Nociceptive Steady-State Evoked Potentials Elicited by Rapid Periodic Thermal Stimulation of Cutaneous Nociceptors

Mouraux, André; Iannetti, Gian Domenico; Colon, Elisabeth; Nozaradan, Sylvie; Legrain, Valéry; Plaghki, Léon

doi:10.1523/jneurosci.3977-10.2011

Cited by 83 publications

(85 citation statements)

References 61 publications

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“…It has recently been demonstrated in both rat and human that, somewhat counter-intuitively, a cutaneously applied CO 2 laser heat stimulus recruits first C-fibers, and then Aδ-fibers when its intensity is increased (Sikandar, personal communication; Mouraux et al, 2011). It is, therefore, likely that the potentiation of mid-range mechanical and upper range thermal-evoked responses by XE991 would be consistent with localization of M-channels primarily on Aδ-fiber peripheral terminals.…”

Section: Discussionmentioning

confidence: 99%

Functional significance of M-type potassium channels in nociceptive cutaneous sensory endings

Passmore¹,

Reilly²,

Thakur³

et al. 2012

Front. Mol. Neurosci.

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M-channels carry slowly activating potassium currents that regulate excitability in a variety of central and peripheral neurons. Functional M-channels and their Kv7 channel correlates are expressed throughout the somatosensory nervous system where they may play an important role in controlling sensory nerve activity. Here we show that Kv7.2 immunoreactivity is expressed in the peripheral terminals of nociceptive primary afferents. Electrophysiological recordings from single afferents in vitro showed that block of M-channels by 3 μM XE991 sensitized Aδ- but not C-fibers to noxious heat stimulation and induced spontaneous, ongoing activity at 32°C in many Aδ-fibers. These observations were extended in vivo: intraplantar injection of XE991 selectively enhanced the response of deep dorsal horn (DH) neurons to peripheral mid-range mechanical and higher range thermal stimuli, consistent with a selective effect on Aδ-fiber peripheral terminals. These results demonstrate an important physiological role of M-channels in controlling nociceptive Aδ-fiber responses and provide a rationale for the nocifensive behaviors that arise following intraplantar injection of the M-channel blocker XE991.

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Section: Discussionmentioning

confidence: 99%

Functional significance of M-type potassium channels in nociceptive cutaneous sensory endings

Passmore¹,

Reilly²,

Thakur³

et al. 2012

Front. Mol. Neurosci.

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“…whereas the nociceptive SEPs elicited by stimuli delivered with a short and constant ISI, as well as nociceptive steady-state evoked potentials (Colon et al 2012;Mouraux et al 2011), are symmetrically distributed over the two hemispheres. The lack of lateralized responses in short-ISI nociceptive SEPs and nociceptive steady-state evoked potentials suggests that these lateralized responses do not reflect cortical processes that are obligatory for nociception, i.e., that these lateralized responses are dependent on the context within which the stimulus is delivered.…”

Section: Contribution Of S1 To Nociceptive and Nonnociceptive Sepsmentioning

confidence: 99%

Unmasking the obligatory components of nociceptive event-related brain potentials

Mouraux

Paepe

Marot

et al. 2013

Journal of Neurophysiology

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-It has been hypothesized that the human cortical responses to nociceptive and nonnociceptive somatosensory inputs differ. Supporting this view, somatosensory-evoked potentials (SEPs) elicited by thermal nociceptive stimuli have been suggested to originate from areas 1 and 2 of the contralateral primary somatosensory (S1), operculo-insular, and cingulate cortices, whereas the early components of nonnociceptive SEPs mainly originate from area 3b of S1. However, to avoid producing a burn lesion, and sensitize or fatigue nociceptors, thermonociceptive SEPs are typically obtained by delivering a small number of stimuli with a large and variable interstimulus interval (ISI). In contrast, the early components of nonnociceptive SEPs are usually obtained by applying many stimuli at a rapid rate. Hence, previously reported differences between nociceptive and nonnociceptive SEPs could be due to differences in signal-to-noise ratio and/or differences in the contribution of cognitive processes related, for example, to arousal and attention. Here, using intraepidermal electrical stimulation to selectively activate A␦-nociceptors at a fast and constant 1-s ISI, we found that the nociceptive SEPs obtained with a long ISI are no longer identified, indicating that these responses are not obligatory for nociception. Furthermore, using a blind source separation, we found that, unlike the obligatory components of nonnociceptive SEPs, the obligatory components of nociceptive SEPs do not receive a significant contribution from a contralateral source possibly originating from S1. Instead, they were best explained by sources compatible with bilateral operculo-insular and/or cingulate locations. Taken together, our results indicate that the obligatory components of nociceptive and nonnociceptive SEPs are fundamentally different.pain; nociception; event-related potentials; primary somatosensory cortex; laser-evoked potentials; intraepidermal stimulation FOR THE PAST 30 YEARS, a large number of studies have aimed at understanding the neural mechanisms underlying the processing of nociceptive input and the perception of pain in the human cortex. Most of these studies have relied on noninvasive techniques to sample brain activity, such as electroencephalography (EEG), magnetoencephalography (MEG), functional magnetic resonance imaging (fMRI), and positron emission tomography (PET) (Bushnell and Apkarian 2005;Garcia-Larrea et al. 2003;Kakigi et al. 2005;Peyron et al. 2002;Treede et al. 1999). With these techniques, it has been shown repeatedly that nociceptive stimuli elicit responses in a wide array of brain areas, including postcentral, operculo-insular, and cingulate areas. A number of investigators have considered that the combined activation of these brain regions is responsible for the transformation of nociceptive input into a conscious perception of pain, in particular, the coding of pain intensity and pain unpleasantness (Boly et al.

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“…Since Regan firstly described the recording of SSRs as an alternative approach to investigate the neural activities in EEG [35], an increasing number of studies have used SSRs to explore the neural activities evoked by periodic repetition of various sensory stimuli (e.g., visual, auditory, somatosensory, and nociceptive) [13]–[15], [36]. However, we are not clear about how SSRs emerge from EEG, and it still remains a debate about the relationship between SSRs and transient ERPs [5].…”

Section: Discussionmentioning

confidence: 99%

“…Although transient ERPs and SSRs have been popularly employed by physiologists, psychologists, and physicians for their respective applications [9]–[13], their relationship remains a matter of debate [5]. While many researchers believe that SSRs are simply the result of the linear summation of successive transient brain responses evoked by the long-lasting periodic repetition of a sensory stimulus (superposition hypothesis) [14]–[18], others support the concept that SSRs are attributed to the stimulus-driven entrainment of an oscillatory network of neurons driven by the periodic repetition of a sensory stimulus (oscillatory entrainment mechanism) [19]–[23].…”

Section: Introductionmentioning

confidence: 99%

Distinct Features of Auditory Steady-State Responses as Compared to Transient Event-Related Potentials

et al. 2013

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Transient event-related potentials (ERPs) and steady-state responses (SSRs) have been popularly employed to investigate the function of the human brain, but their relationship still remains a matter of debate. Some researchers believed that SSRs could be explained by the linear summation of successive transient ERPs (superposition hypothesis), while others believed that SSRs were the result of the entrainment of a neural rhythm driven by the periodic repetition of a sensory stimulus (oscillatory entrainment hypothesis). In the present study, taking auditory modality as an example, we aimed to clarify the distinct features of SSRs, evoked by the 40-Hz and 60-Hz periodic auditory stimulation, as compared to transient ERPs, evoked by a single click. We observed that (1) SSRs were mainly generated by phase synchronization, while late latency responses (LLRs) in transient ERPs were mainly generated by power enhancement; (2) scalp topographies of LLRs in transient ERPs were markedly different from those of SSRs; (3) the powers of both 40-Hz and 60-Hz SSRs were significantly correlated, while they were not significantly correlated with the N1 power in transient ERPs; (4) whereas SSRs were dominantly modulated by stimulus intensity, middle latency responses (MLRs) were not significantly modulated by both stimulus intensity and subjective loudness judgment, and LLRs were significantly modulated by subjective loudness judgment even within the same stimulus intensity. All these findings indicated that high-frequency SSRs were different from both MLRs and LLRs in transient ERPs, thus supporting the possibility of oscillatory entrainment hypothesis to the generation of SSRs. Therefore, SSRs could be used to explore distinct neural responses as compared to transient ERPs, and help us reveal novel and reliable neural mechanisms of the human brain.

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Nociceptive Steady-State Evoked Potentials Elicited by Rapid Periodic Thermal Stimulation of Cutaneous Nociceptors

Cited by 83 publications

References 61 publications

Functional significance of M-type potassium channels in nociceptive cutaneous sensory endings

Functional significance of M-type potassium channels in nociceptive cutaneous sensory endings

Unmasking the obligatory components of nociceptive event-related brain potentials

Distinct Features of Auditory Steady-State Responses as Compared to Transient Event-Related Potentials

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