Background & Aims
Previous studies have established a link between sensorimotor ?-oscillations and pain anticipation/perception [1-5], along with the potential of transcranial alternating current stimulation (tACS) in the ?-frequency band to influence cortical ?-oscillations [6-10]. This study aimed to explore the impact of sensorimotor ?-tACS on pain anticipation and perception, specifically examining whether these effects depend on the certainty of expectations.
Methods
In a double-blinded, sham-controlled design, 80 healthy participants underwent a 20-minute session of either real or sham high-definition ?-tACS over the right sensorimotor region. Participants in the real group received 20 minutes of ?-tACS stimulation, while those in the sham group received 20 minutes of sham stimulation. Before (T0), immediately after (T1), and 30 minutes after (T2) the end of tACS application, participants in both groups completed a pain-rating task in which pain or no pain stimuli were delivered in either certain or uncertain contexts. Following each painful stimulation, participants verbally rated the intensity and unpleasantness of the perceived pain. Laser-evoked behavioral and neural responses, as well as anticipatory EEG oscillations recorded before, immediately after, and 30 minutes after ?-tACS in both certain and uncertain conditions, were compared between the real and sham groups.
Results
Real ?-tACS disrupted the habituation of laser-evoked potentials (N2-P2 complex), particularly in conditions with certain expectations and persisting 30 minutes post-stimulation. In anticipatory cortical oscillations, real ?-tACS enhanced somatosensory lower-frequency ?-oscillations and increased midfrontal ?-oscillations in conditions with certain expectations, with the ?-oscillation modulation showing sustained effects. Mediation analysis revealed that ?-tACS reduced pain-related reactivity by enhancing somatosensory ?-oscillations and increased pain-related reactivity through midfrontal ?-oscillations enhancement, with the latter effect being more pronounced.
Conclusions
Our results demonstrated that ?-tACS augmented prestimulus ?1- and ?-oscillations, leading to opposing effects on subsequent pain-related neural and behavioral activities. This dual antagonistic effect arises from the distinct functional aspects of ?- and ?-band activities. While sensorimotor ?-tACS holds potential for pain relief through improved somatosensory ?-oscillations, its more pronounced and sustained effect may lead to hyperalgesia via modulation of midfrontal ?-oscillations, selectively in certain contexts. This discovery sheds light on the intricate relationship between cortical oscillations and pain anticipation/perception, offering insights for refining tACS systems for pain relief. Future studies could develop dual-target neuromodulatory interventions that focus on enhancing sensorimotor ?-oscillations and also consider the potential modulation of ?-oscillation activity.
References
[1] Ploner M, Sorg C, Gross J. Brain Rhythms of Pain. Trends Cogn Sci 2017;21(2):100-110.
[2] Ploner M, Gross J, Timmermann L, Pollok B, Schnitzler A. Pain suppresses spontaneous brain rhythms. Cereb Cortex 2006;16(4):537-540.
[3] Babiloni C, Brancucci A, Del Percio C, Capotosto P, Arendt-Nielsen L, Chen AC, Rossini PM. Anticipatory electroencephalography alpha rhythm predicts subjective perception of pain intensity. J Pain 2006;7(10):709-717.
[4] Hu L, Peng W, Valentini E, Zhang Z, Hu Y. Functional features of nociceptive-induced suppression of alpha band electroencephalographic oscillations. J Pain 2013;14(1):89-99.
[5] Tu Y, Zhang Z, Tan A, Peng W, Hung YS, Moayedi M, Iannetti GD, Hu L. Alpha and gamma oscillation amplitudes synergistically predict the perception of forthcoming nociceptive stimuli. Hum Brain Mapp 2016;37(2):501-514.
[6] Cabral-Calderin Y, Wilke M. Probing the Link Between Perception and Oscillations: Lessons from Transcranial Alternating Current Stimulation. Neuroscientist 2020;26(1):57-73.
[7] Herrmann CS, Rach S, Neuling T, Strüber D. Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes. Front Hum Neurosci 2013;7:279.
[8] Clancy KJ, Andrzejewski JA, You Y, Rosenberg JT, Ding M, & Li W (2022). Transcranial stimulation of alpha oscillations up-regulates the default mode network. Proceedings of the National Academy of Sciences, 119(1), e2110868119.
[9] Zaehle T, Rach S, Herrmann CS (2010). Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PloS one, 5(11), e13766.
[10] Peng W, Zhan Y, Jin R, Lou W, Li X. Aftereffects of alpha transcranial alternating current stimulation over the primary sensorimotor cortex on cortical processing of pain. Pain 2023;164(6):1280-1290.