Response properties of nociceptive and low‐threshold neurons in rat trigeminal pars caudalis

Abstract

There is little doubt that trigeminal nociceptive neurons play a critical role in signaling the presence of harmful, or potentially harmful, orofacial stimuli. Unfortunately, there is only a limited understanding of how these neurons code such stimuli and whether this code is maintained in those structures responsible for generating overt reactions. The present series of experiments were designed to quantitatively document the response properties of nociceptive neurons in the rat trigeminal pars caudalis using the same electrical and innocuous and/or noxious mechanical and thermal stimuli employed in the characterization of nociceptive neurons with orofacial receptive fields in the rat superior colliculus. Neurons were classified as either low-threshold mechanoreceptive, wide-dynamic-range, or nociceptive-specific (type I, II) depending on their responsiveness to these stimuli. Nociceptive pars caudalis neurons (92/135, 68%) had receptive field organizations and input fibers (as indicated by latencies to electrical stimuli) quite different from those of low-threshold neurons (43/135, 32%). Nociceptive stimulus-response relationships for the population of wide-dynamic-range and nociceptive-specific type I neurons to contact heat stimuli were positively accelerating power functions with exponents of 3.9 and 4.4, respectively. This contrasted sharply with the low-threshold component of wide-dynamic-range neurons which was a negatively accelerating power function with an exponent of 0.7. All categories of nociceptive neurons also responded vigorously to cold stimuli. The thresholds of both hot and cold stimuli were often below psychophysical estimates of thermal pain, suggesting that "nociceptive" neurons process far more information than that required to signal potentially harmful stimuli. The fundamental similarities in nociceptive properties in pars caudalis and other structures of the central nervous system suggest that there is little transformation of the information encoded at successive levels of the neuraxis. This is consistent with the idea that the functional role of nociceptive neurons is reflected more in which circuits they are integrated and less in differences in their physiological properties.

Pharmacological dissection of the paradoxical pain induced by a thermal grill

“…Consistent with this hypothesis, which is not mutually exclusive with the disinhibition theory, numerous cells with a very large range of responses to thermal stimuli (ie Wide Dynamic Range (WDR) neurones) have been recorded in both the spinal cord and thalamus in rats, cats and primates (e.g. Poulos and Benjamin, 1967;Burton, 1975;Price et al, 1978;Yamasoto and Pierau, 1980;Kenshalo et al, 1982;Bushnell et al, 1993;McHaffie et al, 1994;Apkarian and Shi, 1994), although they rarely responded to both cool and warm stimuli (Khasabov et al, 2001). Thus, the perceptual discrimination of the quality and intensity of the sensation might depend on the relative activities of the so-called "labelled sensory lines" (i.e.…”

Increase in NADPH-Diaphorase-Positive and Neuronal NO Synthase Immunoreactive Neurons in the Rat Spinal Trigeminal Nucleus Following Infusion of a NO Donor—Evidence for a Feed-Forward Process in NO Production Involved in Trigeminal Nociception

“…The superficial laminae of the medullary and spinal dorsal horn, in particular lamina IIa (substantia gelatinosa), are known to receive most of the afferent input of thin (Ad and C) fibres (34,(42)(43)(44) and show the most dense immune staining with antibodies against neuropeptides such as substance P or calcitonin gene-related peptide (CGRP) (45,46), which are regarded as typical for nociceptive afferents. The deep layers are less clearly defined in the STN, and in functional studies are usually not divided into separate laminae (47)(48)(49). There is convergent evidence that the deep laminae contain large wide-dynamic range (WDR) neurons that receive both low-threshold and nociceptive information (50)(51)(52), and most of our previous electrophysiological recordings are from those neurons (17,32,33,53).…”

Trigeminal intersubnuclear neurons: Morphometry and input‐dependent structural plasticity in adult rats

“…The Journal of Comparative Neurology | Research in Systems Neuroscience primarily in laminae I, II, and deep V . Wide-dynamic range neurons also abound in the magnocellular laminae (McHaffie et al, 1994). Moreover, low-threshold mechanosensitive neurons have denser trees of fairly thick dendrites with few or no spines, whereas nociceptive neurons tend to display sparser arbors of thinner dendrites with numerous spines .…”