Abolition of reflex bradycardia by cardiac vagotomy has no effect on the regulation of oxygen uptake by Atlantic cod in progressive hypoxia

David McKenzie, Peter Vilhelm Skov, E.W.T. Taylor, Tobias Wang, John Fleng Steffensen

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

The functional significance of chemoreflexive hypoxic bradycardia was explored in Atlantic cod Gadus morhua L. (mean mass similar to 800 g, acclimated to a seawater temperature of 11 degrees C) by investigating responses to progressive hypoxia following section of the cardiac branches of cranial nerve X Cardiac denervation had no effect on oxygen uptake rate (M-O2), gill ventilation rate (f(G)) or opercular pressure amplitude (P-OP) under normoxic conditions, but caused a significant increase in heart rate (f(H)), to 50 +/- 1 beats min(-1) by comparison to 40 +/- 2 beats min(-1) in sham-operated cod (mean +/- s.e.m., n=9). Sham-operated cod exhibited transient profound bradycardia following oxygen chemoreceptor stimulation by bolus injection of sodium cyanide into the buccal cavity (2 mg in 2 ml seawater), but this cardiac chemoreflex was abolished in denervated cod. Both groups, however, exhibited similar marked transient chemoreflexive hyperventilation following NaCN. When exposed from normoxia (PO2 similar to 18 kPa) to progressive hypoxia at nominal water PO2'S of 8, 6, 5, 4 and 3 kPa, both groups exhibited the same pattern of homeostatic regulation of M-O2, with no significant difference in their mean critical PO2 (P-crit) values, which were 7.40 +/- 0.81 kPa and 8.73 +/- 0.71 kPa, respectively (n=9). Both groups exhibited significant bradycardia during progressive hypoxia, although denervated fish always had higher mean f(H). The incipient threshold for bradycardia coincided with P-crit in sham-operated cod whereas, in denervates, the threshold was below their P-crit and bradycardia presumably reflected direct effects of hypoxia on the myocardium. The sham-operated group displayed a significantly more pronounced ventilatory response than denervates in hypoxia, in particular for P-OP. In sham-operated cod, peak ventilatory responses occurred in deep hypoxia below P-crit whereas, in denervates, more modest peak responses coincided with Pit and, in deep hypoxia, they exhibited a significant decline in f(G) below their normoxic rate. Only a minority of shams lost equilibrium in hypoxia whereas a majority of denervates did, some of which failed to recover. The results indicate that chemoreflexive bradycardia plays no role in the homeostatic regulation of oxygen uptake by cod in hypoxia, but does contribute to maintenance of overall functional integrity below P-crit.
Original languageEnglish
JournalComparative Biochemistry and Physiology A
Volume153
Issue number3
Pages (from-to)332-338
ISSN1095-6433
DOIs
Publication statusPublished - 2009

Keywords

  • Sodium cyanide
  • Gas exchange
  • Ventilation
  • Hypoxia
  • Heart rate
  • Vagus
  • Fish
  • Cranial nerve X

Cite this

@article{c4d935cd1cf04b0888ed6ece69285424,
title = "Abolition of reflex bradycardia by cardiac vagotomy has no effect on the regulation of oxygen uptake by Atlantic cod in progressive hypoxia",
abstract = "The functional significance of chemoreflexive hypoxic bradycardia was explored in Atlantic cod Gadus morhua L. (mean mass similar to 800 g, acclimated to a seawater temperature of 11 degrees C) by investigating responses to progressive hypoxia following section of the cardiac branches of cranial nerve X Cardiac denervation had no effect on oxygen uptake rate (M-O2), gill ventilation rate (f(G)) or opercular pressure amplitude (P-OP) under normoxic conditions, but caused a significant increase in heart rate (f(H)), to 50 +/- 1 beats min(-1) by comparison to 40 +/- 2 beats min(-1) in sham-operated cod (mean +/- s.e.m., n=9). Sham-operated cod exhibited transient profound bradycardia following oxygen chemoreceptor stimulation by bolus injection of sodium cyanide into the buccal cavity (2 mg in 2 ml seawater), but this cardiac chemoreflex was abolished in denervated cod. Both groups, however, exhibited similar marked transient chemoreflexive hyperventilation following NaCN. When exposed from normoxia (PO2 similar to 18 kPa) to progressive hypoxia at nominal water PO2'S of 8, 6, 5, 4 and 3 kPa, both groups exhibited the same pattern of homeostatic regulation of M-O2, with no significant difference in their mean critical PO2 (P-crit) values, which were 7.40 +/- 0.81 kPa and 8.73 +/- 0.71 kPa, respectively (n=9). Both groups exhibited significant bradycardia during progressive hypoxia, although denervated fish always had higher mean f(H). The incipient threshold for bradycardia coincided with P-crit in sham-operated cod whereas, in denervates, the threshold was below their P-crit and bradycardia presumably reflected direct effects of hypoxia on the myocardium. The sham-operated group displayed a significantly more pronounced ventilatory response than denervates in hypoxia, in particular for P-OP. In sham-operated cod, peak ventilatory responses occurred in deep hypoxia below P-crit whereas, in denervates, more modest peak responses coincided with Pit and, in deep hypoxia, they exhibited a significant decline in f(G) below their normoxic rate. Only a minority of shams lost equilibrium in hypoxia whereas a majority of denervates did, some of which failed to recover. The results indicate that chemoreflexive bradycardia plays no role in the homeostatic regulation of oxygen uptake by cod in hypoxia, but does contribute to maintenance of overall functional integrity below P-crit.",
keywords = "Sodium cyanide, Gas exchange, Ventilation, Hypoxia, Heart rate, Vagus, Fish, Cranial nerve X",
author = "David McKenzie and Skov, {Peter Vilhelm} and E.W.T. Taylor and Tobias Wang and Steffensen, {John Fleng}",
year = "2009",
doi = "10.1016/j.cbpa.2009.03.009",
language = "English",
volume = "153",
pages = "332--338",
journal = "Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology",
issn = "1095-6433",
publisher = "Elsevier",
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}

Abolition of reflex bradycardia by cardiac vagotomy has no effect on the regulation of oxygen uptake by Atlantic cod in progressive hypoxia. / McKenzie, David; Skov, Peter Vilhelm; Taylor, E.W.T.; Wang, Tobias; Steffensen, John Fleng.

In: Comparative Biochemistry and Physiology A, Vol. 153, No. 3, 2009, p. 332-338.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Abolition of reflex bradycardia by cardiac vagotomy has no effect on the regulation of oxygen uptake by Atlantic cod in progressive hypoxia

AU - McKenzie, David

AU - Skov, Peter Vilhelm

AU - Taylor, E.W.T.

AU - Wang, Tobias

AU - Steffensen, John Fleng

PY - 2009

Y1 - 2009

N2 - The functional significance of chemoreflexive hypoxic bradycardia was explored in Atlantic cod Gadus morhua L. (mean mass similar to 800 g, acclimated to a seawater temperature of 11 degrees C) by investigating responses to progressive hypoxia following section of the cardiac branches of cranial nerve X Cardiac denervation had no effect on oxygen uptake rate (M-O2), gill ventilation rate (f(G)) or opercular pressure amplitude (P-OP) under normoxic conditions, but caused a significant increase in heart rate (f(H)), to 50 +/- 1 beats min(-1) by comparison to 40 +/- 2 beats min(-1) in sham-operated cod (mean +/- s.e.m., n=9). Sham-operated cod exhibited transient profound bradycardia following oxygen chemoreceptor stimulation by bolus injection of sodium cyanide into the buccal cavity (2 mg in 2 ml seawater), but this cardiac chemoreflex was abolished in denervated cod. Both groups, however, exhibited similar marked transient chemoreflexive hyperventilation following NaCN. When exposed from normoxia (PO2 similar to 18 kPa) to progressive hypoxia at nominal water PO2'S of 8, 6, 5, 4 and 3 kPa, both groups exhibited the same pattern of homeostatic regulation of M-O2, with no significant difference in their mean critical PO2 (P-crit) values, which were 7.40 +/- 0.81 kPa and 8.73 +/- 0.71 kPa, respectively (n=9). Both groups exhibited significant bradycardia during progressive hypoxia, although denervated fish always had higher mean f(H). The incipient threshold for bradycardia coincided with P-crit in sham-operated cod whereas, in denervates, the threshold was below their P-crit and bradycardia presumably reflected direct effects of hypoxia on the myocardium. The sham-operated group displayed a significantly more pronounced ventilatory response than denervates in hypoxia, in particular for P-OP. In sham-operated cod, peak ventilatory responses occurred in deep hypoxia below P-crit whereas, in denervates, more modest peak responses coincided with Pit and, in deep hypoxia, they exhibited a significant decline in f(G) below their normoxic rate. Only a minority of shams lost equilibrium in hypoxia whereas a majority of denervates did, some of which failed to recover. The results indicate that chemoreflexive bradycardia plays no role in the homeostatic regulation of oxygen uptake by cod in hypoxia, but does contribute to maintenance of overall functional integrity below P-crit.

AB - The functional significance of chemoreflexive hypoxic bradycardia was explored in Atlantic cod Gadus morhua L. (mean mass similar to 800 g, acclimated to a seawater temperature of 11 degrees C) by investigating responses to progressive hypoxia following section of the cardiac branches of cranial nerve X Cardiac denervation had no effect on oxygen uptake rate (M-O2), gill ventilation rate (f(G)) or opercular pressure amplitude (P-OP) under normoxic conditions, but caused a significant increase in heart rate (f(H)), to 50 +/- 1 beats min(-1) by comparison to 40 +/- 2 beats min(-1) in sham-operated cod (mean +/- s.e.m., n=9). Sham-operated cod exhibited transient profound bradycardia following oxygen chemoreceptor stimulation by bolus injection of sodium cyanide into the buccal cavity (2 mg in 2 ml seawater), but this cardiac chemoreflex was abolished in denervated cod. Both groups, however, exhibited similar marked transient chemoreflexive hyperventilation following NaCN. When exposed from normoxia (PO2 similar to 18 kPa) to progressive hypoxia at nominal water PO2'S of 8, 6, 5, 4 and 3 kPa, both groups exhibited the same pattern of homeostatic regulation of M-O2, with no significant difference in their mean critical PO2 (P-crit) values, which were 7.40 +/- 0.81 kPa and 8.73 +/- 0.71 kPa, respectively (n=9). Both groups exhibited significant bradycardia during progressive hypoxia, although denervated fish always had higher mean f(H). The incipient threshold for bradycardia coincided with P-crit in sham-operated cod whereas, in denervates, the threshold was below their P-crit and bradycardia presumably reflected direct effects of hypoxia on the myocardium. The sham-operated group displayed a significantly more pronounced ventilatory response than denervates in hypoxia, in particular for P-OP. In sham-operated cod, peak ventilatory responses occurred in deep hypoxia below P-crit whereas, in denervates, more modest peak responses coincided with Pit and, in deep hypoxia, they exhibited a significant decline in f(G) below their normoxic rate. Only a minority of shams lost equilibrium in hypoxia whereas a majority of denervates did, some of which failed to recover. The results indicate that chemoreflexive bradycardia plays no role in the homeostatic regulation of oxygen uptake by cod in hypoxia, but does contribute to maintenance of overall functional integrity below P-crit.

KW - Sodium cyanide

KW - Gas exchange

KW - Ventilation

KW - Hypoxia

KW - Heart rate

KW - Vagus

KW - Fish

KW - Cranial nerve X

U2 - 10.1016/j.cbpa.2009.03.009

DO - 10.1016/j.cbpa.2009.03.009

M3 - Journal article

VL - 153

SP - 332

EP - 338

JO - Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology

JF - Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology

SN - 1095-6433

IS - 3

ER -