Seasonal changes of cholinergic response in the atrium of Arctic navaga cod (Eleginus navaga)

Fishes of north-temperate latitudes exhibit marked seasonal changes in electrical excitability of the heart partly as an outcome of temperature-dependent changes in the density of major K⁺ ion currents: delayed rectifiers (I_Kr, I_Ks) and background inward rectifier (I_K1). In the arctic teleost, navaga cod (Eleginus navaga), I_Kr and I_K1 are strongly up-regulated in winter. The current study tests the hypothesis that the ligand-gated K⁺ current, the acetylcholine-activated inward rectifier, I_KACh, is also modified by seasonal acclimatization in atrial myocytes of navaga. In sinoatrial preparations of the summer-acclimatized (SA) navaga, 10^-6 M carbamylcholine chloride (CCh) caused slowing of heart rate, shortening of atrial action potential (AP) duration and a drastic reduction of AP amplitude, eventually resulting in inexcitability. In winter-acclimatized (WA) atria CCh slowed HR and reduced AP duration, but reduction of AP amplitude was modest and never resulted in inexcitability. The difference in cholinergic response between SA and WA navaga is explained by seasonal changes in I_KACh density. The peak density of I_KACh, induced by 10^-5 M CCh, at the common experimental temperature (+6 °C) was 0.97 ± 0.28 pA/pF in SA navaga but only 0.183 ± 0.013 pA/pF in WA navaga (a 5.3-fold difference, P < 0.05). At acclimatization temperatures of the fish I_KACh density was 2.8 ± 0.50 (at +12 °C) and 0.11 ± 0.06 pA/pF (at +3 °C) (a 26-fold difference, P < 0.05) for SA and WA navaga, respectively. Thus, acclimatization to summer induces a drastic up-regulation of the atrial I_KACh, which effectively shortens atrial AP. The reverse temperature compensation of the atrial I_KACh may be advantageous in summer under variable water temperatures and oxygen concentrations by reducing workload of the heart.