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The action of high K+ and aglycaemia on the electrical properties and synaptic transmission in rat intracardiac ganglion neurones in vitro.

Dyavanapalli J, Rimmer K, Harper AA - Exp. Physiol. (2008)

Bottom Line: High K(+) had no impact on this behaviour but reduced the time-dependent rectification response to hyperpolarizing currents.However, the combination of aglycaemia and 20 mm K(+) displayed an improvement in passive properties and ganglionic transmission when compared with 20 mm K(+) PSS.These data indicate that the presynaptic terminal is the primary target of high extracellular potassium and that aglycaemia may have protective actions against this challenge.

View Article: PubMed Central - PubMed

Affiliation: College of Life Sciences, University of Dundee, UK.

ABSTRACT
We have investigated the action of two elements of acute ischaemia, high potassium and aglycaemia, on the electrophysiological properties and ganglionic transmission of adult rat intracardiac ganglion (ICG) neurones. We used a whole-mount ganglion preparation of the right atrial ganglion plexus and sharp microelectrode recording techniques. Increasing extracellular K(+) from its normal value of 4.7 mm to 10 mm decreased membrane potential and action potential after-hyperpolarization amplitude but otherwise had no effect on postganglionic membrane properties. It did, however, reduce the ability of synaptically evoked action potentials to follow high-frequency (100 Hz) repetitive stimulation. A further increase in K(+) changed both the passive and the active membrane properties of the postganglionic neurone: time constant, membrane resistance and action potential overshoot were all decreased in high K(+) (20 mm). The ICG neurones display a predominantly phasic discharge in response to prolonged depolarizing current pulses. High K(+) had no impact on this behaviour but reduced the time-dependent rectification response to hyperpolarizing currents. At 20 mm, K(+) practically blocked ganglionic transmission in most neurones at all frequencies tested. Aglycaemia, nominally glucose-free physiological saline solution (PSS), increased the time constant and membrane resistance of ICG neurones but otherwise had no action on their passive or active properties or ganglionic transmission. However, the combination of aglycaemia and 20 mm K(+) displayed an improvement in passive properties and ganglionic transmission when compared with 20 mm K(+) PSS. These data indicate that the presynaptic terminal is the primary target of high extracellular potassium and that aglycaemia may have protective actions against this challenge.

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The action of high [K+]o (20 mm) on somatic action potential characteristicsSomatic action potential traces produced by brief depolarizing current pulses from ICG neurones with short (A) and long AHP50 durations (B) in control and 20 mm K+ PSS. Top time calibration bar refers to A and bottom bar refers to B. C, AHP50 values in 4.7 and in 20 mm K+; data taken from Tables 1 and 3 (n= 14).
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fig03: The action of high [K+]o (20 mm) on somatic action potential characteristicsSomatic action potential traces produced by brief depolarizing current pulses from ICG neurones with short (A) and long AHP50 durations (B) in control and 20 mm K+ PSS. Top time calibration bar refers to A and bottom bar refers to B. C, AHP50 values in 4.7 and in 20 mm K+; data taken from Tables 1 and 3 (n= 14).

Mentions: Action potential parameters measured were its overshoot and the after-hyperpolarization (AHP) following the action potential, characterized by its amplitude and decay time. Adult ICG neurones had action potentials (APs) with large AHP amplitudes (17 ± 6 mV, n= 22) and a wide range of durations (9–62 ms), in good agreement with previous reports (Rimmer & Harper, 2006). The action of 20 mm K+ was dependent on AHP duration as gauged by time to 50% recovery (AHP50; Edwards et al. 1995); see Tables 1 and 3. The AHP50 values recorded in 4.7 and 20 mm K+ are plotted in Fig. 3C. High K+ had no apparent action on short AHP50 values but progressively increased the duration of longer AHP50 values. The overshoot and AHP amplitude decreased with increasing [K+]o; see Table 1 and Fig. 3. The increase in [K+]o was compensated for by a decrease in [Na+]o. The decrease in overshoot amplitude was, however, greater than can be accounted for by the expected shift in ENa (∼−3 mV for 20 mm K+ PSS), presumably reflecting increased Na+ channel inactivation accompanying membrane potential depolarization in this solution. The absolute amplitude of the AHP changed by ∼20 mV (from −63 to −45 mV in 4.7 and 20 mm K+ PSS, respectively) tracking the calculated decrease in EK (∼38 mV). This action was similar in neurones displaying either long or short AHP50 values; see Fig. 3. Apart from a rare brief burst of action potentials in response to switching to high-K+ PSS, there was no evidence of any progressive change in AP parameters over the exposure time. The evoked responses to long depolarizing pulses were unaffected by high-K+ solutions, remaining predominantly phasic; see Fig. 2.


The action of high K+ and aglycaemia on the electrical properties and synaptic transmission in rat intracardiac ganglion neurones in vitro.

Dyavanapalli J, Rimmer K, Harper AA - Exp. Physiol. (2008)

The action of high [K+]o (20 mm) on somatic action potential characteristicsSomatic action potential traces produced by brief depolarizing current pulses from ICG neurones with short (A) and long AHP50 durations (B) in control and 20 mm K+ PSS. Top time calibration bar refers to A and bottom bar refers to B. C, AHP50 values in 4.7 and in 20 mm K+; data taken from Tables 1 and 3 (n= 14).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2713859&req=5

fig03: The action of high [K+]o (20 mm) on somatic action potential characteristicsSomatic action potential traces produced by brief depolarizing current pulses from ICG neurones with short (A) and long AHP50 durations (B) in control and 20 mm K+ PSS. Top time calibration bar refers to A and bottom bar refers to B. C, AHP50 values in 4.7 and in 20 mm K+; data taken from Tables 1 and 3 (n= 14).
Mentions: Action potential parameters measured were its overshoot and the after-hyperpolarization (AHP) following the action potential, characterized by its amplitude and decay time. Adult ICG neurones had action potentials (APs) with large AHP amplitudes (17 ± 6 mV, n= 22) and a wide range of durations (9–62 ms), in good agreement with previous reports (Rimmer & Harper, 2006). The action of 20 mm K+ was dependent on AHP duration as gauged by time to 50% recovery (AHP50; Edwards et al. 1995); see Tables 1 and 3. The AHP50 values recorded in 4.7 and 20 mm K+ are plotted in Fig. 3C. High K+ had no apparent action on short AHP50 values but progressively increased the duration of longer AHP50 values. The overshoot and AHP amplitude decreased with increasing [K+]o; see Table 1 and Fig. 3. The increase in [K+]o was compensated for by a decrease in [Na+]o. The decrease in overshoot amplitude was, however, greater than can be accounted for by the expected shift in ENa (∼−3 mV for 20 mm K+ PSS), presumably reflecting increased Na+ channel inactivation accompanying membrane potential depolarization in this solution. The absolute amplitude of the AHP changed by ∼20 mV (from −63 to −45 mV in 4.7 and 20 mm K+ PSS, respectively) tracking the calculated decrease in EK (∼38 mV). This action was similar in neurones displaying either long or short AHP50 values; see Fig. 3. Apart from a rare brief burst of action potentials in response to switching to high-K+ PSS, there was no evidence of any progressive change in AP parameters over the exposure time. The evoked responses to long depolarizing pulses were unaffected by high-K+ solutions, remaining predominantly phasic; see Fig. 2.

Bottom Line: High K(+) had no impact on this behaviour but reduced the time-dependent rectification response to hyperpolarizing currents.However, the combination of aglycaemia and 20 mm K(+) displayed an improvement in passive properties and ganglionic transmission when compared with 20 mm K(+) PSS.These data indicate that the presynaptic terminal is the primary target of high extracellular potassium and that aglycaemia may have protective actions against this challenge.

View Article: PubMed Central - PubMed

Affiliation: College of Life Sciences, University of Dundee, UK.

ABSTRACT
We have investigated the action of two elements of acute ischaemia, high potassium and aglycaemia, on the electrophysiological properties and ganglionic transmission of adult rat intracardiac ganglion (ICG) neurones. We used a whole-mount ganglion preparation of the right atrial ganglion plexus and sharp microelectrode recording techniques. Increasing extracellular K(+) from its normal value of 4.7 mm to 10 mm decreased membrane potential and action potential after-hyperpolarization amplitude but otherwise had no effect on postganglionic membrane properties. It did, however, reduce the ability of synaptically evoked action potentials to follow high-frequency (100 Hz) repetitive stimulation. A further increase in K(+) changed both the passive and the active membrane properties of the postganglionic neurone: time constant, membrane resistance and action potential overshoot were all decreased in high K(+) (20 mm). The ICG neurones display a predominantly phasic discharge in response to prolonged depolarizing current pulses. High K(+) had no impact on this behaviour but reduced the time-dependent rectification response to hyperpolarizing currents. At 20 mm, K(+) practically blocked ganglionic transmission in most neurones at all frequencies tested. Aglycaemia, nominally glucose-free physiological saline solution (PSS), increased the time constant and membrane resistance of ICG neurones but otherwise had no action on their passive or active properties or ganglionic transmission. However, the combination of aglycaemia and 20 mm K(+) displayed an improvement in passive properties and ganglionic transmission when compared with 20 mm K(+) PSS. These data indicate that the presynaptic terminal is the primary target of high extracellular potassium and that aglycaemia may have protective actions against this challenge.

Show MeSH
Related in: MedlinePlus