Sensitization of myelinated nociceptive afferents that innervate monkey hand

J. N. Campbell, R. A. Meyer, R. H. LaMotte

Research output: Contribution to journalArticlepeer-review

Abstract

Forty-four myelinated primary afferents innervating the monkey hand and sensitive to both mechanical and heat stimuli (AMHs) were studied by the method of single-unit recording. The thermal response properties were studied with use of a noncontact laser thermal stimulator that provided step increases in skin temperature with rise times of 200-250 ms and temperature control within 0.1°C. Mechanical response properties were studied with use of a stimulator that provided step increases in force. The AMHs had a mean conduction velocity of 31.1 ± 1.5 (SE) m/s (range 5.2-53.3 m/s), mean receptive-field area of 37±4 mm2 (range 2.3-121 mm2), a mean pressure threshold of 3.5±0.3 bars (Von Frey technique' range, 1.6-9.4 bars), no response to cooling stimuli, and no spontaneous activity prior to stimulation. The number of impulses evoked by mechanical stimulation with a 0.8 mm-diameter probe increased monotonically with increasing force of skin identation up to 200 g, the highest force used. Each of the AMHs became sensitized to heat after repeated exposure of its receptive field to high intensities of heat. When a 53°C stimulus of 3 s duration was delivered every 28 s, the number of impulses evoked during each stimulus increased, the response latency decreased, the duration of the afterdischarge and the number of impulses in the afterdischarge increased, and spontaneous activity frequently developed. Before sensitization, 88% (37 of 42) had heat thresholds greater than 49°C. After sensitization the heat thresholds were lower for all fibers tested (n=30) and 67% had thresholds less than 45°C. The number of impulses evoked by suprathreshold stimuli increased monotonically with stimulus temperature. The response properties of AMHs were compared with those of polymodal nociceptive C-fibers (CPNs) that innervated the monkey hand. The receptive fields of 12 CPNs were exposed to 53°C stimuli of 3 s duration delivered every 28 s. In contrast to the AMHs, all but one CPN showed response depression as a function of iterative stimulation. The response properties of AMHs were compared with those of eight slowly adapting mechanoreceptive afferents (SAMs) that innervated the monkey hand. The pressure threshold (̄x, 1.09 bars) was significantly less and the conduction velocity (̄x, 42.6 m/s) and receptive-field area (̄x, 65.8mm2) significantly greater than corresponding values for the AMHs. In contrast to AMHs, SAMs responded only during the cooling phase of heat stimuli. This thermal response increased with iterative heating and thus, is considered a special form of sensitization. AMHs are a distinct population of mechanically sensitive cutaneous nociceptive afferents that develop a prolonged increased sensitivity to heat following noxious heating of their receptive fields. Thus, hyperalgesia that follows a cutaneous burn may be mediated, at least in part, by activity in AMHs.

Original languageEnglish (US)
Pages (from-to)1669-1679
Number of pages11
JournalJournal of neurophysiology
Volume42
Issue number6
DOIs
StatePublished - Jan 1 1979

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

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