The role of the paravertebral ganglia in human sympathetic neural discharge patterns

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

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Key Points: The mechanisms affecting recruitment patterns of postganglionic sympathetic nerves remain unclear. The divergent and convergent preganglionic innervation patterns of postganglionic neurons and the presence of differently sized postganglionic nerves suggest that the ganglia may participate in modifying the discharge patterns of single sympathetic postganglionic neurons innervating the skeletal muscle circulation. Whether the ganglia affect the ordered behaviour of varying sized postganglionic sympathetic neurons in humans has not been studied. Trimethaphan infusion produced an ordered pattern of action potential (AP) de-recruitment whereby the firing of larger, low probability APs present at baseline was abolished first, followed by progressive decreased probability of smaller APs. Although integrated sympathetic bursts were no longer detected after several minutes of trimethaphan, firing of the smallest APs was detected. These data suggest the ganglia affect the distribution of firing probabilities exhibited by differently sized sympathetic neurons. The ganglia may contribute to sympathetic neural emission patterns involved in homeostatic regulation. Abstract: Do the ganglia contribute to the ordered behaviour of postganglionic neuronal discharge within the sympathetic nervous system? To further understand the functional organization of the sympathetic nervous system we employed the microneurographic approach to record muscle sympathetic nerve activity (MSNA) and a continuous wavelet transform to study postganglionic action potential (AP) behaviour during nicotinic blockade at the ganglia (trimethaphan camsylate, 1–7 mg min−1) in seven females (37 ± 5 years). Trimethaphan elicited a progressive reduction in sympathetic outflow characterized by fewer integrated bursts with decaying amplitude. Underlying trimethaphan-mediated attenuations in integrated MSNA were reductions in AP incidence (186 ± 101 to 29 ± 31 AP (100 beats)−1) and AP content per integrated burst (7 ± 2 to 3 ± 1 APs burst−1) (both P < 0.01) in the final minute of detectable bursting activity in the trimethaphan condition, compared to baseline. We observed an ordered de-recruitment of larger to smaller AP clusters active at baseline (14 ± 3 to 8 ± 2 active AP clusters, P < 0.01). Following cessation of integrated bursts in the trimethaphan condition, the smallest 6 ± 2 sympathetic AP clusters persisted to fire in an asynchronous pattern (49 ± 41 AP (100 beats)−1) in all participants. Valsalva's manoeuvre did not increase the incidence of these persistent APs (60 ± 42 AP (100 beats)−1, P = 0.52), or recruit any larger APs in six of seven participants (6 ± 1 total AP clusters, P = 0.30). These data suggest that the ganglia participate in the ordered recruitment of differently sized postganglionic sympathetic nerves.

Original languageEnglish (US)
JournalJournal of Physiology
DOIs
StateAccepted/In press - Jan 1 2018

Fingerprint

Ganglia
Trimethaphan
Action Potentials
Neurons
Sympathetic Nervous System
Valsalva Maneuver
Wavelet Analysis
Muscles
Incidence
Skeletal Muscle

Keywords

  • Microneurography
  • Muscle Sympathetic Nerve Activity
  • Paravertebral Ganglia
  • Sympathetic Neural Recruitment
  • Trimethaphan

ASJC Scopus subject areas

  • Physiology

Cite this

The role of the paravertebral ganglia in human sympathetic neural discharge patterns. / Klassen, Stephen A.; Limberg, Jacqueline K.; Baker, Sarah E.; Nicholson, Wayne T.; Curry, Timothy B; Joyner, Michael Joseph; Shoemaker, J. Kevin.

In: Journal of Physiology, 01.01.2018.

Research output: Contribution to journalArticle

Klassen, Stephen A. ; Limberg, Jacqueline K. ; Baker, Sarah E. ; Nicholson, Wayne T. ; Curry, Timothy B ; Joyner, Michael Joseph ; Shoemaker, J. Kevin. / The role of the paravertebral ganglia in human sympathetic neural discharge patterns. In: Journal of Physiology. 2018.
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