Evoked oscillatory cortical activity during acute pain: Probing brain in pain by transcranial magnetic stimulation combined with electroencephalogram

Enrico De Martino, Adenauer Casali, Silvia Casarotto, Gabriel Hassan, Mario Rosanova, Bruno Andry Nascimento Couto, Thomas Graven-Nielsen, Daniel Ciampi de Andrade
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Abstract

Temporal dynamics of local cortical rhythms during acute pain remain largely unknown. The current study used a novel approach based on transcranial magnetic stimulation combined with electroencephalogram (TMS-EEG) to investigate evoked-oscillatory cortical activity during acute pain. Motor (M1) and dorsolateral prefrontal cortex (DLPFC) were probed by TMS, respectively, to record oscillatory power (event-related spectral perturbation and relative spectral power) and phase synchronization (inter-trial coherence) by 63 EEG channels during experimentally induced acute heat pain in 24 healthy participants. TMS-EEG was recorded before, during, and after noxious heat (Acute Pain condition) and non-noxious warm (Control condition), delivered in a randomized sequence. The main frequency bands (α, β1, and β2) of TMS-evoked potentials after M1 and DLPFC stimulation were recorded close to the TMS coil and remotely. Cold and heat pain thresholds were measured before TMS-EEG. Over M1, Acute pain decreased α-band oscillatory power locally and α-band phase synchronization remotely in parietal-occipital clusters compared with non-noxious warm (all P<0.05). The remote (parietal-occipital) decrease in α-band phase synchronization during Acute Pain correlated with the cold (P=0.001) and heat pain thresholds (P=0.023) and to local (M1) α-band oscillatory power decrease (P=0.024). Over DLPFC, Acute Pain only decreased β1-band power locally compared with non-noxious warm (P=0.015). Thus, evoked-oscillatory cortical activity to M1 stimulation is reduced by acute pain in central and parietal-occipital regions and correlated with pain sensitivity, in contrast to DLPFC, which had only local effects. This finding expands the significance of α and β band oscillations and may have relevance for pain therapies.
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急性疼痛时大脑皮层的诱发振荡活动:通过经颅磁刺激结合脑电图探测疼痛中的大脑
急性疼痛时局部皮层节律的时间动态在很大程度上仍不为人所知。本研究采用了一种基于经颅磁刺激结合脑电图(TMS-EEG)的新方法来研究急性疼痛时的诱发振荡皮层活动。在实验诱发急性热痛期间,24 名健康参与者的运动皮层(M1)和背外侧前额叶皮层(DLPFC)分别受到经颅磁刺激,通过 63 个脑电图通道记录振荡功率(与事件相关的频谱扰动和相对频谱功率)和相位同步(试验间相干性)。在毒性热(急性疼痛条件)和非毒性温(对照条件)之前、期间和之后,以随机顺序记录了 TMS-EEG 信号。M1和DLPFC受到刺激后,TMS诱发电位的主要频段(α、β1和β2)是在靠近TMS线圈的地方远程记录的。在 TMS-EEG 之前测量了冷痛和热痛阈值。在 M1 上,与无毒性的暖痛相比,急性疼痛降低了顶叶-枕叶簇局部的 α 波段振荡功率和远程的 α 波段相位同步(所有 P<0.05)。急性疼痛期间α波段相位同步的远程(顶叶-枕叶)下降与冷(P=0.001)和热痛阈值(P=0.023)以及局部(M1)α波段振荡功率下降(P=0.024)相关。在 DLPFC 上,与非毒性温热相比,急性疼痛仅降低局部的 β1 波段功率(P=0.015)。因此,在中央区和顶枕区,急性疼痛会降低 M1 刺激的诱发-振荡皮质活动,并与疼痛敏感性相关,而 DLPFC 仅有局部影响。这一发现拓展了α和β波段振荡的意义,可能与疼痛疗法有关。
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