Metrics of high cofluctuation and entropy to describe control of cardiac function in the stellate ganglion

  1. Nil Z Gurel  Is a corresponding author
  2. Koustubh B Sudarshan
  3. Joseph Hadaya
  4. Alex Karavos
  5. Taro Temma
  6. Yuichi Hori
  7. J Andrew Armour
  8. Guy Kember
  9. Olujimi A Ajijola
  1. University of California, Los Angeles, United States
  2. Dalhousie University, Canada

Abstract

Stellate ganglia within the intrathoracic cardiac control system receive and integrate central, peripheral, and cardiopulmonary information to produce postganglionic cardiac sympathetic inputs. Pathological anatomical and structural remodeling occurs within the neurons of the stellate ganglion (SG) in the setting of heart failure. A large proportion of SG neurons function as interneurons whose networking capabilities are largely unknown. Current therapies are limited to targeting sympathetic activity at the cardiac level or surgical interventions such as stellectomy, to treat heart failure. Future therapies that target the stellate ganglion will require understanding of their networking capabilities to modify any pathological remodeling. We observe SG networking by examining cofluctuation and specificity of SG networked activity to cardiac cycle phases. We investigate network processing of cardiopulmonary transduction by SG neuronal populations in porcine with chronic pacing-induced heart failure and control subjects during extended in-vivo extracellular microelectrode recordings. We find that information processing and cardiac control in chronic heart failure by the SG, relative to controls, exhibits: i) more frequent, short-lived, high magnitude cofluctuations, ii) greater variation in neural specificity to cardiac cycles, and iii) neural network activity and cardiac control linkage that depends on disease state and cofluctuation magnitude.

Data availability

Data is available in the Dryad repositoryCode AvailabilitySupporting Apache License codes are at GitHub (https://github.com/Koustubh2111/Cofluctuation-and-Entropy-Code-Data).

The following data sets were generated

Article and author information

Author details

  1. Nil Z Gurel

    UCLA Cardiac Arrhythmia Center, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    gurelnil@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3702-0449
  2. Koustubh B Sudarshan

    Department of Engineering Mathematics and Internetworking, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Joseph Hadaya

    UCLA Cardiac Arrhythmia Center, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Alex Karavos

    Department of Engineering Mathematics and Internetworking, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Taro Temma

    UCLA Cardiac Arrhythmia Center, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Yuichi Hori

    UCLA Cardiac Arrhythmia Center, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. J Andrew Armour

    UCLA Cardiac Arrhythmia Center, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Guy Kember

    Department of Engineering Mathematics and Internetworking, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  9. Olujimi A Ajijola

    UCLA Cardiac Arrhythmia Center, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6197-7593

Funding

National Institutes of Health (DP2 OD024323-01)

  • Olujimi A Ajijola

NHLBI Division of Intramural Research (R01 HL159001)

  • Olujimi A Ajijola

National Science Foundation (ASEE 2127509)

  • Nil Z Gurel

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Mone Zaidi, Icahn School of Medicine at Mount Sinai, United States

Ethics

Animal experimentation: The study was performed under a protocol approved by the University of California Los Angeles (UCLA) Animal Research Committee (ARC), in compliance with the UCLA Institutional Animal Care and Use Committee (IACUC) guidelines and the National Institutes of Health (NIH) Guide for the Care and Use of Laboratory Animals (Protocol #: ARC 2015-022). For SG neural data collection, the animals were sedated with tiletamine and zolazepam (Telazol, 4-8mg/kg) intramuscularly, intubated, and maintained under general anesthesia with inhaled isoflurane (2%). Continuous intravenous saline (8 − 10𝑚𝑙∕𝑘𝑔∕h) was infused throughout the protocol and animals were temperature maintained using heated water blankets (37𝑜𝐶 − 38𝑜𝐶).At the end of the protocol, animals were euthanized under deep sedation of isoflurane and cardiac fibrillation was induced.

Version history

  1. Preprint posted: September 30, 2021 (view preprint)
  2. Received: March 10, 2022
  3. Accepted: November 25, 2022
  4. Accepted Manuscript published: November 25, 2022 (version 1)
  5. Version of Record published: January 4, 2023 (version 2)

Copyright

© 2022, Gurel et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Nil Z Gurel
  2. Koustubh B Sudarshan
  3. Joseph Hadaya
  4. Alex Karavos
  5. Taro Temma
  6. Yuichi Hori
  7. J Andrew Armour
  8. Guy Kember
  9. Olujimi A Ajijola
(2022)
Metrics of high cofluctuation and entropy to describe control of cardiac function in the stellate ganglion
eLife 11:e78520.
https://doi.org/10.7554/eLife.78520

Share this article

https://doi.org/10.7554/eLife.78520

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