Synaptic complexes formed by functionally defined primary afferent units with fine myelinated fibers

Abstract

The individual fine myelinated fibers of cutaneous mechanical nociceptors and “D‐hair” receptors were identified by electrophysiological recording with micropipette electrodes in cats and monkeys. Their intraspinal terminations were labeled by iontophoresing horseradish peroxidase intracellularly and subsequent diaminobenzidine histochemistry. These terminations were examined with light and electron microscopy to determine the nature and organization of their synaptic contacts. Myelinated fibers of the mechanical nociceptors became unmyelinated before exhibiting many enlargements that made multiple synaptic contacts in the marginal zone (lamina I) and lamina V. Pre‐or postsynaptic contacts were found only on enlargements. In the marginal zone of the cat, enlargements made simple axodendritic contacts or were scalloped, central terminals in glomeruli. In glomeruli, myelinated mechanical nociceptor enlargements were presynaptic to several dendritic appendages and postsynaptic to two different types of profiles. One type was interpreted as a presynaptic axon terminal, the other as a presynaptic, vesicle‐containing, dendritic appendage. In lamina V of the cat the nociceptor synaptic complexes were similar, but simpler, and only axonal profiles were found to be presynaptic to them. In the monkey marginal zone and deep nucleus proprius, myelinated nociceptor terminations formed the central element of glomeruli, which consisted of postsynaptic dendritic appendages and presynaptic axon terminals. D‐hair axons terminated in large numbers of enlargements in the nucleusproprius (laminae III and IV) and inner substantia gelatinosa (lamina III). Their large rounded enlargements formed the central terminals in glomeruli and were presynaptic to both ordinary and vesicle‐containing dendritic appendages; the presynaptic dendritic profiles also often contacted each other. Profiles interpreted as axonal in origin were the only terminals presynaptic to the primary ending within the D‐hair glomeruli. The results suggest that transfer of primary afferent information occurs only at enlargements of the primary fiber and that each primary fiber enters into more than one kind of synaptic arrangement. They also point out that synaptic glomeruli are common to functionally different types of primary afferent fibers and that the internal organization of glomeruli varies with the kind of primary fiber and the locus of the complex.