Elsevier

Heart Rhythm

Volume 18, Issue 3, March 2021, Pages 465-472
Heart Rhythm

Experimental
The frequency spectrum of sympathetic nerve activity and arrhythmogenicity in ambulatory dogs

https://doi.org/10.1016/j.hrthm.2020.11.023Get rights and content

Background

Sympathetic nerve activity, heart rate (HR), and blood pressure (BP) all have very low frequency (VLF), low frequency (LF), and high frequency (HF) oscillations.

Objective

The purpose of this study was to test the hypothesis that the frequency spectra of subcutaneous nerve activity (ScNA), stellate ganglion nerve activity (SGNA), HR, and BP are important to cardiac arrhythmogenesis.

Methods

We used radiotransmitters to record SGNA, ScNA, HR, and BP in 6 ambulatory dogs and determined the dominant frequency and paroxysmal atrial tachyarrhythmias (PATs) episodes in 3-minute windows over a 24-hour period.

Results

The frequency spectra determined in ScNA reflected that in SGNA. HF oscillations were present in both ScNA and SGNA at all time but could be overshadowed by the much larger LF and VLF burst activities. The dominant frequency could occur in any of the 3 frequency bands. There were circadian variations with more frequent occurrences of HF oscillations at night. HF oscillations in HR and BP matched HF oscillations in SGNA and ScNA. PATs occurred only when dominant frequencies of SGNA and ScNA were in the LF and VLF bands.

Conclusion

HF oscillations in BP and HR correlate with HF oscillations in sympathetic nerve activity and are present at all time. HF oscillations can be overshadowed by the much larger LF and VLF burst activities. PATs occur only when LF or VLF, but not when HF, is the dominant frequency. The frequency spectra determined in ScNA reflect that in SGNA.

Introduction

The nerve structures transmit electrical signals to the end organs by both amplitude modulation and frequency modulation.1 The frequency modulation signal is more resistant to distortion by noise than the amplitude modulation signal. Sympathetic nerve activity (SNA) recorded by microneurography and other physiological activities such as heart rate (HR), blood pressure (BP), and respiration have very high frequency (VHF, >0.40 Hz), high frequency (HF, 0.15–0.40 Hz), low frequency (LF, 0.04–0.15 Hz), and very low frequency (VLF, 0.01–0.04 Hz) periodicities (oscillations).2, 3, 4, 5, 6, 7 There are marked respiratory periodicities that correspond to HF oscillations in muscle SNA, indicating that SNA oscillations secondary to loading/unloading of carotid sinus baroreceptors and pulmonary stretch receptors are responsible for the HF band. The LF and VLF bands are not coherent with respiration. Nitroglycerine infusion, exercise, and transient coronary occlusion increase the LF component and the LF/HF ratio,8 suggesting their positive correlation with the sympathetic tone. Because sympathetic activity induces periodic LF changes of repolarization, the LF periodic repolarization dynamics measured with the T-wave vector can be used to predict mortality after myocardial infarction.9 Better understanding of the mechanisms of various frequencies of oscillations may significantly improve the understanding of cardiac arrhythmogenesis. None of the previous studies were done with direct recordings of stellate ganglion nerve activity (SGNA), which is a major source of extrinsic cardiac innervation. In addition, whether the frequency oscillations are observed in the subcutaneous nerve activity (ScNA) remains unknown. The purpose of the present study was to perform simultaneous recording of SGNA, electrocardiogram (ECG), ScNA, and arterial BP to test the hypotheses that (1) the fast Fourier transform analyses of SGNA can detect VLF, LF, and HF bands as in analyses of HR, BP, and muscle SNA; (2) the frequency spectrum of ScNA is the same as that of SGNA; and (3) spontaneous paroxysmal atrial tachyarrhythmias (PATs) occur in the time windows only when VLF or LF is the dominant frequency (DF).

Section snippets

Surgical procedures

Animal protocol was approved by the Institutional Animal Care and Use Committee of Indiana University and conformed to the National Institute of Health Guide for the Care and Use of Laboratory Animals. The baseline recordings of 6 dogs used in a previous study10 were analyzed to test the proposed hypotheses. The detailed surgical procedures have been described in that article. The recordings were performed while the dogs were ambulatory. D70-CCTP radiotransmitters manufactured by the Data

Patterns of SNA

Dogs were allowed to recover for >2 weeks (average 18 ± 3 days) before a 24-hour recording during which SGNA, ScNA, BP, and HR were continuously collected. Manual analyses identified nerve bursts occurred at intervals consistent with VLF, LF, and HF in SGNA, BP, and HR (Figures 1 and 2). Figure 1A shows a 3-minute recording from 1 dog, showing several distinct bursts in SGNA and ScNA. The periods (intervals between bursts) were 16.7, 16.9, or 52.5 seconds. These periods were consistent with LF

Discussion

We found that both SGNA and ScNA had distinct VLF, LF, and HF discharge patterns in normal ambulatory dogs. The frequency spectrum of ScNA matched with that of SGNA. HF oscillations were seen both in the SNA and in the HR and BP analyses. All PATs episodes occurred when the DF was in the VLF and LF bands. These findings suggest an association between the frequency spectra of SNA and PATs.

Conclusion

HF oscillations in BP and HR correlate with HF oscillations in SNA and are present at all time. HF oscillations can be overshadowed by the much larger LF and VLF burst activities. PATs occur only when LF or VLF, but not when HF, is the DF. The frequency spectra determined in ScNA reflect that in SGNA.

Acknowledgments

We thank David Adams, MSEE, Christopher Corr, MS, and Nicole Courtney, AS, LAT, for their assistance.

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      Table 1 also presents racial diversity of the study population. Our previous study8 in canine models indicate that SNA has a regular background HF oscillation that could be overshadowed by LF and VLF oscillations, most of which are burst activities. Similar patterns were observed in the present study.

    Funding sources: This study was supported in part by National Institutes of Health grants TR002208-01, HL139829, and OT2OD028190; Charles Fisch Cardiovascular Research Award endowed by Dr Suzanne B. Knoebel of the Krannert Institute of Cardiology (to Drs Liu, Yuan, and Everett); a Medtronic-Zipes Chair of Indiana University; and the Burns & Allen Chair of Cardiology Research at the Cedars-Sinai Medical Center.

    Disclosures: Indiana University was awarded US patent no. 10,448,852 for inventing neuECG recording. Drs Peng-Sheng Chen and Shien-Fong Lin are co-inventors of that patent. The other authors report no conflicts of interest.

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