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Reactive oxygen species alters the electrophysiological properties and raises [Ca2+]i in intracardiac ganglion neurons

Journal Article


Abstract


  • We have investigated the effects of the reactive oxygen species (ROS) donors hydrogen peroxide (H2O2) and tert-butyl hydroperoxide (t-BHP) on the intrinsic electrophysiological characteristics: ganglionic transmission and resting [Ca2+]i in neonate and adult rat intracardiac ganglion (ICG) neurons. Intracellular recordings were made using sharp microelectrodes filled with either 0.5 M KCl or Oregon Green 488 BAPTA-1, allowing recording of electrical properties and measurement of [Ca2+]i. H2O2 and t-BHP both hyperpolarized the resting membrane potential and reduced membrane resistance. In adult ICG neurons, the hyperpolarizing action of H2O2 was reversed fully by Ba2+ and partially by tetraethylammonium, muscarine, and linopirdine. H2O2 and t-BHP reduced the action potential afterhyperpolarization (AHP) amplitude but had no impact on either overshoot or AHP duration. ROS donors evoked an increase in discharge adaptation to long depolarizing current pulses. H2O2 blocked ganglionic transmission in most ICG neurons but did not alter nicotine-evoked depolarizations. By contrast, t-BHP had no significant action on ganglionic transmission. H2O2 and t-BHP increased resting intracellular Ca2+ levels to 1.6 (�� 0.6, n = 11, P < 0.01) and 1.6 (�� 0.3, n = 8, P < 0.001), respectively, of control value (1.0, ���60 nM). The ROS scavenger catalase prevented the actions of H 2O2, and this protection extended beyond the period of application. Superoxide dismutase partially shielded against the action of H2O2, but this was limited to the period of application. These data demonstrate that ROS decreases the excitability and ganglionic transmission of ICG neurons, attenuating parasympathetic control of the heart. Copyright �� 2010 the American Physiological Society.

UOW Authors


  •   Harper, Alexander (external author)

Publication Date


  • 2010

Citation


  • Dyavanapalli, J., Rimmer, K., & Harper, A. A. (2010). Reactive oxygen species alters the electrophysiological properties and raises [Ca2+]i in intracardiac ganglion neurons. American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 299(1). doi:10.1152/ajpregu.00053.2010

Scopus Eid


  • 2-s2.0-77954397311

Volume


  • 299

Issue


  • 1

Place Of Publication


Abstract


  • We have investigated the effects of the reactive oxygen species (ROS) donors hydrogen peroxide (H2O2) and tert-butyl hydroperoxide (t-BHP) on the intrinsic electrophysiological characteristics: ganglionic transmission and resting [Ca2+]i in neonate and adult rat intracardiac ganglion (ICG) neurons. Intracellular recordings were made using sharp microelectrodes filled with either 0.5 M KCl or Oregon Green 488 BAPTA-1, allowing recording of electrical properties and measurement of [Ca2+]i. H2O2 and t-BHP both hyperpolarized the resting membrane potential and reduced membrane resistance. In adult ICG neurons, the hyperpolarizing action of H2O2 was reversed fully by Ba2+ and partially by tetraethylammonium, muscarine, and linopirdine. H2O2 and t-BHP reduced the action potential afterhyperpolarization (AHP) amplitude but had no impact on either overshoot or AHP duration. ROS donors evoked an increase in discharge adaptation to long depolarizing current pulses. H2O2 blocked ganglionic transmission in most ICG neurons but did not alter nicotine-evoked depolarizations. By contrast, t-BHP had no significant action on ganglionic transmission. H2O2 and t-BHP increased resting intracellular Ca2+ levels to 1.6 (�� 0.6, n = 11, P < 0.01) and 1.6 (�� 0.3, n = 8, P < 0.001), respectively, of control value (1.0, ���60 nM). The ROS scavenger catalase prevented the actions of H 2O2, and this protection extended beyond the period of application. Superoxide dismutase partially shielded against the action of H2O2, but this was limited to the period of application. These data demonstrate that ROS decreases the excitability and ganglionic transmission of ICG neurons, attenuating parasympathetic control of the heart. Copyright �� 2010 the American Physiological Society.

UOW Authors


  •   Harper, Alexander (external author)

Publication Date


  • 2010

Citation


  • Dyavanapalli, J., Rimmer, K., & Harper, A. A. (2010). Reactive oxygen species alters the electrophysiological properties and raises [Ca2+]i in intracardiac ganglion neurons. American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 299(1). doi:10.1152/ajpregu.00053.2010

Scopus Eid


  • 2-s2.0-77954397311

Volume


  • 299

Issue


  • 1

Place Of Publication