Effects of hypoxic acclimation, muscle strain, and contraction frequency on nitric oxide-mediated myocardial performance in steelhead trout (Oncorhynchus mykiss).

Whether hypoxic acclimation influences nitric oxide (NO)-mediated control of fish cardiac function is not known. Thus, we measured the function/performance of myocardial strips from normoxic- and hypoxic-acclimated (40% air saturation; ∼8 kPa O2) trout at several frequencies (20-80 contractions·min-1) and two muscle strain amplitudes (8% and 14%) when exposed to increasing concentrations of the NO donor sodium nitroprusside (SNP) (10-9 to 10-4 M). Further, we examined the influence of 1) nitric oxide synthase (NOS) produced NO [by blocking NOS with 10-4 M NG-monomethyl-l-arginine (l-NMMA)] and 2) soluble guanylyl cyclase mediated, NOS-independent, NO effects (i.e., after blockade with 10-4 M ODQ), on myocardial contractility. Hypoxic acclimation increased twitch duration by 8%-10% and decreased mass-specific net power by ∼35%. However, hypoxic acclimation only had minor impacts on the effects of SNP and the two blockers on myocardial function. The most surprising finding of the current study was the degree to which contraction frequency and strain amplitude influenced NO-mediated effects on myocardial power. For example, at 8% strain, 10-4 SNP resulted in a decrease in net power of ∼30% at 20 min-1 but an increase of ∼20% at 80 min-1, and this effect was magnified at 14% strain. This research suggests that hypoxic acclimation has only minor effects on NO-mediated myocardial contractility in salmonids, is the first to report the high frequency- and strain-dependent nature of NO effects on myocardial contractility in fishes, and supports previous work showing that NO effects on the heart (myocardium) are finely tuned spatiotemporally.

Effects of hypoxic acclimation on contractile properties of the spongy and compact ventricular myocardium of steelhead trout (Oncorhynchus mykiss).

The trout ventricle has an outer compact layer supplied with well-oxygenated arterial blood from the coronary circulation, and an inner spongy myocardium supplied with oxygen poor venous blood. It was hypothesized that: (1) the spongy myocardium of steelhead trout (Oncorhynchus mykiss), given its routine exposure to low partial pressures of oxygen (PO2), would be better able to maintain contractile performance (work) when exposed to acute hypoxia (100 to 10% air saturation) relative to the compact myocardium, and would show little benefit from hypoxic acclimation; and (2) the compact myocardium from hypoxia-acclimated (40% air saturation) fish would be better able to maintain work during acute exposure to hypoxia relative to normoxia-acclimated individuals. Consistent with our expectations, when PO2 was acutely lowered, net work from the compact myocardium of normoxia-acclimated fish declined more (by ~ 73%) than the spongy myocardium (~ 50%), and more than the compact myocardium of hypoxia-acclimated fish (~ 55%), and hypoxic acclimation did not benefit the spongy myocardium in the face of reduced PO2. Further, while hypoxic acclimation resulted in a 25% (but not significant) decrease in net work of the spongy myocardium, the performance of the compact myocardium almost doubled. This research suggests that, in contrast to the spongy myocardium, performance of the compact myocardium is improved by hypoxic acclimation; and supports previous research suggesting that the decreased contractile performance of the myocardium upon exposure to lowered PO2 may be adaptive and mediated by mechanisms within the muscle itself.