Peripheral neural correlates of magnitude of cutaneous pain and hyperalgesia: a comparison of neural events in monkey with sensory judgments in human

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Abstract
The peripheral neural contributions to the magnitude of pain sensations elicited by heat stimulations of the skin and the increased pain to heat following a mild heat injury to the skin were studied by comparing psychophysical measures of pain in humans with impulse activity elicited by heat in single nociceptive afferents in the monkey. Human subjects made continuous magnitude ratings of pain elicitd by short-duration stimuli of 39.degree.-51.degree. C delivered before and at varying intervals of time following a heat injury induced by a conditioning stimulus (CS) of 50.degree. C and 100 s duration. The same stimuli were delivered to the receptive fields in hairy and glabrous skin of C-fiber and A-fiber mechanoheat nocicepotrs (CMH and AMH, respectively). For heat stimulations of normal skin, that is, uninjured skin stimulated prior to the CS, pain thresholds ranged from 41.degree. to 49.degree. C. For most subjects, magnitude scaling functions for pain relating the maximum rating of pain elicited by each stimulus to stimulus temperature were slightly positively accelerating. The median maximum pain rating increased as a positively accelerating function of stimulus temperature. In hyperalgesic skin, the median maximum pain rating increased as a negatively accelerating function of stimulus temperature, with the greatest increases over normal in pain ratings occurring in response to stimuli of 43.degree.-45.degree. C in hairy skin and 47.degree.-49.degree. C in glabrous skin with little, if any, increase in the magnitude of pain elicited by the highest stimulus of 51.degree. C. In contrast, the impulse discharges of most CMH nociceptors exhibited the greatest increases in response to stimuli of 47.degree.-49.degree. C. Since the overall amount of sensitization of glabrous skin CMH was not significant, the increases in CMH responses following a heat injury to either type of skin were not in proportion to increases in magnitude ratings of pain at each stimulus temperature. Evidence from control experiments indicated it was unlikely that the magnitude scaling of heat pain in normal skin and the changes in magnitude scaling following the development of hyperalgesia after heat injury depended on activity in AMH nociceptors, low-threshold thermoreceptors or regional changes in blood flow. Apparently, the activity in CMH nociceptors is a major peripheral determinant of heat pain sensation in normal skin and also contributes to the hyperalgesia following heat injury to the skin. If the magnitude of heat pain in normal skin is coded in the mean impulse discharge of CMH nociceptors as the data suggest, then the same neural code, at least as revealed in the responses of nociceptors in the monkey, does not fully account for the magnitude of change in pain sensation in humans following mild heat injury. Candidate explanations for certain mismatches between sensory and monkey neural events are discussed.