Respiratory sinus arrhythmia and submersion bradycardia in bottlenose dolphins (Tursiops truncatus)

ABSTRACTAmong the many factors that influence the cardiovascular adjustments of marine mammals is the act of respiration at the surface, which facilitates rapid gas exchange and tissue re-perfusion between dives. We measured heart rate (fH) in six adult male bottlenose dolphins (Tursiops truncatus) spontaneously breathing at the surface to quantify the relationship between respiration and fH, and compared this with fH during submerged breath-holds. We found that dolphins exhibit a pronounced respiratory sinus arrhythmia (RSA) during surface breathing, resulting in a rapid increase in fH after a breath followed by a gradual decrease over the following 15–20 s to a steady fH that is maintained until the following breath. RSA resulted in a maximum instantaneous fH (ifH) of 87.4±13.6 beats min−1 and a minimum ifH of 56.8±14.8 beats min−1, and the degree of RSA was positively correlated with the inter-breath interval (IBI). The minimum ifH during 2 min submerged breath-holds where dolphins exhibited submersion bradycardia (36.4±9.0 beats min−1) was lower than the minimum ifH observed during an average IBI; however, during IBIs longer than 30 s, the minimum ifH (38.7±10.6 beats min−1) was not significantly different from that during 2 min breath-holds. These results demonstrate that the fH patterns observed during submerged breath-holds are similar to those resulting from RSA during an extended IBI. Here, we highlight the importance of RSA in influencing fH variability and emphasize the need to understand its relationship to submersion bradycardia.

Download Full-text

Assessment of parasympathetic control of heart rate by a noninvasive method

AJP Heart and Circulatory Physiology ◽

10.1152/ajpheart.1984.246.6.h838 ◽

1984 ◽

Vol 246 (6) ◽

pp. H838-H842 ◽

Cited By ~ 25

Author(s):

F. M. Fouad ◽

R. C. Tarazi ◽

C. M. Ferrario ◽

S. Fighaly ◽

C. Alicandri

Keyword(s):

Heart Rate ◽

Respiratory Sinus Arrhythmia ◽

Separate Group ◽

Noninvasive Method ◽

Sinus Arrhythmia ◽

Beta Adrenergic ◽

Normal Volunteers ◽

Vagal Control ◽

Parasympathetic Control ◽

The Relationship

The degree of parasympathetic control of heart rate was assessed by the abolition of respiratory sinus arrhythmia with atropine. Peak-to-peak variations in heart periods (VHP) before atropine injection correlated significantly (r = 0.90, P less than 0.001) with parasympathetic control, indicating that VHP alone may be used as a noninvasive indicator of the parasympathetic control of heart rate. Pharmacologic blockade of beta-adrenergic supply in a separate group of normal volunteers did not alter the relationship between VHP and parasympathetic control, indicating that the condition of the experiment (complete rest in a quiet atmosphere) allows the use of VHP alone without pharmacologic interventions to characterize the vagal control of heart rate in humans.

Download Full-text

The diving physiology of bottlenose dolphins (Tursiops truncatus). I. Balancing the demands of exercise for energy conservation at depth

Journal of Experimental Biology ◽

10.1242/jeb.202.20.2739 ◽

1999 ◽

Vol 202 (20) ◽

pp. 2739-2748 ◽

Cited By ~ 10

Author(s):

T.M. Williams ◽

J.E. Haun ◽

W.A. Friedl

Keyword(s):

Heart Rate ◽

Blood Lactate ◽

Tursiops Truncatus ◽

Marine Mammals ◽

Bottlenose Dolphins ◽

Lactate Concentration ◽

Blood Lactate Concentration ◽

Energetic Cost ◽

Breath Holding ◽

Breath Hold

During diving, marine mammals must rely on the efficient utilization of a limited oxygen reserve sequestered in the lungs, blood and muscles. To determine the effects of exercise and apnea on the use of these reserves, we examined the physiological responses of adult bottlenose dolphins (Tursiops truncatus) trained to breath-hold on the water surface or to dive to submerged targets at depths between 60 and 210 m. Changes in blood lactate levels, in partial pressures of oxygen and carbon dioxide and in heart rate were assessed while the dolphins performed sedentary breath-holds. The effects of exercise on breath-hold capacity were examined by measuring heart rate and post-dive respiration rate and blood lactate concentration for dolphins diving in Kaneohe Bay, Oahu, Hawaii. Ascent and descent rates, stroke frequency and swimming patterns were monitored during the dives. The results showed that lactate concentration was 1.1+/−0.1 mmol l(−1) at rest and increased non-linearly with the duration of the sedentary breath-hold or dive. Lactate concentration was consistently higher for the diving animals at all comparable periods of apnea. Breakpoints in plots of lactate concentration and blood gas levels against breath-hold duration (P(O2), P(CO2)) for sedentary breath-holding dolphins occurred between 200 and 240 s. In comparison, the calculated aerobic dive limit for adult dolphins was 268 s. Descent and ascent rates ranged from 1.5 to 2.5 m s(−1) during 210 m dives and were often outside the predicted range for swimming at low energetic cost. Rather than constant propulsion, diving dolphins used interrupted modes of swimming, with more than 75 % of the final ascent spent gliding. Physiological and behavioral measurements from this study indicate that superimposing swimming exercise on apnea was energetically costly for the diving dolphin but was circumvented in part by modifying the mode of swimming.

Download Full-text

Conditioned Variation in Heart Rate During Static Breath-Holds in the Bottlenose Dolphin (Tursiops truncatus)

Frontiers in Physiology ◽

10.3389/fphys.2020.604018 ◽

2020 ◽

Vol 11 ◽

Cited By ~ 2

Author(s):

Andreas Fahlman ◽

Bruno Cozzi ◽

Mercy Manley ◽

Sandra Jabas ◽

Marek Malik ◽

...

Keyword(s):

Heart Rate ◽

Tursiops Truncatus ◽

Marine Mammals ◽

Bottlenose Dolphins ◽

Bubble Formation ◽

Rate Of Change ◽

Breath Hold ◽

Short Breath ◽

Breath Hold Duration ◽

Spontaneous Breath

Previous reports suggested the existence of direct somatic motor control over heart rate (fH) responses during diving in some marine mammals, as the result of a cognitive and/or learning process rather than being a reflexive response. This would be beneficial for O2 storage management, but would also allow ventilation-perfusion matching for selective gas exchange, where O2 and CO2 can be exchanged with minimal exchange of N2. Such a mechanism explains how air breathing marine vertebrates avoid diving related gas bubble formation during repeated dives, and how stress could interrupt this mechanism and cause excessive N2 exchange. To investigate the conditioned response, we measured the fH-response before and during static breath-holds in three bottlenose dolphins (Tursiops truncatus) when shown a visual symbol to perform either a long (LONG) or short (SHORT) breath-hold, or during a spontaneous breath-hold without a symbol (NS). The average fH (ifHstart), and the rate of change in fH (difH/dt) during the first 20 s of the breath-hold differed between breath-hold types. In addition, the minimum instantaneous fH (ifHmin), and the average instantaneous fH during the last 10 s (ifHend) also differed between breath-hold types. The difH/dt was greater, and the ifHstart, ifHmin, and ifHend were lower during a LONG as compared with either a SHORT, or an NS breath-hold (P < 0.05). Even though the NS breath-hold dives were longer in duration as compared with SHORT breath-hold dives, the difH/dt was greater and the ifHstart, ifHmin, and ifHend were lower during the latter (P < 0.05). In addition, when the dolphin determined the breath-hold duration (NS), the fH was more variable within and between individuals and trials, suggesting a conditioned capacity to adjust the fH-response. These results suggest that dolphins have the capacity to selectively alter the fH-response during diving and provide evidence for significant cardiovascular plasticity in dolphins.

Download Full-text

A Theoretical Appraisal of the Dependence of Respiratory Sinus Arrhythmia on Gradual Vagal Blockade

Methods of Information in Medicine ◽

10.1055/s-0038-1633834 ◽

2004 ◽

Vol 43 (01) ◽

pp. 52-55 ◽

Cited By ~ 3

Author(s):

E. Pyetan ◽

S. Akselrod

Keyword(s):

Heart Rate ◽

Respiratory Sinus Arrhythmia ◽

Vagal Tone ◽

Vagal Activity ◽

Theoretical Evaluation ◽

Sinus Arrhythmia ◽

Cardiac Vagal Tone ◽

Closed Set ◽

Vagal Blockade ◽

The Relationship

Summary Motivation: The high frequency (HF) indices of heart rate variability (HRV), which reflect the magnitude of respiratory sinus arrhythmia (RSA), have been repeatedly used as measures of cardiac vagal tone. Recent studies, however, have shown experimentally that variations in these indices do not necessarily reflect proportional changes in cardiac parasympathetic outflow. Objective: The goal of this study was to obtain a physiological-based theoretical evaluation of the relationship between RSA and cardiac vagal tone, which will help explain conflicting experimental results previously published. Methods: We derived a theoretical model for heart rate (HR) response to gradual vagal blockade. The model implements the integral-pulse-frequency-modulation (IPFM) approach to sinoatrial (SA) node physiology. The level of vagal blockade was simulated by the addition of a cardio-selective muscarinic antagonist. Results and Conclusion: The derivations of the model lead to a closed set of equations, from which the dependence of the HF indices on the level of vagal blockade is deduced. It is shown that several aspects of the physiological condition may have a substantial effect on this relationship: the level of baseline vagal activity, the relationship between vagal tone and the fluctuations in its traffic, the level of sympathetic activity, etc… Hence, changes in the HF indices of HRV provide a plausible assessment of the changes in cardiac vagal tone only under a specific range of physiological conditions.

Download Full-text

Respiratory sinus arrhythmia is associated with efficiency of pulmonary gas exchange in healthy humans

AJP Heart and Circulatory Physiology ◽

10.1152/ajpheart.00893.2002 ◽

2003 ◽

Vol 284 (5) ◽

pp. H1585-H1591 ◽

Cited By ~ 65

Author(s):

Nicholas D. Giardino ◽

Robb W. Glenny ◽

Soo Borson ◽

Leighton Chan

Keyword(s):

Heart Rate ◽

Gas Exchange ◽

Tidal Volume ◽

Respiration Rate ◽

Respiratory Sinus Arrhythmia ◽

Minute Ventilation ◽

Pulmonary Gas Exchange ◽

Sinus Arrhythmia ◽

Paced Breathing ◽

Healthy Humans

Respiratory sinus arrhythmia (RSA) may be associated with improved efficiency of pulmonary gas exchange by matching ventilation to perfusion within each respiratory cycle. Respiration rate, tidal volume, minute ventilation (V˙e), exhaled carbon dioxide (V˙co 2), oxygen consumption (V˙o 2), and heart rate were measured in 10 healthy human volunteers during paced breathing to test the hypothesis that RSA contributes to pulmonary gas exchange efficiency. Cross-spectral analysis of heart rate and respiration was computed to calculate RSA and the coherence and phase between these variables. Pulmonary gas exchange efficiency was measured as the average ventilatory equivalent of CO2(V˙e/V˙co 2) and O2(V˙e/V˙o 2). Across subjects and paced breathing periods, RSA was significantly associated with CO2 (partial r = −0.53, P = 0.002) and O2 (partial r = −0.49, P = 0.005) exchange efficiency after controlling for the effects of age, respiration rate, tidal volume, and average heart rate. Phase between heart rate and respiration was significantly associated with CO2 exchange efficiency (partial r = 0.40, P = 0.03). These results are consistent with previous studies and further support the theory that RSA may improve the efficiency of pulmonary gas exchange.

Download Full-text

Measures of RSA Suppression, Attentional Control, and Negative Affect Predict Self-Ratings of Executive Functions

Journal of Psychophysiology ◽

10.1027/0269-8803/a000053 ◽

2011 ◽

Vol 25 (4) ◽

pp. 164-173 ◽

Cited By ~ 7

Author(s):

Brian Healy ◽

Aaron Treadwell ◽

Mandy Reagan

Keyword(s):

College Students ◽

Heart Rate ◽

Regression Analysis ◽

Individual Differences ◽

Negative Affect ◽

Respiratory Sinus Arrhythmia ◽

Attentional Control ◽

Executive Processes ◽

Sinus Arrhythmia ◽

Low Levels

The current study was an attempt to determine the degree to which the suppression of respiratory sinus arrhythmia (RSA) and attentional control were influential in the ability to engage various executive processes under high and low levels of negative affect. Ninety-four college students completed the Stroop Test while heart rate was being recorded. Estimates of the suppression of RSA were calculated from each participant in response to this test. The participants then completed self-ratings of attentional control, negative affect, and executive functioning. Regression analysis indicated that individual differences in estimates of the suppression of RSA, and ratings of attentional control were associated with the ability to employ executive processes but only when self-ratings of negative affect were low. An increase in negative affect compromised the ability to employ these strategies in the majority of participants. The data also suggest that high attentional control in conjunction with attenuated estimates of RSA suppression may increase the ability to use executive processes as negative affect increases.

Download Full-text

Direct effect of PaCO2 on respiratory sinus arrhythmia in conscious humans

AJP Heart and Circulatory Physiology ◽

10.1152/ajpheart.00554.2001 ◽

2002 ◽

Vol 282 (3) ◽

pp. H973-H976 ◽

Cited By ~ 38

Author(s):

Nobuko Sasano ◽

Alex E. Vesely ◽

Junichiro Hayano ◽

Hiroshi Sasano ◽

Ron Somogyi ◽

...

Keyword(s):

Gas Exchange ◽

Direct Effect ◽

Respiratory Sinus Arrhythmia ◽

Random Order ◽

Mean Amplitude ◽

Frequency Component ◽

Pulmonary Gas Exchange ◽

High Frequency Component ◽

Sinus Arrhythmia ◽

End Tidal

Respiratory sinus arrhythmia (RSA) may improve the efficiency of pulmonary gas exchange by matching the pulmonary blood flow to lung volume during each respiratory cycle. If so, an increased demand for pulmonary gas exchange may enhance RSA magnitude. We therefore tested the hypothesis that CO2directly affects RSA in conscious humans even when changes in tidal volume (VT) and breathing frequency ( F B), which indirectly affect RSA, are prevented. In seven healthy subjects, we adjusted end-tidal Pco 2 (Pet CO2 ) to 30, 40, or 50 mmHg in random order at constant VT and F B. The mean amplitude of the high-frequency component of R-R interval variation was used as a quantitative assessment of RSA magnitude. RSA magnitude increased progressively with Pet CO2 ( P < 0.001). Mean R-R interval did not differ at Pet CO2 of 40 and 50 mmHg but was less at 30 mmHg ( P < 0.05). Because VT and F B were constant, these results support our hypothesis that increased CO2directly increases RSA magnitude, probably via a direct effect on medullary mechanisms generating RSA.

Download Full-text

Respiratory sinus arrhythmia in the denervated human heart

Journal of Applied Physiology ◽

10.1152/jappl.1989.67.4.1447 ◽

1989 ◽

Vol 67 (4) ◽

pp. 1447-1455 ◽

Cited By ~ 192

Author(s):

L. Bernardi ◽

F. Keller ◽

M. Sanders ◽

P. S. Reddy ◽

B. Griffith ◽

...

Keyword(s):

Heart Rate ◽

Respiratory Sinus Arrhythmia ◽

Human Heart ◽

Normal Subjects ◽

Respiratory Frequency ◽

Autonomic Tone ◽

Sinus Arrhythmia ◽

Transplant Patients ◽

Myocardial Wall ◽

Analysis Technique

We performed this study to test whether the denervated human heart has the ability to manifest respiratory sinus arrhythmia (RSA). With the use of a highly sensitive spectral analysis technique (cross correlation) to define beat-to-beat coupling between respiratory frequency and heart rate period (R-R) and hence RSA, we compared the effects of patterned breathing at defined respiratory frequency and tidal volumes (VT), Valsalva and Mueller maneuvers, single deep breaths, and unpatterned spontaneous breathing on RSA in 12 normal volunteers and 8 cardiac allograft transplant recipients. In normal subjects R-R changes closely followed changes in respiratory frequency (P less than 0.001) but were little affected by changes in VT. On the R-R spectrum, an oscillation peak synchronous with respiration was found in heart transplant patients. However, the average magnitude of the respiration-related oscillations was 1.7–7.9% that seen in normal subjects and was proportionally more influenced by changes in VT. Changes in R-R induced by Valsalva and Mueller maneuvers were 3.8 and 4.9% of those seen in normal subjects, respectively, whereas changes in R-R induced by single deep breaths were 14.3% of those seen in normal subjects. The magnitude of RSA was not related to time since the heart transplantation, neither was it related to patient age or sex. Thus the heart has the intrinsic ability to vary heart rate in synchrony with ventilation, consistent with the hypothesis that changes, or rate of changes, in myocardial wall stretch might alter intrinsic heart rate independent of autonomic tone.

Download Full-text