Analysis of passive and active electrophysiologic properties of neurons in mammalian nodose ganglia maintained in vitro.

Abstract

1. We studied the passive and active electrical properties of the soma membrane of neurons in nodose ganglia removed from cats and rabbits and maintained in vitro. The ganglia were superfused at 37 degrees C with a solution formulated to approximate the extracellular fluid of each species. The solution was buffered to pH 7.34, continuously equilibrated with 95% O2 and 5% CO2, and contained dialyzed calf serum and glucose. We also examined these properties in nodose ganglion neurons in vivo. Intracellular recordings were obtained with glass micropipettes filled with either 3 M KCl or 5 M K acetate. 2. We determined mean values for a variety of passive and active electrophysiologic properties. Values obtained in vitro did not differ significantly from those obtained in vivo. Based on the passive electrical properties of the soma membrane, neurons in the nodose ganglion appear to be a uniform population, despite the different sensory modalities conveyed by the afferent fibers. 3. Cell bodies of neurons generated action potentials in response to impulses in their afferent fibers. Somatic spikes could be evoked by stimulation of either the supranodose or infranodose vagus nerve, and an inflection point could be seen on their rising phase. When the vagus nerve was stimulated at frequencies greater than 10-20 Hz, the generation of somatic spikes often became progressively delayed and then failed completely, leaving a smaller potential (IS spike) which was apparently generated in the initial complex. The afterhyperpolarization was associated only with the somatic spike. 4. Many neurons, both in vitro and in vivo, developed a persistent hyperpolarization when repetitive action potentials occurred in the soma. This hyperpolarization was apparent at frequencies as low as 1-2 Hz, persisted for up to 5 s after the occurrence of the last somatic spike, and sometimes caused failure of somatic spikes to be generated. 5. Neurons in both species differed in their responses to suprathreshold depolarization applied through the recording electrode. Some neurons produced a train of action potentials which lasted for the duration of the depolarizing pulse, the frequency of the train being related to the magnitude of depolarization. The trains were characterized by gradually decreasing spike amplitudes and increasing interspike intervals. Other neurons responded with only a single spike or brief burst of action potentials at the beginning of depolarization to threshold. 6. It is suggested that the adaptive properties of the soma membrane of a peripheral sensory neuron are similar to those of its sensory ending, and that electrophysiological studies of the soma membrane may provide an opportunity to examine mechanisms of receptor adaptation.