Review
An overview of the phylogeny of cardiorespiratory control in vertebrates with some reflections on the ‘Polyvagal Theory’

https://doi.org/10.1016/j.biopsycho.2022.108382Get rights and content
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Highlights

  • The efferent cardiac vagus in vertebrates shows rapid conduction rates, via MEF.

  • Phasic, respiration-related activity in the PNS generates CRI within HRV in all vertebrates.

  • CRI vary between vertebrates, from CRS in fish to RSA in mammals.

  • All air-breathing vertebrates, from lungfish to mammals, show RSA-like CRI.

  • RSA in mammals may be a relic of its ancestral role in controlling lung perfusion.

Abstract

Mammals show clear changes in heart rate linked to lung ventilation, characterized as respiratory sinus arrhythmia (RSA). These changes are controlled in part by variations in the level of inhibitory control exerted on the heart by the parasympathetic arm of the autonomic nervous system (PNS). This originates from preganglionic neurons in the nucleus ambiguous that supply phasic, respiration-related activity to the cardiac branch of the vagus nerve, via myelinated, efferent fibres with rapid conduction velocities. An elaboration of these central mechanisms, under the control of a ‘vagal system’ has been endowed by psychologists with multiple functions concerned with ‘social engagement’ in mammals and, in particular, humans. Long-term study of cardiorespiratory interactions (CRI) in other major groups of vertebrates has established that they all show both tonic and phasic control of heart rate, imposed by the PNS. This derives centrally from neurones located in variously distributed nuclei, supplying the heart via fast-conducting, myelinated, efferent fibres. Water-breathing vertebrates, which include fishes and larval amphibians, typically show direct, 1:1 CRI between heart beats and gill ventilation, controlled from the dorsal vagal motor nucleus. In air-breathing, ectothermic vertebrates, including reptiles, amphibians and lungfish, CRI mirroring RSA have been shown to improve oxygen uptake during phasic ventilation by changes in perfusion of their respiratory organs, due to shunting of blood over across their undivided hearts. This system may constitute the evolutionary basis of that generating RSA in mammals, which now lacks a major physiological role in respiratory gas exchange, due to their completely divided systemic and pulmonary circulations.

Abbreviations

AB
air-breathing
ABO
air-breathing organs
ANS
autonomic nervous system
CRI
cardio-respiratory interactions
CRS
cardiorespiratory synchrony
CVPN
cardiac vagal preganglionic neurons
DMNX
dorso-medial vagal motor nucleus (as used in PVT)
DVN
dorso-medial vagal motor nucleus (presently accepted acronym)
HR
heart rate
HF
high frequency
HRV
heart rate variability
LF
low frequency
NA
nucleus ambiguous
PVT
The Polyvagal Theory
R-L shunt
Right to Left intracardiac shunt
RSA
respiratory sinus arrhythmia
VPN
vagal preganglionic motoneurons
PNS
Parasympathetic nervous system
MEF
Myelinated efferent fibres

Keywords

Autonomic nervous system
Parasympathetic
Vagus nerve
Heart rate variability
Cardiorespiratory interactions
Respiratory sinus arrhythmia

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