Adult; Alpha Rhythm/physiology; Analysis of Variance; Female; Habituation, Psychophysiologic; Humans; Male; Thermosensing/physiology; Time Factors; Young Adult; Cold Temperature; Electroencephalography; Hot Temperature; Perception; Signal Processing, Computer-Assisted; Alpha Rhythm; Thermosensing; Biochemistry, Genetics and Molecular Biology (all); Agricultural and Biological Sciences (all); Multidisciplinary
Abstract :
[en] Thermosensation is crucial for humans to probe the environment and detect threats arising from noxious heat or cold. Over the last years, EEG frequency-tagging using long-lasting periodic radiant heat stimulation has been proposed as a means to study the cortical processes underlying tonic heat perception. This approach is based on the notion that periodic modulation of a sustained stimulus can elicit synchronized periodic activity in the neuronal populations responding to the stimulus, known as a steady-state response (SSR). In this paper, we extend this approach using a contact thermode to generate both heat- and cold-evoked SSRs. Furthermore, we characterize the temporal dynamics of the elicited responses, relate these dynamics to perception, and assess the effects of displacing the stimulated skin surface to gain insight on the heat- and cold-sensitive afferents conveying these responses. Two experiments were conducted in healthy volunteers. In both experiments, noxious heat and innocuous cool stimuli were applied during 75 seconds to the forearm using a Peltier-based contact thermode, with intensities varying sinusoidally at 0.2 Hz. Displacement of the thermal stimulation on the skin surface was achieved by independently controlling the Peltier elements of the thermal probe. Continuous intensity ratings to sustained heat and cold stimulation were obtained in the first experiment with 14 subjects, and the EEG was recorded in the second experiment on 15 subjects. Both contact heat and cool stimulation elicited periodic EEG responses and percepts. Compared to heat stimulation, the responses to cool stimulation had a lower magnitude and shorter latency. All responses tended to habituate along time, and this response attenuation was most pronounced for cool compared to warm stimulation, and for stimulation delivered using a fixed surface compared to a variable surface.
Disciplines :
Neurology
Author, co-author :
Mulders, Dounia ; ICTEAM institute, Université Catholique de Louvain, Louvain-la-Neuve, Belgium ; IONS institute, Université Catholique de Louvain, Brussels, Belgium
de Bodt, Cyril; ICTEAM institute, Université Catholique de Louvain, Louvain-la-Neuve, Belgium
Lejeune, Nicolas ; Université de Liège - ULiège > GIGA > GIGA Consciousness - Coma Science Group ; IONS institute, Université Catholique de Louvain, Brussels, Belgium
Courtin, Arthur ; IONS institute, Université Catholique de Louvain, Brussels, Belgium
Liberati, Giulia ; IONS institute, Université Catholique de Louvain, Brussels, Belgium
Verleysen, Michel; ICTEAM institute, Université Catholique de Louvain, Louvain-la-Neuve, Belgium
Mouraux, André; IONS institute, Université Catholique de Louvain, Brussels, Belgium
Language :
English
Title :
Dynamics of the perception and EEG signals triggered by tonic warm and cool stimulation.
DM, CdB and NL are Research Fellows of the Fonds de la Recherche Scientique - FNRS (https://www.frs-fnrs.be/fr/). AC is supported by a FRIA doctoral grant from the FNRS. GL is a FNRS researcher. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Meyer RA, Campbell JN. Evidence for two distinct classes of unmyelinated nociceptive afferents in monkey. Brain research. 1981; 224(1):149-152. https://doi.org/10.1016/0006-8993(81)91124-0 PMID: 7284829
Dubin AE, Patapoutian A. Nociceptors: the sensors of the pain pathway. The Journal of clinical investigation. 2010; 120(11):3760-3772. https://doi.org/10.1172/JCI42843 PMID: 21041958
Wooten M, Weng HJ, Hartke TV, Borzan J, Klein AH, Turnquist B, et al. Three functionally distinct classes of C-fibre nociceptors in primates. Nature communications. 2014; 5:4122. https://doi.org/10.1038/ ncomms5122 PMID: 24947823
Serra J, Campero M, Ochoa J, Bostock H. Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin. The Journal of physiology. 1999; 515(3):799-811. https://doi.org/10.1111/j.1469-7793.1999.799ab.x PMID: 10066906
Campero M, Serra J, Bostock H, Ochoa J. Partial reversal of conduction slowing during repetitive stimulation of single sympathetic efferents in human skin. Acta physiologica scandinavica. 2004; 182(3):305-311. https://doi.org/10.1111/j.1365-201X.2004.01357.x PMID: 15491409
Cruccu G, Aminoff M, Curio G, Guerit J, Kakigi R, Mauguiere F, et al. Recommendations for the clinical use of somatosensory-evoked potentials. Clinical neurophysiology. 2008; 119(8):1705-1719. https:// doi.org/10.1016/j.clinph.2008.03.016 PMID: 18486546
Nahra H, Plaghki L. The effects of A-fiber pressure block on perception and neurophysiological correlates of brief non-painful and painful CO2 laser stimuli in humans. European Journal of Pain. 2003; 7 (2):189-199. https://doi.org/10.1016/S1090-3801(02)00099-X PMID: 12600801
Bromm B, Treede RD. Human cerebral potentials evoked by CO2 laser stimuli causing pain. Experimental brain research. 1987; 67(1):153-162. https://doi.org/10.1007/bf00269463 PMID: 3622675
Plaghki L, Mouraux A. EEG and laser stimulation as tools for pain research. Curr Opin Investig Drugs. 2005; 6(1):58-64. PMID: 15675604
Legrain V, Iannetti GD, Plaghki L, Mouraux A. The pain matrix reloaded: a salience detection system for the body. Progress in neurobiology. 2011; 93(1):111-124. https://doi.org/10.1016/j.pneurobio.2010.10. 005 PMID: 21040755
Jankovski A, Plaghki L, Mouraux A. Reliable EEG responses to the selective activation of C-fibre afferents using a temperature-controlled infrared laser stimulator in conjunction with an adaptive staircase algorithm. PAIN®. 2013; 154(9):1578-1587.
Hüllemann P, Nerdal A, Binder A, Helfert S, Reimer M, Baron R. Cold-evoked potentials-Ready for clinical use? European Journal of Pain. 2016; 20(10):1730-1740. https://doi.org/10.1002/ejp.896 PMID: 27263529
De Keyser R, van den Broeke EN, Courtin A, Dufour A, Mouraux A. Event-related brain potentials elicited by high-speed cooling of the skin: A robust and non-painful method to assess the spinothalamic system in humans. Clinical Neurophysiology. 2018; 129(5):1011-1019. https://doi.org/10.1016/j.clinph. 2018.02.123 PMID: 29567583
Leone C, Dufour A, Di GS, Fasolino A, Di AL, La SC, et al. Cooling the skin for assessing small-fibre function. Pain. 2019;. https://doi.org/10.1097/j.pain.0000000000001584 PMID: 30985621
Becerra LR, Breiter HC, Stojanovic M, Fishman S, Edwards A, Comite AR, et al. Human brain activation under controlled thermal stimulation and habituation to noxious heat: an fMRI study. Magnetic Resonance in Medicine: An Official Journal of the International Society for Magnetic Resonance in Medicine. 1999; 41(5):1044-1057. https://doi.org/10.1002/(SICI)1522-2594(199905)41:5%3C1044::AIDMRM25% 3E3.0.CO;2-M
Segerdahl AR, Mezue M, Okell TW, Farrar JT, Tracey I. The dorsal posterior insula subserves a fundamental role in human pain. Nature neuroscience. 2015; 18(4):499. https://doi.org/10.1038/nn.3969 PMID: 25751532
Freund W, Klug R, Weber F, Stuber G, Schmitz B, Wunderlich A. Perception and suppression of thermally induced pain: a fMRI study. Somatosensory & motor research. 2009; 26(1):1-10. https://doi.org/ 10.1080/08990220902738243
Derbyshire S, Jones A. Cerebral responses to a continual tonic pain stimulus measured using positron emission tomography. Pain. 1998; 76(1-2):127-135. https://doi.org/10.1016/s0304-3959(98)00034-7 PMID: 9696465
Dowman R, Rissacher D, Schuckers S. EEG indices of tonic pain-related activity in the somatosensory cortices. Clinical Neurophysiology. 2008; 119(5):1201-1212. https://doi.org/10.1016/j.clinph.2008.01. 019 PMID: 18337168
Schulz E, May ES, Postorino M, Tiemann L, Nickel MM, Witkovsky V, et al. Prefrontal gamma oscillations encode tonic pain in humans. Cerebral cortex. 2015; 25(11):4407-4414. https://doi.org/10.1093/ cercor/bhv043 PMID: 25754338
Peng W, Hu L, Zhang Z, Hu Y. Changes of spontaneous oscillatory activity to tonic heat pain. PLoS One. 2014; 9(3):e91052. https://doi.org/10.1371/journal.pone.0091052 PMID: 24603703
Nir RR, Sinai A, Moont R, Harari E, Yarnitsky D. Tonic pain and continuous EEG: prediction of subjective pain perception by alpha-1 power during stimulation and at rest. Clinical Neurophysiology. 2012; 123(3):605-612. https://doi.org/10.1016/j.clinph.2011.08.006 PMID: 21889398
Baliki MN, Chialvo DR, Geha PY, Levy RM, Harden RN, Parrish TB, et al. Chronic pain and the emotional brain: specific brain activity associated with spontaneous fluctuations of intensity of chronic back pain. Journal of Neuroscience. 2006; 26(47):12165-12173. https://doi.org/10.1523/JNEUROSCI.3576-06.2006 PMID: 17122041
Colon E, Liberati G, Mouraux A. EEG frequency tagging using ultra-slow periodic heat stimulation of the skin reveals cortical activity specifically related to C fiber thermonociceptors. Neuroimage. 2017; 146:266-274. https://doi.org/10.1016/j.neuroimage.2016.11.045 PMID: 27871921
Colon E, Legrain V, Mouraux A. EEG frequency tagging to dissociate the cortical responses to nociceptive and nonnociceptive stimuli. Journal of cognitive neuroscience. 2014; 26(10):2262-2274. https://doi. org/10.1162/jocn_a_00648 PMID: 24738772
Mouraux A, Iannetti GD, Colon E, Nozaradan S, Legrain V, Plaghki L. Nociceptive steady-state evoked potentials elicited by rapid periodic thermal stimulation of cutaneous nociceptors. Journal of Neuroscience. 2011; 31(16):6079-6087. https://doi.org/10.1523/JNEUROSCI.3977-10.2011 PMID: 21508233
Nozaradan S, Mouraux A, Cousineau M. Frequency tagging to track the neural processing of contrast in fast, continuous sound sequences. Journal of neurophysiology. 2017; 118(1):243-253. https://doi. org/10.1152/jn.00971.2016 PMID: 28381494
Zoefel B, Ten Oever S, Sack AT. The involvement of endogenous neural oscillations in the processing of rhythmic input: More than a regular repetition of evoked neural responses. Frontiers in neuroscience. 2018; 12:95. https://doi.org/10.3389/fnins.2018.00095 PMID: 29563860
Baumgärtner U, Greffrath W, Treede RD. Contact heat and cold, mechanical, electrical and chemical stimuli to elicit small fiber-evoked potentials: merits and limitations for basic science and clinical use. Neurophysiologie Clinique/Clinical Neurophysiology. 2012; 42(5):267-280. https://doi.org/10.1016/j. neucli.2012.06.002 PMID: 23040698
Greffrath W, Baumgärtner U, Treede RD. Peripheral and central components of habituation of heat pain perception and evoked potentials in humans. Pain. 2007; 132(3):301-311. https://doi.org/10.1016/j. pain.2007.04.026 PMID: 17533117
Smith BW, Tooley EM, Montague EQ, Robinson AE, Cosper CJ, Mullins PG. Habituation and sensitization to heat and cold pain in women with fibromyalgia and healthy controls. Pain. 2008; 140(3):420-428. https://doi.org/10.1016/j.pain.2008.09.018 PMID: 18947923
Li J, Simone DA, Larson AA. Windup leads to characteristics of central sensitization. Pain. 1999; 79 (1):75-82. https://doi.org/10.1016/s0304-3959(98)00154-7 PMID: 9928779
Petre B, Tetreault P, Mathur V, Schurgin M, Chiao J, Huang L, et al. A central mechanism enhances pain perception of noxious thermal stimulus changes. Scientific reports. 2017; 7(1):1-14. https://doi. org/10.1038/s41598-017-04009-9
Huynh H, Feldt LS. Estimation of the Box correction for degrees of freedom from sample data in randomized block and split-plot designs. Journal of educational statistics. 1976; 1(1):69-82. https://doi.org/ 10.3102/10769986001001069
Mauchly JW. Significance test for sphericity of a normal n-variate distribution. The Annals of Mathematical Statistics. 1940; 11(2):204-209. https://doi.org/10.1214/aoms/1177731915
Kleinböhl D, Trojan J, Konrad C, Hölzl R. Sensitization and habituation of AMH and C-fiber related percepts of repetitive radiant heat stimulation. Clinical neurophysiology. 2006; 117(1):118-130. https://doi. org/10.1016/j.clinph.2005.08.023 PMID: 16256426
Mancini F, Pepe A, Bernacchia A, Di Stefano G, Mouraux A, Iannetti GD. Characterizing the short-term habituation of event-related evoked potentials. eNeuro. 2018; 5(5). https://doi.org/10.1523/ENEURO. 0014-18.2018 PMID: 30280121
Mouraux A, Iannetti GD. Across-trial averaging of event-related EEG responses and beyond. Magnetic resonance imaging. 2008; 26(7):1041-1054. https://doi.org/10.1016/j.mri.2008.01.011 PMID: 18479877
Bell AJ, Sejnowski TJ. An information-maximization approach to blind separation and blind deconvolution. Neural computation. 1995; 7(6):1129-1159. https://doi.org/10.1162/neco.1995.7.6.1129 PMID: 7584893
Artoni F, Delorme A, Makeig S. Applying dimension reduction to EEG data by Principal Component Analysis reduces the quality of its subsequent Independent Component decomposition. NeuroImage. 2018; 175:176-187. https://doi.org/10.1016/j.neuroimage.2018.03.016 PMID: 29526744
Chemin B, Huang G, Mulders D, Mouraux A. EEG time-warping to study non-strictly-periodic EEG signals related to the production of rhythmic movements. Journal of neuroscience methods. 2018; 308:106-115. https://doi.org/10.1016/j.jneumeth.2018.07.016 PMID: 30053483
Bach M, Meigen T. Do's and don'ts in Fourier analysis of steady-state potentials. Documenta Ophthalmologica. 1999; 99(1):69-82. https://doi.org/10.1023/a:1002648202420 PMID: 10947010
Tognola G, Grandori F, Ravazzani P. Wavelet analysis of click-evoked otoacoustic emissions. IEEE transactions on biomedical engineering. 1998; 45(6):686-697. https://doi.org/10.1109/10.678603 PMID: 9609934
Vialatte FB, Bakardjian H, Prasad R, Cichocki A. EEG paroxysmal gamma waves during Bhramari Pranayama: a yoga breathing technique. Consciousness and cognition. 2009; 18(4):977-988. https://doi. org/10.1016/j.concog.2008.01.004 PMID: 18299208
Hu L, Zhang Z, Hung Y, Luk K, Iannetti G, Hu Y. Single-trial detection of somatosensory evoked potentials by probabilistic independent component analysis and wavelet filtering. Clinical Neurophysiology. 2011; 122(7):1429-1439. https://doi.org/10.1016/j.clinph.2010.12.052 PMID: 21296019
Hu L, Mouraux A, Hu Y, Iannetti GD. A novel approach for enhancing the signal-to-noise ratio and detecting automatically event-related potentials (ERPs) in single trials. Neuroimage. 2010; 50(1):99-111. https://doi.org/10.1016/j.neuroimage.2009.12.010 PMID: 20004255
Hülsdünker T, Strüder HK, Mierau A. The pre-stimulus oscillatory alpha phase affects neural correlates of early visual perception. Neuroscience letters. 2018; 685:90-95. https://doi.org/10.1016/j.neulet. 2018.08.020 PMID: 30130554
Liberati G, Algoet M, Santos SF, Ribeiro-Vaz JG, Raftopoulos C, Mouraux A. Tonic thermonociceptive stimulation selectively modulates ongoing neural oscillations in the human posterior insula: Evidence from intracerebral EEG. NeuroImage. 2019; 188:70-83. https://doi.org/10.1016/j.neuroimage.2018.11. 059 PMID: 30529399
Haykin S. Communication Systems. Wiley; 2004.
McCoy ES, Taylor-Blake B, Street SE, Pribisko AL, Zheng J, Zylka MJ. Peptidergic CGRPα primary sensory neurons encode heat and itch and tonically suppress sensitivity to cold. Neuron. 2013; 78 (1):138-151. https://doi.org/10.1016/j.neuron.2013.01.030 PMID: 23523592
Norcia AM, Appelbaum LG, Ales JM, Cottereau BR, Rossion B. The steady-state visual evoked potential in vision research: a review. Journal of vision. 2015; 15(6):4-4. https://doi.org/10.1167/15.6.4 PMID: 26024451
Nozaradan S. Exploring how musical rhythm entrains brain activity with electroencephalogram frequency- tagging. Philosophical Transactions of the Royal Society B: Biological Sciences. 2014; 369 (1658):20130393. https://doi.org/10.1098/rstb.2013.0393
Adriaensen H, Gybels J, Handwerker H, Van Hees J. Suppression of C-fibre discharges upon repeated heat stimulation may explain characteristics of concomitant pain sensations. Brain research. 1984; 302 (2):203-211. https://doi.org/10.1016/0006-8993(84)90232-4 PMID: 6733511
Dyck PJ, Zimmerman I, Gillen D, Johnson D, Karnes J, O'brien P. Cool, warm, and heat-pain detection thresholds: testing methods and inferences about anatomic distribution of receptors. Neurology. 1993; 43(8):1500-1500. https://doi.org/10.1212/wnl.43.8.1500 PMID: 8351002
Darian-Smith I, Johnson KO, Dykes R. "Cold" fiber population innervating palmar and digital skin of the monkey: responses to cooling pulses. Journal of Neurophysiology. 1973; 36(2):325-346. https://doi. org/10.1152/jn.1973.36.2.325 PMID: 4196271
Giehl J, Meyer-Brandis G, Kunz M, Lautenbacher S. Responses to tonic heat pain in the ongoing EEG under conditions of controlled attention. Somatosensory & motor research. 2014; 31(1):40-48. https:// doi.org/10.3109/08990220.2013.837045
Ploner M, Sorg C, Gross J. Brain Rhythms of Pain. Trends in Cognitive Sciences. 2016;. https://doi.org/ 10.1016/j.tics.2016.12.001 PMID: 28025007
Jun JH, Park JR, Kim SP, Bae YM, Park JY, Kim HS, et al. Laser-induced thermoelastic effects can evoke tactile sensations. Scientific reports. 2015; 5:11016. https://doi.org/10.1038/srep11016 PMID: 26047142
Pfurtscheller G, Da Silva FL. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clinical neurophysiology. 1999; 110(11):1842-1857. https://doi.org/10.1016/s1388-2457 (99)00141-8 PMID: 10576479
Hu L, Peng W, Valentini E, Zhang Z, Hu Y. Functional features of nociceptive-induced suppression of alpha band electroencephalographic oscillations. The Journal of Pain. 2013; 14(1):89-99. https://doi. org/10.1016/j.jpain.2012.10.008 PMID: 23273836
Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. European journal of pain. 2005; 9(4):463-463. https://doi.org/10.1016/ j.ejpain.2004.11.001 PMID: 15979027
Owen DG, Clarke CF, Ganapathy S, Prato FS, Lawrence KSS. Using perfusion MRI to measure the dynamic changes in neural activation associated with tonic muscular pain. PAIN®. 2010; 148(3):375-386.
