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. 2015 Oct;156(10):1936-1944.
doi: 10.1097/j.pain.0000000000000253.

Touch inhibits subcortical and cortical nociceptive responses

Flavia Mancini  1 , Anne-Lise Beaumont, Li Hu, Patrick Haggard, Gian Domenico D Iannetti
Affiliations

Touch inhibits subcortical and cortical nociceptive responses

Flavia Mancini et al. Pain. 2015 Oct.

Erratum in

  • Erratum.
    [No authors listed] [No authors listed] Pain. 2015 Dec;156(12):2636. doi: 10.1097/j.pain.0000000000000424. Pain. 2015. PMID: 26580683 Free PMC article. No abstract available.

Abstract

The neural mechanisms of the powerful analgesia induced by touching a painful body part are controversial. A long tradition of neurophysiologic studies in anaesthetized spinal animals indicate that touch can gate nociceptive input at spinal level. In contrast, recent studies in awake humans have suggested that supraspinal mechanisms can be sufficient to drive touch-induced analgesia. To investigate this issue, we evaluated the modulation exerted by touch on established electrophysiologic markers of nociceptive function at both subcortical and cortical levels in humans. Aδ and C skin nociceptors were selectively activated by high-power laser pulses. As markers of subcortical and cortical function, we recorded the laser blink reflex, which is generated by brainstem circuits before the arrival of nociceptive signals at the cortex, and laser-evoked potentials, which reflect neural activity of a wide array of cortical areas. If subcortical nociceptive responses are inhibited by concomitant touch, supraspinal mechanisms alone are unlikely to be sufficient to drive touch-induced analgesia. Touch induced a clear analgesic effect, suppressed the laser blink reflex, and inhibited both Aδ-fibre and C-fibre laser-evoked potentials. Thus, we conclude that touch-induced analgesia is likely to be mediated by a subcortical gating of the ascending nociceptive input, which in turn results in a modulation of cortical responses. Hence, supraspinal mechanisms alone are not sufficient to mediate touch-induced analgesia.

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Conflict of interest statement

Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.

Figures

Figure 1
Figure 1
Experimental paradigm. Each trial corresponded to one of the following 3 experimental conditions: Laser (L), Laser + Touch (L + T), and Catch. In each condition, white noise was played for 7 seconds. In the L + T condition, a robot delivered a pair of tactile stimuli from 1.5 to 1.7 seconds before until 1.5 to 1.7 seconds after the onset of the laser pulse. In the L condition, no tactile stimulation was delivered. In the Catch condition, neither nociceptive nor tactile stimulation occurred. At the end of the white noise, participants were instructed to respond, by verbally reporting both the quality and the intensity of the sensation evoked by laser stimulation.
Figure 2
Figure 2
Psychophysical results. Probability of detecting the laser stimulus (A), and average rating of subjective pain intensity when the laser was detected (B), in the “Laser” (L) and “Laser + Touch” (L + T) conditions. Each thin line represents a single subject, whereas the thick line depicts the group average. (C) Average frequency of occurrence of the descriptors of the quality of the elicited sensation when the laser was detected, in the L and L + T conditions.
Figure 3
Figure 3
Aδ-laser-evoked potentials (Aδ-LEPs). Laser-evoked potentials (LEPs) were elicited by the stimulation of the right hand dorsum and recorded from 32 electrodes. Displayed signals show group-level LEPs recorded from the vertex (Cz vs nose) and from the contralateral central electrode (C3 vs Fz). Point-by-point t values are shown below the LEPs. Time intervals during which the LEP was significantly different in the “Laser” (L) and “Laser + Touch” (L + T) conditions are highlighted in gray. Scalp topographies of the response amplitude in the L and L + T conditions are displayed at the peak latency of the Aδ-N1, Aδ-N2, Aδ-P2, and Aδ-P4 waves. The topographical distribution of t values reflecting the statistical comparison between the L and L + T conditions is shown for each of the 4 waves. The line graphs on the right-hand side show the single-subject peak amplitudes of each wave in the 2 conditions. The P values reflect the significance of the paired t test between the peak amplitudes in the L and L + T conditions (Bonferroni-corrected t tests, α = 0.0125, 2-tailed).
Figure 4
Figure 4
C-laser-evoked potentials (C-LEPs). Waveforms were aligned according to the peak latency of the Aδ-N2, Aδ-P2, C-N2, and C-P2 waves, using a validated method. Displayed signals show group-level LEPs recorded from the vertex (Cz vs nose). Point-by-point t values are shown below the LEPs. Time intervals during which the LEP was significantly different in the “Laser” (L) and “Laser + Touch” (L + T) conditions are highlighted in gray. Scalp topographies of the response amplitude in the L and L + T conditions are displayed at the peak latency of the C-N2 and C-P2 waves, together with the topographical distribution of t values reflecting the statistical comparison between the L and L + T conditions.
Figure 5
Figure 5
Laser Blink Reflex (LBR). Group-level average waveforms of the LBR elicited by laser stimulation of the hand. The EMG signals were recorded from the OO muscle ipsilateral to the stimulated hand, using surface electrodes. Point-by-point t values are displayed below the LBR waveforms. The time interval during which the LBR was significantly different in the “Laser” and “Laser + Touch” conditions is highlighted in gray. OO, orbicularis oculi.
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