Asynchronous action potential discharge in human muscle sympathetic nerve activity

Stephen A. Klassen, M. Erin Moir, Jacqueline K. Limberg, Sarah E. Baker, Wayne T. Nicholson, Timothy B. Curry, Michael J. Joyner, J. Kevin Shoemaker

Research output: Contribution to journalArticle

Abstract

What strategies are employed by the sympathetic system to communicate with the circulation? Muscle sympathetic nerve activity (MSNA) occurs in bursts of synchronous action potential (AP) discharge, yet whether between-burst asynchronous AP firing exists remains unknown. Using multiunit microneurography and a continuous wavelet transform to isolate APs, we studied AP synchronicity within human MSNA. Asynchronous APs were defined as those which occurred between bursts. Experiment 1 quantified AP synchronicity in eight individuals at baseline (BSL), -10 mmHg lower body negative pressure (LBNP), -40 mmHg LBNP, and end-expiratory apnea (APN). At BSL, 33 ± 12% of total AP activity was asynchronous. Asynchronous discharge was unchanged from BSL (67 ± 37 AP/min) to -10 mmHg LBNP (69 ± 33 AP/min), -40 mmHg LBNP (83 ± 68 AP/min), or APN (62 ± 39 AP/min). Across all conditions, asynchronous AP probability and frequency decreased with increasing AP size. Experiment 2 examined the impact of the ganglia on AP synchronicity by using nicotinic blockade (trimethaphan). The largest asynchronous APs were derecruited from BSL (11 ± 4 asynchronous AP clusters) to the last minute of the trimethaphan infusion with visible bursts (7 ± 2 asynchronous AP clusters). However, the 6 ± 2 smallest asynchronous AP clusters could not be blocked by trimethaphan and persisted to fire 100 ± 0% asynchronously without forming bursts. Nonnicotinic ganglionic mechanisms affect some, but not all, asynchronous activity. The fundamental behavior of human MSNA contains between-burst asynchronous AP discharge, which accounts for a considerable amount of BSL activity.NEW & NOTEWORTHY Historically, sympathetic nerve activity destined for the blood vessels supplying skeletal muscle (MSNA) has been characterized by spontaneous bursts formed by synchronous action potential (AP) discharge. However, this study found a considerable amount (~30% during baseline) of sympathetic AP discharge to fire asynchronously between bursts of human MSNA. Trimethaphan infusion revealed that nonnicotinic ganglionic mechanisms contribute to some, but not all, asynchronous discharge. Asynchronous sympathetic AP discharge represents a fundamental behavior of MSNA.

Original languageEnglish (US)
Pages (from-to)H754-H764
JournalAmerican journal of physiology. Heart and circulatory physiology
Volume317
Issue number4
DOIs
StatePublished - Oct 1 2019

Fingerprint

Action Potentials
Muscles
Trimethaphan
Lower Body Negative Pressure
Apnea
Wavelet Analysis
Ganglia
Blood Vessels

Keywords

  • action potential
  • asynchronous discharge
  • microneurography
  • muscle sympathetic nerve activity
  • paravertebral ganglia
  • sympathetic nervous system
  • sympathetic neural recruitment

ASJC Scopus subject areas

  • Physiology
  • Cardiology and Cardiovascular Medicine
  • Physiology (medical)

Cite this

Asynchronous action potential discharge in human muscle sympathetic nerve activity. / Klassen, Stephen A.; Moir, M. Erin; Limberg, Jacqueline K.; Baker, Sarah E.; Nicholson, Wayne T.; Curry, Timothy B.; Joyner, Michael J.; Shoemaker, J. Kevin.

In: American journal of physiology. Heart and circulatory physiology, Vol. 317, No. 4, 01.10.2019, p. H754-H764.

Research output: Contribution to journalArticle

Klassen, Stephen A. ; Moir, M. Erin ; Limberg, Jacqueline K. ; Baker, Sarah E. ; Nicholson, Wayne T. ; Curry, Timothy B. ; Joyner, Michael J. ; Shoemaker, J. Kevin. / Asynchronous action potential discharge in human muscle sympathetic nerve activity. In: American journal of physiology. Heart and circulatory physiology. 2019 ; Vol. 317, No. 4. pp. H754-H764.
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