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. 2014 Sep:41:781-784.

Three Independent Forms of Cardio-Respiratory Coupling: Transitions across Sleep Stages

Ronny P Bartsch  1 , Kang Kl Liu  2 , Qianli Dy Ma  3 , Plamen Ch Ivanov  4
Affiliations

Three Independent Forms of Cardio-Respiratory Coupling: Transitions across Sleep Stages

Ronny P Bartsch et al. Comput Cardiol (2010). 2014 Sep.

Abstract

We demonstrate that the cardiac and respiratory system exhibit three distinct forms of coupling that are independent from each other, respond differently to key physiologic parameters, and act on different time scales. We find that all three forms of coupling undergo pronounced phase transitions across sleep stages characterized by different stratification patterns, indicating markedly different response to changes in neuroautonomic control. Our analyses show that all three forms of cardio-respiratory interaction are not of constant strength but are of transient and intermittent nature with "on" and "off" periods, and that these forms of coupling, representing different aspects of physiologic regulation, can simultaneously coexist.

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Figures

Figure 1
Figure 1. Respiratory sinus arrhythmia (RSA), classic form of cardio-respiratory coupling
characterized by a periodic variation of the heart rate (HR) within each breathing cycle. The strength of the coupling is defined by the amplitude of the HR variation measured relative to the mean heart rate HR¯ (RSA amplitude). Data points represent instantaneous HR, normalized to the mean HR¯ within each breathing cycle, for a period of 200 sec over pairs of consecutive breathing cycles. RSA is highlighted by a sinusoidal least-square-fit line to the data points. Data are recorded from a healthy subject during deep sleep.
Figure 2
Figure 2. Coexisting forms of cardio-respiratory coupling: RSA and phase synchronization (CRPS) represent different and independent forms of coupling
While RSA leads to periodic modulation of the heart rate within each breathing cycle (sinusoidal line), CRPS leads to clustering of heartbeats (ovals) at certain phases ϕr of the breathing cycle. Shown are consecutive heartbeats over a period of 200 sec. The x-axis indicates the phases ϕr of the breathing cycle where heartbeats occur. Data are selected from the same healthy subject during the same deep sleep episode as in Fig. 1, but represent a different segment of the episode where both RSA and CRPS coexist.
Figure 3
Figure 3. RSA and phase synchronization (CRPS) are distinct forms of cardio-respiratory coupling and their strength depend differently on breathing frequency
(a) RSA nonlinearly increases (> 250%) with decreasing breathing frequency, and drops abruptly for very low breathing frequencies (Spearman’s rank order correlation: ρ = −0.42, p < 10−3). (b) In contrast to RSA, the strength of CRPS (length of CRPS episodes) is independent of the breathing frequency (Spearman ρ ≈ 0, p < 10−3). Error bars represent the standard error. Data are averaged over all subjects during the entire sleep period.
Figure 4
Figure 4. RSA and CRPS involve different mechanisms of cardio-respiratory coupling and respond differently to changes in autonomic parasympathetic control
(a) RSA strongly increases with increasing RMSSD of heartbeat RR intervals, a measure of parasympathetic tone (Spearman ρ = 0.69, p < 10−3). (b) In contrast to RSA, the strength of CRPS does not significantly change with increasing RMSSD (Spearman ρ ≈ 0, p < 10−3). Error bars represent the standard error. Data are averaged over all subjects during the entire sleep period as in Fig. 3.
Figure 5
Figure 5. Phase transitions in the strength of two different forms of cardio-respiratory coupling across sleep stages
(a) RSA and (b) CRPS exhibit very different stratification patterns across sleep stages, indicating (i) that each form of cardio-respiratory coupling undergoes a complex re-organization with sleep-stage transitions; and (ii) that RSA and CRPS are two independent forms of coupling, the streghten of which change differently during different sleep stages. Columns in each panel represent the group average of all subjects; error bars correspond to the standard error. CRPS is estimated as the percent of data segments in the entire recording for a given sleep stage where heart rate and respiratory rate are phase-synchronized.
Figure 6
Figure 6. Change in the strength of CRPS, RSA and breathing frequency (Bfreq) across sleep stages
Group average values for each sleep stage are normalized with respect to REM sleep. Notably, the sensitivity of CRPS to sleep-stage transitions is by a factor of 10 higher than RSA, indicating that sleep regulation and related changes in breathing frequency across sleep stages affect these two forms of cardio-respiratory coupling very differently.
Figure 7
Figure 7. Third form of cardio-respiratory coupling: time delay stability (TDS)
Segments of (a) heart rate (HR) and (b) respiratory rate (Resp) in 60 sec time windows (I), (II), (III) and (IV). Synchronous bursts in HR and Resp (signals normalized to zero mean and unit standard deviation) lead to pronounced cross-correlation (c) within each time window in (a) and (b), and stable time delay characterized by segments of constant τ0 as shown in (d) — four red dots highlighted by a blue box in panel (d) represents the time delay for the 4 time windows. Note the transition from strongly fluctuating behavior in τ0 to a stable time delay regime at the transition from deep sleep to light sleep at around 9400 sec (shaded area) in panel (d). The TDS analysis is performed on overlapping moving windows with a step of 30 sec. Long periods of constant τ0 indicate strong TDS coupling. (e) Note the pronounced stratification pattern in TDS: stronger coupling during wake and light sleep, and weaker during REM and deep sleep, which is very different from the stratification pattern of RSA and CRPS across sleep stages in Fig. 5.
Figure 8
Figure 8. Coexisting forms of cardio-respiratory coupling, CRPS and TDS, function at different time scales
Probability distributions of the length of CRPS epochs (red) and of TDS epochs (light-blue) indicate significant difference in the average epoch length. Thus, different forms of coupling acting on very different time scales are captured by these two measures. Both measures, CRPS and TDS, reveal a transient nature of the cardio-respiratory coupling, with “on” and “off” periods even within a single sleep stage. Results are obtained from all healthy subjects during the entire sleep period.
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