Electrophysiological properties and chemosensitivity of guinea pig nodose ganglion neurons in vitro

Bradley J. Undem, Daniel Weinreich

Research output: Contribution to journalArticlepeer-review

Abstract

Conventional intracellular recording techniques were employed to obtain information on the electrophysiological and pharmacological characteristics of C-type neurons in the guinea pig nodose ganglia. Approximately 90% of the cell bodies gave rise to axons with conduction velocities consistent with C-fibers (0.9-1.1 m/s). The average resting membrane potential and input impedence was about -60 mV and 45 Mω, respectively. Orthodromic electrical stimulation of the vagus nerve 20-30 mm caudal to the ganglion produced overshooting action potentials in the nodose neurons. The falling phase of the action potential was followed by a transient (50-300 ms) fast hyperpolarization (AHPfast). In 20% of C-type neurons the AHPfast was followed by a slowly developing, long-lasting afterhyperpolarization (AHPslow) that limited the ability of the neuron to fire action potentials at high frequency. The AHPslow magnitude was dependent on the number of spikes, had a reversal potential of -87 mV, and was abolished by 100 μM cadmium chloride, suggesting that it is produced by a calcium-dependent potassium current. In about 30% of the nodose neurons, hyperpolarizing current steps from resting potential produced a time- and voltage-dependent anomalous rectification in the electrotonic potential. External cesium (1 mM), but not barium (100 μM) reversibly blocked this effect. Single-electrode voltage-clamp measurements revealed a slowly developing inward current in these neurons that grows in magnitude with step hyperpolarizations from resting potential, and has an estimated reversal potential of about -44 mV. These properties suggest that this current is analogous to Ih observed in many peripheral and central neurons. Autacoids including serotonin, histamine, several prostanoids, peptidoleukotriene, and bradykinin, were examined for their ability to affect the excitability of the nodose neurons. Serotonin was the only autacoid capable of depolarizing the membrane potential to action potential firing threshold. The serotonin-induced membrane depolarization was associated with a significant increase in input conductance. Histamine depolarized the membrane potential of the C-type neurons in 28/30 neurons. Bradykinin, prostacyclin, and leukotriene C4 were found to cause membrane depolarizations in a subset (73%, 31%, and 50%, respectively) of nodose neurons. The AHPslow was virtually abolished by bradykinin, prostacylin, and in a subset of neurons, leukotriene C4. Inhibition of the AHPslow was accompanied by a change in the accommodative properties of the neurons, reflected by the increased frequency at which the neuron could successfully elicit repetitive action potentials. The results demonstrate that most autacoids do not overtly evoke action potentials in the somata of the guinea pig nodose ganglion C-type neurons, rather they influence their excitability by producing subthreshold membrane depolarizations and by modulating the rate of neuronal discharge.

Original languageEnglish (US)
Pages (from-to)17-33
Number of pages17
JournalJournal of the Autonomic Nervous System
Volume44
Issue number1
DOIs
StatePublished - Jul 1993

Keywords

  • Autacoid
  • C-fiber
  • Nodose ganglion
  • Sensory neuron
  • Vagal afferent
  • Visceral afferent

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology
  • Clinical Neurology

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