Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: Indications of their place in dorsal horn functional organization

Abstract

Electrophysiological recordings were made from superficial parts of the spinal dorsal horn in monkeys, using dye-filled micropipette electrodes to permit iontophoretic marking of the recording sites for subsequent histological recovery. Focal field potentials and unitary activity evoked by dorsal root volleys including slowly-conducting components (both myelinated and unmyelinated) were found in the posteromarginal zone and the substantia gelatinosa (SG). Unitary potentials identified as being of the type recorded from cellular regions were separated into categories according to which group of slowly-conducting fibers and which kinds of cutaneous stimulation evoked the discharge. Recording locations for units excited by volleys in myelinated fibers conducting under 35 m/sec, by the types of skin stimulation activating either high-threshold mechanoreceptors (nociceptors) or cooling thermoreceptors, and giving no evidence of suprathreshold C-fiber excitation were centered on the posteromarginal zone. In contrast, recording loci for units exhibiting a strong C-fiber excitation and responses to cutaneous stimulation known to effectively excite C-fiber polymodal nociceptors or C-mechanoreceptors were centered in the SG. There appeared varying degrees of convergence of primary afferent input to the neuronal units, although most showed substantial specificity in their afferent excitation. On the bases of these results and consideration of existing morphological data, it is proposed that the marginal zone is a major synaptic termination region for the afferent fibers from high-threshold mechanoreceptors, cooling thermoreceptors, and perhaps other receptors with fine myelinated peripheral fibers. The SG, on the other hand, is suggested to be the terminal region for all types of unmyelinated primary afferent sensory neurons, and to have the complex role of integrating and distributing this input.

Myelinated Skin Sensory Neurons Project Extensively throughout Adult Mouse Substantia Gelatinosa

“…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).…”

Hypothalamic Hypocretin (Orexin): Robust Innervation of the Spinal Cord

“…Although most of the axons in Lissauer's tract, dorsolateral to the dorsal horn, are primary sensory axons (Chung and Coggeshall, 1982), hypocretin axons descend here before entering lamina 1. Previous work has shown fine-caliber primary afferents terminating in lamina 1 (Kumazawa and Perl, 1978). Three types of cells in lamina 1 were found in physiological studies: those that respond to mechanical or thermal nociception and a type that responds to both noxious stimuli and non-pain-related temperature changes (Christensen and Perl, 1970).…”

Direct GABAergic and Glycinergic Inhibition of the Substantia Gelatinosa from the Rostral Ventromedial Medulla Revealed byIn VivoPatch-Clamp Analysis in Rats

“…The superficial dorsal horn, especially the substantia gelatinosa [(SG) lamina II] of the spinal cord (Rexed, 1952), is implicated in nociceptive processing, because small myelinated A␦-afferent and unmyelinated C-afferent fibers that convey predominantly noxious sensation make synaptic contacts with SG neurons (Kumazawa and Perl, 1978;Cervero and Iggo, 1980;Sugiura et al, 1986;Yoshimura and Jessell, 1989;Yoshimura, 1996). To characterize the descending inhibitory pathway from the RVM in this study, we recorded IPSCs of SG neurons by means of the in vivo patch-clamp technique and examined the effects of chemical and electrical stimulation (ES) of the RVM.…”