An intracellular study of chemosensory fibers and endings

Abstract

1. The carotid body and its nerve, removed from anesthetized cats, were placed in physiological saline flowing under paraffin oil. The nerve, lifted into the oil, was used for either electrical stimulation or recording of the total afferent discharge. Intracellular recordings were obtained from individual nerve fibers and endings within the carotid body. The recording sites were identified by injecting Procion yellow through the intracellular electrodes; the tissues were then prepared for histology and observed with episcopic fluorescence or Nomarski optics. 2. Intracellularly recorded chemosensory fibers conducted at 1.1-30 m/s and usually displayed action potentials of regular amplitude. At times, however, some spikes become partially blocked while others maintained their original amplitude. "Natural" (hypoxia) or chemical (ACh or NaCN) stimulation induced different patterns of frequency changes of the large and small action potentials. This indicated nerve fiber branching at some distance from the recording site. 3. Intra- and extracellularly recorded spikes were blocked in 0 [Na+]0 by tetrodotoxin (TTX) or procaine. 4. During chemical stimulation, a slowly occurring depolarization (receptor or generator potential) was recorded intracellularly from the afferent fibers. It developed concomitantly with the increase in discharge. 5. Impalement of single nerve terminals (histologically identified) showed numerous "spontaneous" depolarizing potentials (SDPs) that had a mean amplitude of 5.6 mV, a mean duration of 46.1 ms, and nearly random distribution. They increased in frequency and summated during chemical stimulation. SDPs originated from either the site of recording or from neighboring areas. When the SDPs attained a certain amplitude, they seemed to give rise to action potentials. Also, relatively well developed or partially blocked spikes (apparently originating elsewhere) were recorded from single nerve terminals. 6. The receptor (generator) potential of chemosensory receptors appears to be an integrated response formed by multiple activity originating in different nerve endings.

Peripheral Chemoreceptors: Function and Plasticity of the Carotid Body

“…Not all evidence is so supportive for a presynaptic role for type I cells and Donnelly and coworkers (218, 222) consider the generation of postsynaptic action potentials to occur, not via the presumed summation of synaptic depolarizing potentials in the nerve terminal consequent to neurotransmitter release from type I cells (352, 951), but instead via the slow modulation of channel noise associated with a persistent sodium current (735) located in the nerve terminal. These authors cite the ultrastructural findings of Gronblad (323) and Verna (862) who examined stimulus-induced, exocytotic fusion profiles in type I cells and, independently, failed to observe such events occurring between the type I cell and nerve terminal.…”

The influence of chronic hypoxia upon chemoreception

“…Chemosensitivity in the afferent nerve endings is an attractive hypothesis that might explain experimental results such as the recovery of chemosensitivity in the carotid sinus nerve after removal of the carotid body (Mitchell et al, 1972), and the large variation in effects of a given neurotransmitter or neuromodulators on chemoreception between species (see below). This hypothesis deserves further study because it has been difficult to experimentally test given the challenges in making neural recordings from the fine nerve endings in the carotid body (Hayashida et al, 1980). However, at this time the mechanism is only hypothetical and any role for afferent nerve chemosensitivity in plasticity of carotid body function during chronic hypoxia remains hypothetical.…”

Dissociation of hypoxia‐induced chemosensory responses and catecholamine efflux in cat carotid body superfused in vitro.

“…In the cat carotid body, nerve endings present numerous and extended appositions with glomus cells, their membranes being separated by about 30 nm only (Hess, 1968). Each of these synapses may act as a generator for nerve impulses, which are conducted at 1-2-30 m s-' (Hayashida, Koyano & Eyzaguirre, 1980). Thus, chemosensory nerve activity recorded at the carotid nerve will be an almost instantaneous detector of transmitter release from glomus cells.…”