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

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.

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

“…Somatic action potential (AP) parameters measured were overshoot (OS), rate of rise (drise/d t ), rate of fall (dfall/d t ) and the AHP following the action potential, characterized by its depth below resting E m (AHP) and time to 50% recovery AHP 50 ( 15 ). Adult ICG neurons had APs with large AHP amplitudes (18.5 ± 6.1 mV, n = 40) and a wide range of AHP 50 durations (7.5–50.5 ms), in accordance with previously reported values ( 13 , 38 ). Application of H 2 O 2 reduced the AHP in adult and neonatal ICG neurons.…”

“…Resting [Ca 2+ ] i was estimated to be 62 ± 24.3 nM, n = 30 ( 12 ), which is in agreement with the sparse data available on [Ca 2+ ] i in dissociated autonomic ganglion neurons ( 4 , 53 ).…”

“…Akin to its guarding against the action of H 2 O 2 on the electrical properties of ICG neurons, the protective effect of catalase outlived the timeframe of its application, see Supplemental Table 2 and Figure 7B. Resting [Ca 2+ ] i was estimated to be 62 ± 24.3 nM, n=30 (12) agreeing with the sparse data available on [Ca 2+ ] i in dissociated autonomic ganglion neurons (4, 53).…”

“…All ICG neurons included in this study received a strong synaptic input, i.e., they received a suprathreshold EPSP, which evoked an action potential in response to each supramaximal stimulus applied to the preganglionic nerve trunk at 0.2 Hz ( 13 ). Ganglionic transmission was investigated both for low-frequency stimuli (0.2 and 0.5 Hz) and multiple trains of stimuli applied at 5–100 Hz.…”

“…Investigation of ganglionic transmission in the present study was limited to those postganglionic neurons receiving a secure, suprathreshold, input from the vagus, presumed to form efferent outflow ( 13 ). These neurons would be classified as principal cardiac neurons according to the cellular morphological scheme of Cheng and Powley ( 8 ).…”