The vagus nerve mediates cardiorespiratory coupling that changes with metabolic demand in a temperate nototheniod fish

Abstract

The extent and efficiency of cardiorespiratory coupling (CRC) in teleost fishes is unclear. We simultaneously monitored heart rate (fH) and ventilation rate (fV) in Paranotothenia angustata, and applied modern power spectral analysis (PSA) mathematics to examine the rate association under varying levels of oxygen consumption (ṀO2). At low ṀO2 (0.94 mmol O2 kg-1 h-1) there was a correspondingly low fH and fV (25.5±2.4 min -1 and 29.2±2.6 min-1, respectively). Heart rate variability (HRV) consisted of oscillatory components caused by periodic vagal inhibition of the heart beat. Cross-spectral analysis showed that fH and fV were coupled, with the response lag in heart beat being approximately one seventh of each ventilation cycle. Ingestion of food elevated ṀO2 (1.99±0.02 mmol O2 kg-1 h -1) and increased both fH and fV (45±2.3 min-1 and 52±2 min-1, respectively, P<0.05), but CRC was maintained despite a reduction in HRV. The elevated stress caused by handling and placement of fish into respirometry chambers raised fH and fV to a similar rate as observed after feeding, although high-frequency (>0.2 Hz) oscillations in fH were lacking and ṀO2 was lower (1.82±0.03 mmol O2 kg -1 h-1, P<0.05). Subsequent cardiac vagotomy elevated fH and fV (55.5±0.8 min-1 and 48.2±0.7 min-1, respectively; P<0.05) but abolished all HRV and CRC, although ṀO2 was significantly less for a given f H and fV compared to intact fish. Thus, P. angustata exhibits vagally mediated CRC, and the association between fH and fV varies according to oxygen demand.