Morphology and synaptic connections of ultrafine primary axons in lamina I of the spinal dorsal horn: candidates for the terminal axonal arbors of primary neurons with unmyelinated (C) axons

Abstract

Neurons in Rexed's lamina I have the bulk of their dendritic arbors confined within this lamina. This study examines the morphology and synaptic connections of primary axons which generate axonal endings in lamina I of the spinal dorsal horn and are in position to deliver their inputs directly to lamina I neurons. Primary axons were made visible for light and electron microscopical study by applying horseradish peroxidase (HRP) to the severed central stumps of cervical and lumbar dorsal roots and allowing sufficient time for the orthograde movement of the HRP into the terminal axonal arbors. Golgi preparations provided supplementary light microscopical views of these axons. Lamina I receives the terminal arborization of two very different kinds of primary axons. One of these generates many ultrafine endings along unbranched, long rostrocaudally oriented, strand-like collaterals which arise from thin parent branches in Lissauer's tract. In view of these thin parent branches, most ultrafine primary axons are considered to be unmyelinated (C) primary axons. The second kind of primary axon generates large caliber endings on branched collaterals. These arise from relatively thick parent branches in Lissauer's tract which, on the basis of their size, are considered to be myelinated (A delta) primary axons. The scalloped endings of both primary axons lie in the interior of glomeruli where they form axodendritic synapses on small dendritic shafts and spines. It is at these synapses that these two kinds of primary axons are thought to transfer nociceptive and thermal inputs directly to the dendritic arbors of lamina I neurons. Transmitter release at these axodendritic synapses in response to primary inputs can be modified, probably diminished or inhibited, by synaptic events within the glomeruli from at least three sources. Synaptic vesicle-containing dendrites form dendroaxonic synapses on primary endings and two kinds of axons form axoaxonic synapses either on primary endings or on the intervaricose segments of the primary axons.