Modality-Dependent Modulation of Conduction by Impulse Activity in Functionally Characterized Single Cutaneous Afferents in the Rat

Abstract

Cutaneous afferents exhibit changes in excitability after impulse activity that are correlated with functional modality but are independent of axonal diameter, as studied in 39 cold fibers and 51 nociceptors of the rat. Latency of conducted impulses was used to indicate changes in axonal excitability caused by electrical stimulation. Stimuli were applied both at fixed frequencies and at the time intervals of impulses previously recorded during response to natural stimulation. Latency increased following both these forms of electrical stimulation, as well as after natural stimulation of the receptive fields. The latency increase was correlated with the number of impulses and the frequency of the preceding discharge in all of 4 nociceptors and 13 cold fibers studied for this feature. Increase of latency by electrical or natural stimulation led to reduced responsiveness to natural stimulation. The magnitude and time course of latency changes were correlated with fiber modality. In 32 nociceptors the latency increased continuously with time during a stimulus train, whereas in 21 cold fibers there was only an initial increase in latency over the first few seconds, after which the latency remained at a plateau even as the firing response continued. Paralleling this slowing, impulse failure occurred more frequently during repetitive stimulation in both A delta and C nociceptors than in velocity-matched cold fibers of either class. Based on the magnitude of latency increases during stimulus trains at different frequencies, two distinct patterns were discerned in A nociceptors: "Type II" fibers slowed significantly more than "Type I" or cold fibers. The results support the hypotheses (1) that the pattern of latency changes during activity are signatures for the modality in a given fiber; and (2) that endogenous, activity-dependent processes of the axon contribute to adaptation and encoding in cutaneous sensory afferents.

Activity‐dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin

“…Whatever the mechanisms involved, the variations in activity-dependent slowing have important functional implications. The progressive increase in latency of the type 1 fibres was clearly associated with a progressive decrease in excitability, which resulted in conduction block for these nociceptor fibres only, as also noted by Thalhammer et al (1994). The rise in electrical threshold indicates that the fibre would also have a higher threshold for excitation by a natural stimulus, and the absence of any plateau in the latencies suggests that the maximum continuous rate of nociceptor discharge is severely limited by the properties of the axons.…”

“…We have found that these fibres can be segregated into at least three different classes on the basis of their response to repetitive stimulation, and that it is possible unambiguously to differentiate nociceptive from cold-specific C fibres innervating human skin, as has previously been shown for the rat (Thalhammer et al 1994;Gee et al 1996).…”

Activity-Dependent Modulation of Axonal Excitability in Unmyelinated Peripheral Rat Nerve Fibers by the 5-HT(3) Serotonin Receptor

“…1996; Shin and Raymond 1991;Thalhammer et al 1994) and human (Bostock et al 2003;Serra et al 1999;Weidner et al 2002) C-fiber axons. In most of these studies, single-fiber recordings in situ provided a method for correlation of electrophysiological parameters with the function of the C-fiber.…”

A multi-scale view of skin thermal pain: from nociception to pain sensation

“…Although adaptation in the transformation process is supported by decreased CV (Thalhammer et al 1994;Schmelz et al 1995;Serra et al 1999) and reduced kinetics of sensory neuron-specific sodium channels (Waxman et al 1999), there is no evidence for adaptation in the transduction process so far.…”