Does the ventricle limit cardiac contraction rate in the anoxic turtle (Trachemys scripta)? I. Comparison of the intrinsic contractile responses of cardiac chambers to the extracellular changes that accompany prolonged anoxia exposure

Abstract

Multiple lines of evidence suggest that an inability of the ventricle to contract in coordination with the pacemaker during anoxia exposure may suppress cardiac pumping rate in anoxia-tolerant turtles. To determine under what extracellular conditions the ventricle could be the weak link that limits cardiac pumping, we compared, under various extracellular conditions, the intrinsic contractile properties of isometrically-contracting ventricular and atrial strips obtained from 21 °C- to 5 °C- acclimated turtles (Trachemys scripta) that had been exposed to either normoxia or anoxia (16 h at 21 °C; 12 days at 5 °C). We found that combined extracellular anoxia, acidosis, and hyperkalemia (AAK), severely disrupted ventricular, but not right or left atrial, excitability and contractibility of 5 °C anoxic turtles. However, combined hypercalcemia and heightened adrenergic stimulation counteracted the negative effects of AAK. We also report that the turtle heart is resilient to prolonged diastolic intervals, which would ensure that contractile force is maintained if arrhythmia were to occur during anoxia exposure. Finally, our findings reinforce that prior temperature and anoxia experiences are central to the intrinsic contractile response of the turtle myocardium to altered extracellular conditions. At 21 °C, prior anoxia exposure preconditioned the ventricle for anoxic and acidosis exposure. At 5 °C, prior anoxia exposure evoked heightened sensitivity of the ventricle to hyperkalemia, as well as all chambers to combined hypercalcemia and increased adrenergic stimulation. Overall, our findings show that the ventricle could limit cardiac pumping rate during prolonged anoxic submergence in cold-acclimated turtles if hypercalcemia and heightened adrenergic stimulation are insufficient to counteract the negative effects of combined extracellular anoxia, acidosis, and hyperkalemia.