Rapidly adapting pulmonary receptor afferents: II. Fine structure and synaptic organization of central terminal processes in the nucleus of the tractus solitarius

The nucleus of the tractus solitarius (nTS) is a site for termination of primary afferents originating from a variety of different visceral sensory endings (Kalia and Mesulam: J. Comp. Neurol. 193 :523–553, '80). The light and electron microscopic evaluation of bouton terminals of slowly adapting lung stretch (SAR afferent fibers originating from the tracheobronchial tree has been described previously (Kalia and Richter: J. Comp. Neurol. 241 :503–520, 521–535, '85. The companion article (Kalia and Richter: J. Comp. Neurol. 273 :000‐000, '88) describes details of the light microscopic organization of a second group of pulmonary afferents, the rapidly adapting receptors (RARs), that are known to signal transient volume changes in airways (Sellick and Widdicombe: J. Physiol. (Lond. 203 : 359–381, '69; Q.J. Exp. Physiol. 55 :153–163, '70. Terminals from RAR afferents are concentrated within two specific subnuclear groups of the nTS (dnTS and nI) and are distributed over 4 mm of the medulla oblongata rostrocaudally. Within the nTS, axon collaterals of RAR afferents remain myelinated up to a diameter of 0.4–1.0 μm. Preterminal processes are always unmyelinated and range in diameter from 0.15 to 0.3 μm. Bouton terminals (1.0–2.0 μm) are of both the en passant and end terminal varieties. The synaptic profiles formed by 143 bouton terminals of RAR afferents, were examined in uninterrupted sequential sections and are described in this paper. All the bouton terminals examined under the electron microscope were found to contain clear, round synaptic vesicles. Boutons made synaptic contact with different profiles in each of the two subnuclei (dnTS and nI) examined. Contacts were usually asymmetrical (type I) containing clear, round synaptic vesicles 35–50 nm in diameter. In the dorsal subnucleus of the nTS (dnTS), the synaptic arrangement of RAR boutons did not appear to be complex. The RAR bouton terminal was usually located in juxtaposition to unlabeled axon terminals of similar morphological characteristics. Typically, the RAR bouton terminal made synaptic contact with a medium‐sized spiny dendrite. No axosomatic contacts involving RAR afferents were observed in this subnucleus. In the intermediate subnucleus of the nTS (nI), the most common synaptic arrangement of RAR bouton terminals was in the form of a “glomerulus,” which was formed by five to seven different types of neuronal profiles surrounding the labeled RAR bouton terminal. These included 1) medium‐sized spiny dendrites, 2) vesicle‐containing axon terminals that were usually postsynaptic to the RAR bouton terminal, 3) dendritic spines, and 4) vesicle‐containing dendrites in which the RAR bouton was located presynaptically. There were no contacts with somata in the present sample. The average length of synapses made by RAR boutons was 1 pm. Typically, an RAR bouton formed synapses with approximately seven different profiles simultaneously, of which at least three of these contacts were visible in a single ultrathin section. The most complex synaptic arrangement of RAR bouton terminals occurred when the labeled RAR bouton was the central component of a glomerulus and displayed synapses with two axon terminals, two to three dendrites, and one to two dendritic spines. It is concluded that RAR pulmonary afferents convey information to selected subnuclei of the nTS. In addition there are significant ultrastructural differences in the synaptic organization of RAR boutons in these regions. Furthermore, RAR pulmonary afferents differ remarkably from SAR pulmonary afferents while closely resembling RAR afferents from somatic mechanoreceptors (Semba et al.: J. Comp. Neurol. 232229‐240, '85). It appears likely that this complex synaptic organization of RAR pulmonary afferents provides the anatomical substrate for a variety of functional influences in this region.