A novel metric linking stellate ganglion neuronal population dynamics to cardiopulmonary physiology

Am J Physiol Heart Circ Physiol. 2021 Aug 1;321(2):H369-H381. doi: 10.1152/ajpheart.00138.2021. Epub 2021 Jul 2.

Abstract

Cardiopulmonary sympathetic control is exerted via stellate ganglia (SG); however, little is known about how neuronal firing patterns in the stellate ganglion relate to dynamic physiological function in the heart and lungs. We performed continuous extracellular recordings from SG neurons using multielectrode arrays in chloralose-anesthetized pigs (n = 6) for 8-9 h. Respiratory and left ventricular pressures (RP and LVP, respectively) and the electrocardiogram (ECG) were recorded concomitantly. Linkages between sampled spikes and LVP or RP were determined using a novel metric to evaluate specificity in neural activity for phases of the cardiac and pulmonary cycles during resting conditions and under various cardiopulmonary stressors. Firing frequency (mean 4.6 ± 1.2 Hz) varied spatially across the stellate ganglion, suggesting regional processing. The firing pattern of most neurons was synchronized with both cardiac (LVP) and pulmonary (RP) activity indicative of cardiopulmonary integration. Using the novel metric to determine cardiac phase specificity of neuronal activity, we found that spike density was highest during diastole and near-peak systole. This specificity was independent of the actual LVP or population firing frequency as revealed by perturbations to the LVP. The observed specificity was weaker for RP. Stellate ganglion neuronal populations exhibit cardiopulmonary integration and profound specificity toward the near-peak systolic phase of the cardiac cycle. This novel approach provides practically deployable tools to probe stellate ganglion function and its relationship to cardiopulmonary pathophysiology.NEW & NOTEWORTHY Activity of stellate ganglion neurons is often linking indirectly to cardiac function. Using novel approaches coupled with extended period of recordings in large animals, we link neuronal population dynamics to mechanical events occurring at near-peak systole. This metric can be deployed to probe stellate ganglion neuronal control of cardiopulmonary function in normal and disease states.

Keywords: cardiopulmonary; hemodynamics; neural recordings; spike activity; stellate ganglion.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Aorta
  • Cardiac Pacing, Artificial
  • Electrocardiography
  • Heart / physiology*
  • Microelectrodes
  • Neurons / physiology*
  • Pressure*
  • Respiratory Function Tests
  • Respiratory Mechanics
  • Respiratory Physiological Phenomena*
  • Spatio-Temporal Analysis
  • Stellate Ganglion / cytology
  • Stellate Ganglion / physiology*
  • Stress, Physiological / physiology*
  • Sus scrofa
  • Swine
  • Sympathetic Nervous System / physiology
  • Vena Cava, Inferior
  • Ventricular Pressure / physiology*

Associated data

  • figshare/10.6084/m9.figshare.14347061.v2