Anatomical characteristics of tonic and phasic postganglionic neurons in guinea pig bronchial parasympathetic ganglia

Abstract

Anatomical characteristics of principal parasympathetic ganglia neurons on the guinea pig primary bronchus were analyzed, and the procedure for localizing the ganglia without the aid of staining for in vitro physiological studies is described. The neurons were tightly packed within a perineural sheath, and the cell bodies formed a homogeneous population based on size and shape. By using intracellular electrophysiological recordings, unstained neurons within these ganglia were characterized with suprathreshold depolarizing stimuli as having either accommodating action potential patterns (phasic neurons) or repetitive action potential patterns (tonic neurons). After determining whether a cell was tonic or phasic, it was injected with either horseradish peroxidase or Neurobiotin for characterization of its dendrites. There were no differences between tonic and phasic neurons, and both exhibited the following: (1) dendrites were multiple and branching; (2) all processes (axon and dendrites) arose from a circumscribed area on the somatic surface; (3) the initial direction of the processes was usually toward the center of the ganglion, creating a very dense intraganglionic neuropil; (4) tapering processes (presumed dendrites) extended beyond the border of the perineural sheath; and (5) many processes terminated with bouton-like swellings near the somatic surfaces of neighboring neurons within the same ganglion. Electron microscopic examination of dendritic and cell body membranes revealed that greater than 90% of the synapses occurred on dendrites. Based on immunohistochemical staining, all neurons were calbindin negative. These results indicate a relatively homogeneous population of neurons in bronchial parasympathetic ganglia displaying dendritic characteristics compatible with complex integrative properties.

Synaptic and membrane properties of parasympathetic ganglionic neurons innervating mouse trachea and bronchi

“…Spike width was consistently broader in phasic than in tonic cells (Fig. 2), similar to those found in human (9) and guinea pig bronchial ganglia (13,16). Although the AHP amplitude that followed single action potentials was approximately equal in tonic and phasic neurons, the duration of the AHP was nearly twice as long in most phasic neurons.…”

“…These neurons are referred to as phasic or tonic, respectively (4). Phasic and tonic neurons have also been reported for parasympathetic ganglionic neurons in guinea pig (13) and human bronchi (9). Unlike tonic neurons in guinea pig bronchial ganglia (12), mouse bronchial tonic neurons displayed more erratic patterns and a greater range of action potential frequencies at suprathreshold current steps (Fig.…”

“…For all data collection of active and synaptic membrane properties, the resting potential was current clamped to Ϫ50 mV before action potential generation and nerve stimulation. Neurobiotin ionophoresis and development were performed as previously reported (9,13).…”

“…Because of their peripheral location, parasympathetic nerves may be affected by local inflammation and airway remodeling (18). Although the active and passive (electrophysiological) membrane properties of airway ganglionic neurons have been reported for several mammalian species (13), including humans (8), no studies have focused on mice, a species commonly used in airway asthma and allergy studies (23).…”

Structure of peripheral synapses: autonomic ganglia

“…Similarly, although axo-dendritic synapses are often reported to be more common than axo-somatic synapses (e.g. Yamakado and Yohro 1977;Baluk et al 1985;May and Warren 1993;Armour et al 1997;Myers 2000), no unbiased tests of this proposition are available. In all likelihood, axo-dendritic synapses appear more often in sections simply as a result of sampling an essentially random distribution and there is no direct evidence for a preferential distribution of synapses onto dendrites.…”