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

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 nucleus proprius (laminae I11 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.The population of primary afferent neurons with myelinated fibers is composed of a number of sets of functionally distinct sensory receptors, each set consisting of the elements with closely similar features. The functions ClaSsically assigned to the morphologically characterized pe-

Cutaneous excitatory and inhibitory input to neurones of the postsynaptic dorsal column system in the cat.

“…The vigorous responses of these neurones to noxious mechanical and thermal stimuli observed in the present study are consistent with reports that the dendrites of PSDC neurones frequently enter lamina II and even I (Brown & Fyffe, 1981) and that these dendrites may participate in glomerular synaptic complexes (Bannatyne, Brown, Fyffe & Maxwell, 1982;Bannatyne et al 1987), the central terminals of which are thought to originate from Ad or C primary afferent fibres (Gobel, Falls & Humphrey, 1981;Rethelyi, Light & Perl, 1982;Kniyihar-Csillik, Csillik & Rakic, 1982). These observations suggest that PSDC neurones may receive a direct input from nociceptive afferent fibres.…”

Myelinated Skin Sensory Neurons Project Extensively throughout Adult Mouse Substantia Gelatinosa

“…Furthermore, the present studies highlight the fact that the SG of mice also receives substantial inputs from D-HFAs, among the most exquisitely sensitive tactile afferents that innervate the body surface; a rare population of unmyelinated tactile afferents also project to this region (Sugiura et al, 1986;Sugiura, 1996). Importantly, D-HFAs were found to project far more dorsally than previously documented in lamina IIi (Woodbury et al, 2001) [see also , Rethelyi et al (1982), and Hayashi (1985)], well into lamina IIo, where they were clearly in position to intermingle with unmyelinated nociceptor terminals. This suggests that D-hair inputs are not yet fully mature in neonates (cf.…”

“…A few exhibited peripheral CVs in the low A␤ range, and although similar nociceptors arborizing throughout all laminas have not yet been documented outside mice, this distinctive central anatomy exhibits some similarity to a subset of incompletely labeled nociceptors in cat and monkey Rethelyi et al, 1982) and is identical to that of a few unidentified A␤ fibers labeled after nerve injury in rats (Woolf et al, 1992). Importantly, the present findings reveal that this morphologically unique class of afferents is not only present but arborizes extensively throughout the dorsal horn of normal (i.e., uninjured) adult mice and may account for earlier observations of occasional A␤ inputs to marginal neurons in primates (Kumazawa and Perl, 1978).…”

“…However, observations of isolated D-hair arbors invading "the deep two-thirds of lamina II" in the spinal trigeminal nucleus caudalis of cat (Hayashi, 1985) not only suggest otherwise, but may help explain the substantial portion of cat SG that remains unlabeled at spinal levels after isolectin-B 4 transport (Woodbury et al, 2000). Moreover, a more superficial termination of tactile afferents than commonly held is supported by the finding that type II synaptic glomeruli, formed by D-HFAs (Rethelyi et al, 1982), constitute ϳ20% of the glomerular structures in lamina IIo (Ribeiro-da-Silva and Coimbra, 1982). Thus, the most parsimonious explanation may simply reflect the fact that the use of NB in the present studies labeled greater numbers of collaterals in this diminutive species than previous attempts with HRP in larger species Hayashi, 1985), revealing both the most superficially terminating collaterals in the main central projection and deeper isolated outliers (Koerber and Mirnics, 1995;Wilson et al, 1996).…”

Distinct Populations of Spinal Cord Lamina II Interneurons Expressing G-Protein-Gated Potassium Channels

“…Glomeruli with clear morphological features containing dendrites positive for GIRK subunits were classified according to accepted criteria (Rethelyi and Szentagothai, 1969;Rethelyi et al, 1982;Ribiero-da-Silva and Coimbra, 1982;Gerke and Plenderleith, 2004). Type I glomeruli were identified by their large scalloped central termini and contacts with at least four or five dendrites, the presence of densely packed pleiomorphic synaptic vesicles, and the relative dearth of mitochondria.…”