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

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Abstract

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 (IKr, IKs) and background inward rectifier (IK1). In the arctic teleost, navaga cod (Eleginus navaga), IKr and IK1 are strongly up-regulated in winter. The current study tests the hypothesis that the ligand-gated K+ current, the acetylcholine-activated inward rectifier, IKACh, 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 IKACh density. The peak density of IKACh, 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 IKACh 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 IKACh, which effectively shortens atrial AP. The reverse temperature compensation of the atrial IKACh may be advantageous in summer under variable water temperatures and oxygen concentrations by reducing workload of the heart.

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Acknowledgments

Authors thank the director of the White Sea Biological Station Dr. Alexander B. Tzetlin for general support of this study. Authors are also grateful to Valo V. Sivonen, Valentina P. Sivonen, Alexander L. Gvozdev and Dr. Maxim L. Lovat for capturing the fish. The study was supported by the Russian Foundation for Basic Research [14-04-01564 to D.V.A.] and the grant from The Academy of Finland to MV (Project No. 14955).

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Authors and Affiliations

  1. Department of Human and Animal Physiology, Lomonosov Moscow State University, Leninskiye Gory, 1, 12, Moscow, Russia

    Denis V. Abramochkin

  2. Department of Physiology, Pirogov Russian National Research Medical University, Moscow, Russia

    Denis V. Abramochkin

  3. Department of Environmental and Biological Sciences, University of Eastern Finland, Joensuu, Finland

    Matti Vornanen

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  1. Denis V. Abramochkin
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Correspondence to Denis V. Abramochkin.

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All experiments conformed to the Guide for the Care and Use of Laboratory Animals published by the U.S. National Institutes of Health (NIH Publication No. 85–23, revised 1996)

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Communicated by H. V. Carey.

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Abramochkin, D.V., Vornanen, M. Seasonal changes of cholinergic response in the atrium of Arctic navaga cod (Eleginus navaga). J Comp Physiol B 187, 329–338 (2017). https://doi.org/10.1007/s00360-016-1032-y

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  • DOI: https://doi.org/10.1007/s00360-016-1032-y

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