Cortical activity evoked by an acute painful tissue-damaging stimulus in healthy adult volunteers.

Lorenzo Fabrizi,Rebeccah Slater,Judith Meek,Amy Lee,Sofia Olhede,Gemma Williams,Maria Fitzgerald

doi:10.1152/jn.00990.2012

Lorenzo Fabrizi, Rebeccah Slater + Show 5 more

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https://doi.org/10.1152/jn.00990.2012

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Abstract

Everyday painful experiences are usually single events accompanied by tissue damage, and yet most experimental studies of cutaneous nociceptive processing in the brain use repeated laser, thermal, or electrical stimulations that do not damage the skin. In this study the nociceptive activity in the brain evoked by tissue-damaging skin lance was analyzed with electroencephalography (EEG) in 20 healthy adult volunteers (13 men and 7 women) aged 21–40 yr. Time-frequency analysis of the evoked activity revealed a distinct late event-related vertex potential (lance event-related potential, LERP) at 100–300 ms consisting of a phase-locked energy increase between 1 and 20 Hz (delta-beta bands). A pairwise comparison between lance and sham control stimulation also revealed a period of ultralate stronger desynchronization after lance in the delta band (1–5 Hz). Skin application of mustard oil before lancing, which sensitizes a subpopulation of nociceptors expressing the cation channel TRPA1, did not affect the ultralate desynchronization but reduced the phase-locked energy increase in delta and beta bands, suggesting a central interaction between different modalities of nociceptive inputs. Verbal descriptor screening of individual pain experience revealed that lance pain is predominantly due to Aδ fiber activation, but when individuals describe lances as C fiber mediated, an ultralate delta band event-related desynchronization occurs in the brain-evoked activity. We conclude that pain evoked by acute tissue damage is associated with distinct Aδ and C fiber-mediated patterns of synchronization and desynchronization of EEG oscillations in the brain.

Highlights

ELECTROENCEPHALOGRAPHIC (EEG) brain activity in response to noxious experimental stimulation has been extensively studied in human adult volunteers
Potential, consisting of a negative and a positive deflection maximal at the vertex, ascribed to activation of A␦ afferents, has been reported after a wide variety of noxious stimulation, such as electrical (Bromm and Scharein 1982; Miltner et al 1989; Naka and Kakigi 1998), mechanical (Bromm and Scharein 1982), contact heat (Chao et al 2008; Chen et al 2001; Harkins et al 2000), and laser radiant heat (Bromm and Treede 1987; Mouraux et al 2003; Zhang et al 2012). This event-related potentials (ERPs), which differs in latency and in labeling according to the stimulus modality, has been most commonly studied in response to laser radiant heat, when it is often termed laserevoked potential (LEP)
Finger lances evoked a clear late NP complex. This was called the lance event-related potential (LERP) and had a P peak significantly greater in amplitude and latency than that of the NP complex evoked by sham control

Summary

Introduction

ELECTROENCEPHALOGRAPHIC (EEG) brain activity in response to noxious experimental stimulation has been extensively studied in human adult volunteers. Potential, consisting of a negative and a positive deflection maximal at the vertex, ascribed to activation of A␦ afferents, has been reported after a wide variety of noxious stimulation, such as electrical (Bromm and Scharein 1982; Miltner et al 1989; Naka and Kakigi 1998), mechanical (Bromm and Scharein 1982), contact heat (Chao et al 2008; Chen et al 2001; Harkins et al 2000), and laser radiant heat (Bromm and Treede 1987; Mouraux et al 2003; Zhang et al 2012) This ERP, which differs in latency and in labeling according to the stimulus modality, has been most commonly studied in response to laser radiant heat, when it is often termed laserevoked potential (LEP). These properties, together with the selective activation of the two fiber types by different stimulus modalities, have been used to devise a novel assessment tool that discriminates between A␦ and C fibermediated pain based on the selection of verbal descriptors from the McGill Pain Questionnaire (Beissner et al 2010)

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