760–1766.
33.
Brown TE, Beightol LA, Koh J, Eckberg DL. Important
influence of respiration on human R-R interval power spectra is largely
ignored. J Appl Physiol. 1993;75:2310–2317.
34.
O'Leary DS, Seamans DP. Effect of exercise on
autonomic mechanisms of baroreflex control of heart rate. J
Appl Physiol. 1993;75:2251–2257.
This article has been cited by other articles:
 |
|
 |
|
  J. Ng, S. Sundaram, A. H. Kadish, and J. J. Goldberger Autonomic effects on the spectral analysis of heart rate variability after exercise Am J Physiol Heart Circ Physiol, October 1, 2009; 297(4): H1421 - H1428. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Okada, Y.-i. Kamijo, K. Okazaki, S. Masuki, M. Goto, and H. Nose Pressor responses to isometric biting are evoked by somatosensory receptors in periodontal tissue in humans J Appl Physiol, August 1, 2009; 107(2): 531 - 539. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. C. Drew, D. B. McIntyre, C. Ring, and M. J. White Local metabolite accumulation augments passive muscle stretch-induced modulation of carotid-cardiac but not carotid-vasomotor baroreflex sensitivity in man Exp Physiol, September 1, 2008; 93(9): 1044 - 1057. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. P. Fisher, C. N. Young, and P. J. Fadel Effect of muscle metaboreflex activation on carotid-cardiac baroreflex function in humans Am J Physiol Heart Circ Physiol, May 1, 2008; 294(5): H2296 - H2304. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Crisafulli, R. Milia, A. Lobina, M. Caddeo, F. Tocco, A. Concu, and F. Melis Haemodynamic effect of metaboreflex activation in men after running above and below the velocity of the anaerobic threshold Exp Physiol, April 1, 2008; 93(4): 447 - 457. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Gujic, D. Laude, A. Houssiere, S. Beloka, J.-F. Argacha, D. Adamopoulos, O. Xhaet, J.-L. Elghozi, and P. van de Borne Differential effects of metaboreceptor and chemoreceptor activation on sympathetic and cardiac baroreflex control following exercise in hypoxia in human J. Physiol., November 15, 2007; 585(1): 165 - 174. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Stewart, I. Taneja, and M. S. Medow Reduced central blood volume and cardiac output and increased vascular resistance during static handgrip exercise in postural tachycardia syndrome Am J Physiol Heart Circ Physiol, September 1, 2007; 293(3): H1908 - H1917. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Ichinose, S. Koga, N. Fujii, N. Kondo, and T. Nishiyasu Modulation of the spontaneous beat-to-beat fluctuations in peripheral vascular resistance during activation of muscle metaboreflex Am J Physiol Heart Circ Physiol, July 1, 2007; 293(1): H416 - H424. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. Sala-Mercado, M. Ichinose, R. L. Hammond, T. Ichinose, M. Pallante, L. W. Stephenson, D. S. O'Leary, and F. Iellamo Muscle metaboreflex attenuates spontaneous heart rate baroreflex sensitivity during dynamic exercise Am J Physiol Heart Circ Physiol, June 1, 2007; 292(6): H2867 - H2873. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Crisafulli, E. Salis, F. Tocco, F. Melis, R. Milia, G. Pittau, M. A. Caria, R. Solinas, L. Meloni, P. Pagliaro, et al. Impaired central hemodynamic response and exaggerated vasoconstriction during muscle metaboreflex activation in heart failure patients Am J Physiol Heart Circ Physiol, June 1, 2007; 292(6): H2988 - H2996. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Crisafulli, E. Salis, G. Pittau, L. Lorrai, F. Tocco, F. Melis, P. Pagliaro, and A. Concu Modulation of cardiac contractility by muscle metaboreflex following efforts of different intensities in humans Am J Physiol Heart Circ Physiol, December 1, 2006; 291(6): H3035 - H3042. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Iellamo, M. Di Rienzo, D. Lucini, J. M. Legramante, P. Pizzinelli, P. Castiglioni, F. Pigozzi, M. Pagani, and G. Parati Muscle metaboreflex contribution to cardiovascular regulation during dynamic exercise in microgravity: insights from mission STS-107 of the space shuttle Columbia J. Physiol., May 1, 2006; 572(3): 829 - 838. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Iellamo, A. Galante, J. M. Legramante, M. E. Lippi, C. Condoluci, G. Albertini, and M. Volterrani Altered autonomic cardiac regulation in individuals with Down syndrome Am J Physiol Heart Circ Physiol, December 1, 2005; 289(6): H2387 - H2391. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Iellamo, F. Placidi, M. G. Marciani, A. Romigi, M. Tombini, S. Aquilani, M. Massaro, A. Galante, and J. M. Legramante Baroreflex Buffering of Sympathetic Activation During Sleep: Evidence From Autonomic Assessment of Sleep Macroarchitecture and Microarchitecture Hypertension, April 1, 2004; 43(4): 814 - 819. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Halamek, T. Kara, P. Jurak, M. Soucek, D. P. Francis, L. C. Davies, W. K. Shen, A. J.S. Coats, M. Novak, Z. Novakova, et al. Variability of Phase Shift Between Blood Pressure and Heart Rate Fluctuations: A Marker of Short-Term Circulation Control Circulation, July 22, 2003; 108(3): 292 - 297. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Komine, K. Matsukawa, H. Tsuchimochi, and J. Murata Central command blunts the baroreflex bradycardia to aortic nerve stimulation at the onset of voluntary static exercise in cats Am J Physiol Heart Circ Physiol, July 11, 2003; 285(2): H516 - H526. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Fernhall and M. Otterstetter Attenuated responses to sympathoexcitation in individuals with Down syndrome J Appl Physiol, June 1, 2003; 94(6): 2158 - 2165. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Masuki, M. Takeoka, S.'I. Taniguchi, and H. Nose Enhanced baroreflex sensitivity in free-moving calponin knockout mice Am J Physiol Heart Circ Physiol, March 1, 2003; 284(3): H939 - H946. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Iellamo, J. M. Legramante, F. Pigozzi, A. Spataro, G. Norbiato, D. Lucini, and M. Pagani Conversion From Vagal to Sympathetic Predominance With Strenuous Training in High-Performance World Class Athletes Circulation, June 11, 2002; 105(23): 2719 - 2724. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Cui, T. E. Wilson, M. Shibasaki, N. A. Hodges, and C. G. Crandall Baroreflex modulation of muscle sympathetic nerve activity during posthandgrip muscle ischemia in humans J Appl Physiol, October 1, 2001; 91(4): 1679 - 1686. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Iellamo and J. R. G. M. D. H. Groeller Baroreflex control of heart rate during exercise: a topic of perennial conflict J Appl Physiol, March 1, 2001; 90(3): 1184 - 1185. [Full Text] [PDF]
|
|
|
|
|
|
F. Iellamo, J. M. Legramante, M. Massaro, G. Raimondi, and A. Galante Effects of a Residential Exercise Training on Baroreflex Sensitivity and Heart Rate Variability in Patients With Coronary Artery Disease : A Randomized, Controlled Study Circulation, November 21, 2000; 102(21): 2588 - 2592. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. M. Legramante, A. Galante, M. Massaro, A. Attanasio, G. Raimondi, F. Pigozzi, and F. Iellamo Hemodynamic and autonomic correlates of postexercise hypotension in patients with mild hypertension Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2002; 282(4): R1037 - R1043. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||