Effects of aerobic and anaerobic metabolic inhibitors on avian intrapulmonary chemoreceptors

Jason Q. Pilarski, Irene C. Solomon, Delbert L. Kilgore, Steven C. Hempleman

Research output: Contribution to journalArticle

2 Scopus citations

Abstract

Birds have rapidly responding respiratory chemoreceptors [intrapulmonary chemoreceptors (IPC)] that provide vagal sensory feedback about breathing pattern. IPC are exquisitely sensitive to CO2 but are unaffected by hypoxia. IPC continue to respond to CO2 during hypoxic and even anoxic conditions, suggesting that they may generate ATP needed for signal transduction anaerobically. To assess IPC energy metabolism, single-cell action potential discharge and acid-base status were recorded from 26 pentobarbital-anesthetized Anas platyrhynchos before and after intravenous infusion of the glycolytic blocker iodoacetate (10-70 mg/kg), mitochondrial blocker rotenone (2 mg/kg), and/or mitochondrial uncoupler 2,4-dinitrophenol (5-15 mg/kg). After 5 min exposure at the highest dosages, iodoacetate inhibited IPC discharge 65% (15.9 ± 0.3 s-1 to 5.5 ± 0.3 s -1, P < 0.05), rotenone inhibited discharge 80% (12.9 ± 0.5 s-1 to 2.6 ± 0.6 s-1, P < 0.05), and 2,4-dinitrophenol inhibited discharge 19% (14.0 ± 0.3 s-1 to 11.3 ± 0.3 s-1, P < 0.05). These results suggest that IPC utilize glucose, require an intact glycolytic pathway, and metabolize the products of glycolysis to CO2 and H2O by mitochondrial respiration. The small but significant effect of 2,4-dinitrophenol suggests that ATP production by glycolysis may be sufficient to meet IPC energy demands if NADH can be oxidized to NAD experimentally by uncoupling mitochondria, or physiologically by transient lactate production. A model for IPC spike frequency adaptation is proposed, whereby the rapid onset of phasic IPC discharge requires ATP from anaerobic glycolysis, using lactate as the electron acceptor, and the roll-off in IPC discharge reflects transient acidosis due to intracellular lactic acid accumulation.

Original languageEnglish (US)
Pages (from-to)R1576-R1584
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume296
Issue number5
DOIs
StatePublished - May 1 2009

Keywords

  • ATP
  • Action potential
  • Anas platyrhynchos
  • Energy
  • Glycolysis
  • Ionic homeostasis
  • NAD
  • Oxidative phosphorylation
  • Respiration
  • Spike frequency adaptation

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

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