J Appl Physiol
90: 1559–1564, 2001.
Inconsistent link between low-frequency oscillations:
R-R interval responses to augmented Mayer waves
J. W. HAMNER, RAYMOND J. MORIN, JAMES L. RUDOLPH, AND J. ANDREW TAYLOR
Laboratory for Cardiovascular Research, Research and Training Institute,
Hebrew Rehabilitation Center for Aged, Boston 02131; and Division on Aging,
Harvard Medical School, Boston, Massachusetts 02131
Received 18 July 2000; accepted in final form 20 October 2000
in arterial blood pressure
(Mayer waves) and heart period have long been researched, yet there is no universally accepted theory
regarding their source. Theories suggest that oscillations in blood pressure could originate from various
mechanisms, including endogenous central rhythms
(13, 17), negative-feedback system engagement (10,
19), or vascular autorhymicities (18). Cross-spectral
phase and gain relationships, as well as coherence,
have shown a relatively close link between low-frequency arterial pressure and heart period oscillations
(3). Consequently, arterial baroreflex engagement in
response to pressure oscillations is most commonly
cited as the cause for corresponding low-frequency oscillations in cardiac interval (2, 5, 20). However, the
variable nature of the waves themselves may indicate
a more complex relationship than can be easily explained by the baroreflex.
Unlike respiratory frequency oscillations, arterial
pressure Mayer waves spontaneously appear without
any seeming consistency. Power spectra of heart period
and blood pressure have shown that the frequency of
oscillation differs between and within subjects, with
oscillations occurring across a range of frequencies
from 0.07 to 0.15 Hz (although they are generally
centered at 0.1 Hz) (15). In addition, standard power
spectral indexes show a relatively high degree of dayto-day variability in average amplitudes of low-frequency heart period and blood pressure oscillations
(6, 9). There are also interpretive issues in understanding the link between these low-frequency oscillations.
For example, magnitude may not correlate with standard baroreflex gain measures (27), and elimination of
low-frequency heart period oscillations, through atrial
pacing, increases low-frequency blood pressure oscillations in only upright, and not supine, humans (23).
Thus some data suggest that heart period oscillations
do not buffer pressure consistently through the baroreflex.
In our study, we sought to augment low-frequency
oscillations in humans to delve further into the relationship between arterial pressure and cardiac interval
fluctuations. To accomplish this, we used two levels of
lower body negative pressure (LBNP) oscillating at 0.1
Hz. Low (10 mmHg) and moderate (30 mmHg) LBNP
were used, because the former does not generate a
heart period response, whereas the latter does (12, 16,
28). We hypothesized that the fluctuations in cardiac
filling with low-level oscillatory LBNP would be offset
appropriately, resulting in unchanged Mayer wave amplitude but a lowered cross-spectral coherence to heart
period. That is, preferential engagement of a noncardiogenic response would dissociate arterial pressure
and cardiac interval fluctuations. We further hypothesized that fluctuations in cardiac filling with moderate
oscillatory LBNP would generate an appropriate arterial baroreflex-mediated heart period response, leading
Address for reprint requests and other correspondence: J. A. Taylor, Laboratory for Cardiovascular Research, HRCA Research and
Training Institute, 1200 Centre St., Boston, MA 02131 (E-mail:
[email protected]).
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
arterial blood pressure; power spectral analysis; oscillatory
lower body negative pressure
LOW-FREQUENCY OSCILLATIONS
http://www.jap.org
8750-7587/01 $5.00 Copyright © 2001 the American Physiological Society
1559
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Hamner, J. W., Raymond J. Morin, James L. Rudolph, and J. Andrew Taylor. Inconsistent link between
low-frequency oscillations: R-R interval responses to augmented Mayer waves. J Appl Physiol 90: 1559–1564,
2001.—Low-frequency oscillations in arterial blood pressure
(Mayer waves) and R-R interval are thought to be linked
through the arterial baroreflex. To delve into this relationship, we applied low (10 mmHg) and moderate (30 mmHg)
lower body negative pressure (LBNP) in 10-s cycles to 18
healthy young male subjects. They showed no change in
average blood pressure with this oscillatory stimulus but did
show a significant decrease in R-R interval (P ⬍ 0.05) during
both levels of LBNP. In addition, we succeeded in augmenting low-frequency blood pressure oscillations in a graded
response to oscillatory LBNP level (P ⬍ 0.05) while significantly increasing low-frequency R-R interval oscillations
(P ⬍ 0.05). However, cross-spectral coherence between these
increased oscillations was highly variable across individuals
and stimulus level. Although nearly all subjects showed
significant coherence during basal conditions (n ⫽ 17), only
seven subjects maintained significant coherence during both
levels of LBNP. These results suggest that a complex interaction of regulatory mechanisms determines the link between low-frequency oscillations and the responses to even
low levels of LBNP.
1560
OSCILLATORY LBNP AND MAYER WAVES
METHODS
Subjects. Eighteen healthy young men, aged 22–32 yr
(body mass index 23.3 ⫾ 0.497), gave their informed consent
to participate in the study. The subjects were free from heart
and neurological disorders and were not taking any cardioactive medications. All the participants were normotensive
nonsmokers who refrained from alcohol and caffeine ingestion during the 24 h before the study. The experimental
protocol was approved by the Clinical Investigations Committee of the Hebrew Rehabilitation Center for Aged.
Protocol and measurements. Subjects were studied while
supine with their lower body sealed in an LBNP tank. A
vacuum pump with timing mechanism set to control suction
intervals to produce a 0.1-Hz oscillation was used. A manual
bleed-off valve, in conjunction with a pressure gauge, was
used to control tank pressure. The experimental protocol
consisted of three 5-min measurement periods at LBNP levels of 0 mmHg, oscillatory LBNP of 10 mmHg, and oscillatory
LBNP of 30 mmHg in random order. For all experimental
conditions, breathing was paced at 0.25 Hz; a 3-min acclimation period preceded the 5 min of data acquisition. Electrocardiogram lead II, beat-by-beat photoplethysmographic arterial pressure (Finapres, Ohmeda), respiration (Respitrace,
Ambulatory Monitoring), and tank pressure were recorded
continuously throughout each period. The signals were digitized at 500 Hz and stored for later analysis using commercial hardware and software (Windaq, Dataq Instruments,
and Matlab, The Mathworks).
Data analysis and statistics. Electrocardiogram R waves
and arterial pressure peaks and valleys were identified to
provide beat-by-beat R-R intervals and systolic and diastolic
pressures. Means and SDs were calculated from beat-by-beat
values. The time series of R-R interval, systolic pressure, and
diastolic pressure were linearly interpolated to provide a
1,500-point signal for frequency analysis. The power spectral
estimate of each signal was calculated via Welch’s averaged,
modified periodogram method (26). First, the interpolated
signals were divided into five equally overlapping segments
of 500 points each. Each individual window was then linearly
detrended, smoothed via a Hanning window, and fast Fourier
transformed to produce its magnitude squared. Cross-spectral estimates between variables were calculated from cross-
RESULTS
Mean R-R interval and arterial pressures. Table 1
lists average R-R intervals and arterial pressures for
all experimental conditions. Oscillatory LBNP resulted
in lower average R-R intervals than basal measures
(P ⬍ 0.05). These R-R interval changes corresponded to
a significant difference in heart rate only at moderate
Table 1. Average hemodynamic variables across subjects
Basal
Low OLBNP
Moderate LBNP
R-R Interval, ms
Systolic BP, mmHg
Diastolic BP, mmHg
Mean BP, mmHg
Pulse Pressure, mmHg
1,074 ⫾ 41
1,044 ⫾ 38*
1,027 ⫾ 37*
127 ⫾ 4
126 ⫾ 4
125 ⫾ 4
67 ⫾ 2
67 ⫾ 2
66 ⫾ 3
87 ⫾ 2
87 ⫾ 3
86 ⫾ 3
60 ⫾ 3
58 ⫾ 2
59 ⫾ 3
Values are means ⫾ SE. OLBNP, oscillatory lower body negative pressure; BP, blood pressure. * P ⬍ 0.05 vs. basal.
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spectral densities derived with the same parameters used to
estimate power spectra. Coherence was calculated from the
cross-spectral and power spectral measures to determine
whether a significant relationship existed between the variables at the frequencies of interest. Many researchers consider a coherence of 0.5 to be significant; however, it can be
exactly calculated on the basis of the number of data points
and window parameters (22). For our desired level of significance (P ⬍ 0.10) and our nine degrees of freedom, a coherence of ⱖ0.49 indicated a significant relationship between
variables. If a significant relationship existed, the transfer
function phase and magnitude were determined from the
standard cross spectrum normalized by the input’s (systolic
blood pressure) power spectrum. Frequency ranges for the
examination of Mayer waves were dependent on subject and
experimental condition. For basal conditions, the range of
maximal coherence between 0.05 and 0.15 Hz corresponding
to the peaks in the power spectrum of R-R interval and
systolic pressure was used to define the low-frequency oscillations (on average 0.0872 ⫾ 0.004 to 0.1113 ⫾ 0.003 Hz). For
oscillatory LBNP, the range of maximal coherence between
0.05 and 0.15 Hz corresponding to the peaks in the power
spectrum of tank pressure and systolic pressure was highly
significant for all subjects and was used to define the range of
oscillatory LBNP: from 0.0853 ⫾ 0.001 to 0.1056 ⫾ 0.001 Hz
(low oscillatory LBNP) and from 0.0852 ⫾ 0.001 to 0.1054 ⫾
0.001 Hz (moderate oscillatory LBNP). For all conditions, the
frequency range for respiration was simply defined as 0.2–
0.3 Hz. Mean powers for low-frequency and respiratory oscillations over these defined ranges were calculated for systolic and diastolic pressure and R-R interval, while crossspectral and transfer function indexes were derived for
systolic blood pressure to R-R interval. We chose to use
average values, rather than sums of power, to allow comparison among low-frequency ranges that differed between experimental conditions. Logarithmic transformations were applied to spectral powers to provide normal distributions for
application of standard Gaussian statistics; however, for ease
of interpretation, all values are reported in standard units.
Logarithmic transformations ensured normality in all cases,
except respiratory power. Effects of oscillatory LBNP on
average R-R intervals and arterial pressures were evaluated
by repeated-measure ANOVA with a Student-NewmanKeuls post hoc correction to identify significant differences.
For measures not normally distributed, a nonparametric
ANOVA on ranks with a Student-Newman-Keuls post hoc
correction was applied. Differences were considered significant at P ⬍ 0.05. Values are means ⫾ SE.
to unchanged or increased Mayer wave amplitude and
an augmented cross-spectral coherence relationship.
We found that increased low-frequency arterial pressure oscillations resulted from both low and moderate
levels of oscillatory LBNP that were accompanied by
increased low-frequency heart period oscillations. Surprisingly, the strength of the cross-spectral coherence
between low-frequency oscillations was highly unstable, within and among subjects, across the levels of
oscillatory LBNP. This inconsistent coherence relationship may belie mutable engagement of the multiple-feedback system responsible for generating blood
pressure Mayer waves.
OSCILLATORY LBNP AND MAYER WAVES
LBNP: 57.3 ⫾ 2.18 (basal) vs. 59.7 ⫾ 2.28 (moderate
oscillatory LBNP, P ⬍ 0.05). Oscillatory LBNP did not,
however, cause any change in average systolic, diastolic, or mean pressure.
Spectral characteristics. Figure 1 shows 30 s of representative raw data from one subject collected during
oscillatory LBNP of 10 mmHg at 0.1 Hz. Figure 1
shows the consistency of the generated LBNP wave as
well as the resulting oscillations in blood pressure.
This subject also shows a large corresponding 0.1-Hz
response in R-R interval.
Even with low-level oscillatory LBNP, low-frequency
oscillations in systolic pressure, diastolic pressure, and
R-R interval were significantly larger than corresponding oscillations during 0 mmHg LBNP (Table 2, Fig. 2).
With moderate oscillatory LBNP, systolic and diastolic
pressure powers in the low-frequency range were significantly greater. The higher level of oscillatory LBNP
did not alter R-R interval oscillations further (P ⫽
0.17). Oscillations at the respiratory frequency were
largely unaffected by oscillatory LBNP, except for
Fig. 2. Average spectral powers of all subjects at each oscillatory
LBNP (OLBNP) level from 0.04 to 0.3 Hz. Low-frequency oscillations
in systolic pressure were significantly different between all stimulus
levels (P ⬍ 0.05) and, in R-R interval, were significantly different
between oscillatory LBNP and basal conditions (P ⬍ 0.05).
small effects on systolic and diastolic pressure oscillations with 30 mmHg: 0.69 ⫾ 0.23 and 0.10 ⫾ 0.02
(basal) vs. 0.80 ⫾ 0.21 and 0.21 ⫾ 0.06 (moderate
oscillatory LBNP, P ⬍ 0.05).
The first step of our cross-spectral analysis, for each
subject, is shown in Fig. 3. The minimum coherence
value necessary for significance (0.49) is shown; during
0 mmHg all but one subject is above this minimum
value (and this subject is very close, 0.46). During
either level of oscillatory LBNP, the entire group average coherence was not significantly changed (Table 2).
However, simple group means masked highly variable
inter- and intraindividual differences in coherence
from basal measures. For example, 5 of 18 subjects
lacked coherence at the lower level of LBNP; 2 of these
subjects did not have coherence at the higher level of
LBNP, 3 subjects regained significant coherence, and 5
Table 2. Low-frequency average spectral variables
Basal
Low OLBNP
Moderate OLBNP
R-R Interval,
ms2
Systolic BP,
mmHg2
Diastolic BP,
mmHg2
R-R Interval-Systolic
BP Coherence
291 ⫾ 65
496 ⫾ 96.6*
836 ⫾ 259*
1.79 ⫾ 0.82
3.09 ⫾ 0.718*
5.70 ⫾ 1.300*†
0.658 ⫾ 0.178
2.41 ⫾ 0.533*
6.57 ⫾ 0.915*†
0.68 ⫾ 0.024
0.61 ⫾ 0.058
0.63 ⫾ 0.061
Values are means ⫾ SE. * P ⬍ 0.05 vs. basal. † P ⬍ 0.05 vs. low OLBNP.
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Fig. 1. Thirty seconds of low-level (10 mmHg) oscillatory lower body
negative pressure (LBNP) response from subject 11. Top: R-R interval in tachogram form; middle: arterial pressure; bottom: oscillations
in tank pressure.
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OSCILLATORY LBNP AND MAYER WAVES
four times the systolic blood pressure power (5.52 ⫾ 2.1
vs. 1.40 ⫾ 3.83, P ⫽ 0.0543), and four times the change
in R-R interval power (935 ⫾ 372 vs. 142.5 ⫾ 3.83, P ⬍
0.05). Figure 4 shows the changes in the logarithmically transformed low-frequency powers from basal
conditions to moderate oscillatory LBNP. All subjects
with significant coherence showed increases in both
systolic pressure and R-R interval power, while five of
the seven subjects who did not have significant coherence showed an increase in systolic pressure power
coupled with a decrease in R-R interval power.
DISCUSSION
others lost coherence. Among subjects with significant
coherence at all levels (n ⫽ 7), transfer function gain
and phase between systolic blood pressure and R-R
interval were not affected by oscillatory LBNP (P ⫽
0.79 and 0.273, respectively). In addition, there were
no significant differences in basal gain between the
group that maintained coherence and the group that
did not (P ⫽ 0.49). There were no significant differences in low-frequency basal powers or powers during
low-level oscillatory LBNP between these two groups.
However, examination of those subjects with and without coherence during moderate oscillatory LBNP
showed some significant differences in spectral powers.
Those with coherence between systolic blood pressure
and R-R interval power had almost four times the R-R
interval power (1,170 ⫾ 390 vs. 307 ⫾ 120, P ⬍ 0.05),
Fig. 4. Change in low-frequency R-R interval
power vs. change in low-frequency systolic blood
pressure power between moderate oscillatory
LBNP and basal conditions. Change scores represent logarithmically transformed powers.
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Fig. 3. Low-frequency coherence between systolic blood pressure and
R-R interval for all subjects at each oscillatory LBNP level. Dashed
line, coherence necessary for significance at 0.49. Only 7 of 18
subjects maintained significant coherence for all 3 conditions.
We found that low and moderate oscillatory LBNP
augment low-frequency pressure oscillations in a
graded fashion without affecting average blood pressure. We also observed subtle, yet significant, reductions in average R-R intervals during even low-level
oscillatory LBNP and profound increases in low-frequency R-R interval oscillations during both levels.
Despite the fact that the forced oscillations in blood
pressure and cardiac interval were large in magnitude
and centered within a narrow frequency band, the
relationship between the two was highly inconsistent,
between subjects and across conditions. Our data have
implications for commonly accepted notions of hemodynamic regulation on two fronts. First, low levels of
LBNP can alter arterial pressure, supporting previous
evidence implicating arterial baroreflex engagement.
Second, the simple linear input-output relationship
between low-frequency blood pressure and R-R interval oscillations may not be maintained across individuals and conditions, indicating a level of complexity
commonly overlooked.
Effects of oscillatory LBNP. In agreement with previous work, low-level LBNP had no effect on average
blood pressures (12, 16, 28). However, in contrast to
previous studies, our subjects did not demonstrate any
OSCILLATORY LBNP AND MAYER WAVES
regulatory actions of the arterial baroreflex. It seems
most likely that no single reflex was responsible but
that multiple regulatory systems were engaged and
that nonlinear interactions explain the lack of coherence between arterial pressure and R-R interval oscillations. It should be noted that a lack of significant
coherence does not necessarily indicate that any single
reflex is behaving in a nonlinear fashion, only that, in
a broad assessment of blood pressure’s effect on R-R
interval, the linear single input-output model is insufficient to describe their relationship. However, independent of any mechanism, our data clearly show that
low-level LBNP can generate changes in arterial pressure and R-R interval.
Links between low-frequency oscillations. Our data
raise questions about assumptions commonly made
regarding relationships between low-frequency oscillations in arterial pressure and heart period. We were
able to generate large and consistent low-frequency
oscillations in arterial pressure and R-R interval during oscillatory LBNP. Significant coherence was evident in all but one subject during basal conditions but
in only seven subjects during both levels of oscillatory
LBNP. The lack of R-R interval coherence to consistent-amplitude arterial pressure oscillations may have
implications for the interpretation of spectral data.
Disappearance of cross-spectral coherence may indicate nonlinearities arising from interplay between
blood pressure-buffering mechanisms. For example, a
mechanical damping of central venous pressure
changes by the heart may reduce coherence between
arterial pressure and R-R interval during LBNP (25).
In addition, there is a state dependency in arterial
pressure buffering by R-R interval at the Mayer wave
frequency (23), which suggests that an alterable interaction of cardiac and vascular mechanisms is responsible for arterial pressure fluctuations. Moreover, inconsistency between and among subjects demonstrates
heterogeneous responses in a presumably homogenous
population. Thus the engagement of these nonlinearities may be state and trait dependent. Cross-spectral
analysis requires linearity between input and output,
which may not hold for arterial pressure and R-R
interval in all conditions. Nonetheless, significant coherence tended to occur when R-R interval and arterial
pressure oscillations changed in parallel.
Limitations. Dependency on standard spectral techniques limited the amount of information we could
glean from this study. We had no reason to suspect that
cross-spectral analysis would prove ineffective at examining the relationship between pressure and R-R
interval. Time-varying estimates of spectral power,
such as the Wigner distribution, spectrograms, and
scalograms, show how a signal’s frequency characteristics change with time, and time-varying cross spectra
show the interaction of multiple variables with time
(7). These techniques, however, are most suited to
characterize transients and to eliminate nonstationarities associated with changing experimental and/or behavioral conditions. The nature and consistency of the
arterial pressure oscillations would limit these analy-
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change in average blood pressure during moderate
LBNP and demonstrated significant shortening of R-R
interval during both LBNP levels. The lack of change
in average blood pressure may not be surprising, however, inasmuch as the stimulus we used includes an
acute response and brief recovery from LBNP during a
very short period of time (10 s). The acute response
may involve the expected depression of blood pressure,
followed by an overshoot during the recovery period,
resulting in no change in average blood pressure. The
changes in R-R interval did not necessarily correspond
to a hemodynamic response to low-level LBNP;
changes in heart rate were not significant. However,
the linear relationship between R-R interval and vagal
outflow would suggest an autonomic response (8, 21).
Our subjects also showed a graded increase in lowfrequency blood pressure oscillations with oscillatory
LBNP accompanied by an increase in low-frequency
R-R interval oscillations (which were not graded, however). Cross-spectral coherence, although significant
during basal conditions, showed high inter- and intraindividual variability during oscillatory LBNP. Among
subjects with significant coherence across all LBNP
levels (n ⫽ 7), there was no change in transfer function
magnitude during oscillatory LBNP. During moderate,
but not low, oscillatory LBNP, a decrease in R-R interval power from basal conditions generally indicated
lack of a significant coherence relationship between
systolic blood pressure and R-R interval. This may
reflect a differential engagement of blood pressure regulatory mechanisms that is not uniform across subjects
and between conditions.
It is possible that a mechanistic heterogeneity explains the range of responses that were demonstrated.
Oscillations in tank pressure could have uncovered a
transient arterial baroreflex response to LBNP onset or
could have entrained the cardiopulmonary response. A
sudden drop in stroke volume at the onset of LBNP
would reduce the pulsatile stretch in baroreceptive
arteries and decrease arterial pressure (24). An acute
arterial baroreflex-mediated R-R interval response,
dictated by the pressure change, could generate a synchronous oscillation in cardiac interval. Another possibility is that the response is caused by a synchronization of cardiopulmonary receptor activity to the 0.1-Hz
stimulus. Oscillating changes in central venous pressure could cause oscillations in sympathetic nerve activity, which could result in systemic resistance and,
hence, arterial pressure fluctuations. Thus cyclic cardiopulmonary activation could generate arterial pressure oscillations. Nonetheless, the response could not
be a purely cardiopulmonary one, since there was a
significant R-R interval change, indicating arterial
baroreflex engagement. The oscillations in cardiac filling could also have activated the Bainbridge reflex,
further complicating the regulatory landscape. At high
levels of cardiac filling, the Bainbridge reflex purportedly stimulates vagal withdraw, thereby increasing
R-R interval (11). If the reverse were true at low levels
of cardiac filling induced by LBNP, the corresponding
decrease in R-R interval would work to counteract the
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OSCILLATORY LBNP AND MAYER WAVES
This study was supported by The American Federation for Aging
Research and National Institute on Aging Grants R29 AG-14376
(J. A. Taylor) and R01 AG-14420-01.
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ses, such that they would be unlikely to shed additional
light on the interactions between R-R interval and
blood pressure. Time domain modeling has proven to
be very effective at examining cardiovascular systems;
unfortunately, lengthy physiological recordings are required for proper analysis, and extreme care must be
taken to produce interpretable parameters (1, 4, 5, 14).
Spectral techniques are a valuable scientific tool, but
perhaps too limited to properly examine the underlying
physiology of nonstationary cardiovascular variables.
Another limiting factor is our inability to assess the
effect of the sympathetic nervous system during oscillatory LBNP. If sympathetic nerve recordings had been
obtained or sympathetic blockade achieved, we could
more accurately discern the physiological impact of our
stimulus. However, these limitations do not undermine
the implications of our present findings; they merely
give direction for further study.
Conclusions. The fact that subjects showed a shorter
average R-R interval during oscillatory LBNP challenges the notion that low-level LBNP cannot affect
R-R interval. In addition, we successfully enhanced
low-frequency oscillations in blood pressure and R-R
interval, which is significant in several respects. Oscillatory LBNP provides a stimulus that is reliably able to
create repeated drops in arterial pressure for the examination of a myriad of pressure regulatory systems.
Specifically, we sought to illuminate the R-R interval
response to these repeated drops in arterial pressure.
However, we found that the simple linear arterial
baroreflex model incorporated into cross-spectral analysis cannot explain blood pressure regulation across
conditions. Although standard frequency domain techniques are a powerful tool, ultimately, scientists may
have to move to nonlinear and/or time-varying analysis
methods to further understand cardiovascular regulation of beat-by-beat oscillations.