Similar nociceptive afferents mediate psychophysical and electrophysiological responses to heat stimulation of glabrous and hairy skin in humans

Abstract

The ability to perceive and withdraw rapidly from noxious environmental stimuli is crucial for survival. When heat stimuli are applied to primate hairy skin, first pain sensation is mediated by type-II A-fibre nociceptors (II-AMHs). In contrast, the reported absence of first pain and II-AMH microneurographical responses when heat stimuli are applied to the hand palm has led to the notion that II-AMHs are lacking in this primate glabrous skin. The aim of this study was to assess the effect of hairy and glabrous skin stimulation on neural transmission of nociceptive inputs elicited by different kinds of thermal heating. We recorded psychophysical and EEG brain responses to radiant (laser-evoked potentials, LEPs) and contact heat stimuli (contact heat-evoked potentials, CHEPs) delivered to the dorsum and the palm of the hand in normal volunteers. Brain responses were analysed at a single-trial level, using an automated approach based on multiple linear regression. Laser stimulation of hairy and glabrous skin at the same energy elicited remarkably similar psychophysical ratings and LEPs. This finding provides strong evidence that first pain to heat does exist in glabrous skin, and suggests that similar nociceptive afferents, with the physiological properties of II-AMHs, mediate first pain to heat stimulation of glabrous and hairy skin in humans. In contrast, when contact heat stimuli were employed, a significantly higher nominal temperature had to be applied to glabrous skin in order to achieve psychophysical ratings similar to those obtained following hairy skin stimulation, and CHEPs following glabrous skin stimulation had significantly longer latencies (N2 wave, +25%; P2 wave, +24%) and smaller amplitudes (N2 wave, −40%; P2 wave, −44%) than CHEPs following hairy skin stimulation. Irrespective of the stimulated territory, CHEPs always had significantly longer latencies (hairy skin N2 wave, +75%; P2 wave, +56%) and smaller amplitudes (hairy skin N2 wave, −42%; P2 wave, −19%) than LEPs. These findings are consistent with the thickness-dependent delay and attenuation of the temperature waveform at nociceptor depth when conductive heating is applied, and suggest that the previously reported lack of first pain and microneurographical II-AMH responses following glabrous skin stimulation could have been the result of a search bias consequent to the use of long-wavelength radiant heating (i.e. CO 2 laser) as stimulation procedure.

Neurophysiology of Skin Thermal Sensations

“…hairy) and palm (i.e. glabrous) of human hand, as delivered via non-contact laser stimulation, induced qualitatively and quantitatively similar heat-pain sensations and brain potentials in healthy humans (161). Contrary to laser stimulation, contact heat stimulation of the palm of the hand (performed with a thermal probe) had to be significantly higher than that of the dorsum in order to obtain comparable heat-pain sensations.…”

“…Such differences in thermal sensitivity have long been suggested to dependent upon potential differences in sensory innervation between hairy and glabrous skin sites. However, recent evidence has indicated that, rather than being determined by physiological differences only (160), previously observed differences in thermal sensitivity between hairy and glabrous skin could have been partly determined by biophysical factors related to the properties of these types of skin (161). As opposed to hairy skin, glabrous skin presents a thicker stratum corneum (i.e.…”

“…Furthermore, brain responses (i.e. evoked potentials) to contact heating of the palm presented significantly longer latencies and smaller amplitudes than those resulting from the stimulation of the dorsum, despite the stimulating temperature used for the palm of the hand was higher than that applied to the dorsum of the hand (161). These observations indicated a potential thickness-dependent delay and attenuation of temperature-induced evoked potentials, hence thermal sensations, when conductive (as opposed to laser/radiant) heating was applied to glabrous skin.…”

Gamma-Band Oscillations in the Primary Somatosensory Cortex—A Direct and Obligatory Correlate of Subjective Pain Intensity

“…Noxious radiant-heat stimuli were generated by an infrared neodymium yttrium aluminum perovskite laser with a wavelength of 1.34 m (Electronical Engineering). These laser pulses activate directly and selectively nociceptive terminals located in the most superficial skin layers (Baumgärtner et al, 2005;Iannetti et al, 2006). Laser pulses were directed to the dorsum of the right and left hands, in two separate sessions performed on the same day.…”

Detection of pain from nociceptive laser-evoked potentials using single-trial analysis and pattern recognition

“…These laser pulses activate directly and selectively nociceptive terminals located in the most superficial skin layers [21][22]. Laser pulses were directed to the dorsum of the right and left hands, in two separate sessions performed on the same day.…”