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Functional Features of Nociceptive-Induced Suppression of Alpha Band Electroencephalographic Oscillations

  • Li Hu
    Affiliations
    Key Laboratory of Cognition and Personality (Ministry of Education) and School of Psychology, Southwest University, Chongqing, China
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  • Weiwei Peng
    Affiliations
    Department of Orthopaedics and Traumatology, The University of Hong Kong, Pokfulam, Hong Kong, China
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  • Elia Valentini
    Affiliations
    Psychology Department, Sapienza University of Rome, Rome, Italy

    Santa Lucia Foundation, Scientific Institute for Research, Hospitalization and Health Care, Rome, Italy
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  • Zhiguo Zhang
    Affiliations
    Department of Electrical and Electronic Engineering, The University of Hong Kong, Pokfulam, Hong Kong, China
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  • Yong Hu
    Correspondence
    Address reprint requests to Dr. Yong Hu, Department of Orthopaedics and Traumatology, The University of Hong Kong, Duchess of Kent Children's Hospital, 12 Sandy Bay Road, Pokfulam, Hong Kong, China.
    Affiliations
    Department of Orthopaedics and Traumatology, The University of Hong Kong, Pokfulam, Hong Kong, China
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      Abstract

      Nociceptive stimuli can induce a transient suppression of electroencephalographic oscillations in the alpha frequency band (ie, alpha event-related desynchronization, α-ERD). Here we investigated whether α-ERD could be functionally distinguished in 2 temporally and spatially segregated subcomponents as suggested by previous studies. In addition, we tested whether the degree of dependence of nociceptive-induced α-ERD magnitude on the prestimulus α-power would have been larger than the degree of dependence on the poststimulus α-power. Our findings confirmed the dissociation between a sensory-related α-ERD maximally distributed over contralateral central electrodes, and a task-related α-ERD (possibly affected by motor-related activity), maximally distributed at posterior parietal and occipital electrodes. The cortical sources of these activities were estimated to be located at the level of sensorimotor and bilateral occipital cortices, respectively. Importantly, the time course of the α-ERD revealed that functional segregation emerged only at late latencies (400 to 750 ms) whereas topographic similarity was observed at earlier latencies (250 to 350 ms). Furthermore, the nociceptive-induced α-ERD magnitude was significantly more dependent on prestimulus than poststimulus α-power. Altogether these findings provide direct evidence that the nociceptive-induced α-ERD reflects the summation of sensory-related and task-related cortical processes, and that prestimulus fluctuations can remarkably influence the non-phase-locked nociceptive α-ERD.

      Perspective

      Present results extend the functional understanding of α-oscillation suppression during pain perception and demonstrate the influence of prestimulus variability on this cortical phenomenon. This work has the potential to guide pain clinicians in a more accurate interpretation on physiological and psychological modulations of α-oscillations.

      Key words

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      References

        • Babiloni C.
        • Brancucci A.
        • Del Percio C.
        • Capotosto P.
        • Arendt-Nielsen L.
        • Chen A.C.
        Anticipatory electroencephalography alpha rhythm predicts subjective perception of pain intensity.
        J Pain. 2006; 7: 709-717
        • Backonja M.
        • Howland E.W.
        • Wang J.
        • Smith J.
        • Salinsky M.
        • Cleeland C.S.
        Tonic changes in alpha power during immersion of the hand in cold water.
        Electroencephalogr Clin Neurophysiol. 1991; 79: 192-203
        • Bastuji H.
        • Perchet C.
        • Legrain V.
        • Montes C.
        • Garcia-Larrea L.
        Laser evoked responses to painful stimulation persist during sleep and predict subsequent arousals.
        Pain. 2008; 137: 589-599
        • Becker R.
        • Ritter P.
        • Villringer A.
        Influence of ongoing alpha rhythm on the visual evoked potential.
        Neuroimage. 2008; 39: 707-716
        • Bledowski C.
        • Prvulovic D.
        • Goebel R.
        • Zanella F.E.
        • Linden D.E.
        Attentional systems in target and distractor processing: a combined ERP and fMRI study.
        Neuroimage. 2004; 22: 530-540
        • Bledowski C.
        • Prvulovic D.
        • Hoechstetter K.
        • Scherg M.
        • Linden D.E.
        Localizing P300 generators in visual target and distractor processing: A combined event-related potential and functional magnetic resonance imaging study.
        J Neurosci. 2004; 24: 9353-9360
        • Bradley B.P.
        • Garner M.
        • Hudson L.
        • Mogg K.
        Influence of negative affect on selective attention to smoking-related cues and urge to smoke in cigarette smokers.
        Behav Pharmacol. 2007; 18: 255-263
        • Brandeis D.
        • Naylor H.
        • Halliday R.
        • Callaway E.
        • Yano L.
        Scopolamine effects on visual information processing, attention, and event-related potential map latencies.
        Psychophysiology. 1992; 29: 315-336
        • Brookes M.J.
        • Gibson A.M.
        • Hall S.D.
        • Furlong P.L.
        • Barnes G.R.
        • Hillebrand A.
        GLM-beamformer method demonstrates stationary field, alpha ERD and gamma ERS co-localisation with fMRI BOLD response in visual cortex.
        Neuroimage. 2005; 26: 302-308
        • Delorme A.
        • Makeig S.
        EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis.
        J Neurosci Methods. 2004; 134: 9-21
        • Donchin E.
        • Coles M.G.
        Is the P300 component a manifestation of context updating?.
        Behav Brain Sci. 2006; 11: 357-427
        • Dowman R.
        • Rissacher D.
        • Schuckers S.
        EEG indices of tonic pain-related activity in the somatosensory cortices.
        Clin Neurophysiol. 2008; 119: 1201-1212
        • Egsgaard L.
        • Wang L.
        • Arendt-Nielsen L.
        Volunteers with high versus low alpha EEG have different pain-EEG relationship: A human experimental study.
        Exp Brain Res. 2009; 193: 361-369
        • Fogelson N.
        • Wang X.
        • Lewis J.B.
        • Kishiyama M.M.
        • Ding M.
        • Knight R.T.
        Multimodal effects of local context on target detection: evidence from P3b.
        J Cogn Neurosci. 2009; 21: 1680-1692
        • Fox M.D.
        • Raichle M.E.
        Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging.
        Nat Rev Neurosci. 2007; 8: 700-711
        • Fries P.
        Neuronal gamma-band synchronization as a fundamental process in cortical computation.
        Annu Rev Neurosci. 2009; 32: 209-224
        • Girden E.
        ANOVA: Repeated measures.
        Sage, Newbury Park, CA1992
        • Goldman R.I.
        • Stern J.M.
        • Engel J.
        • Cohen M.S.
        Simultaneous EEG and fMRI of the alpha rhythm.
        Neuroreport. 2002; 13: 2487-2492
        • Grabner R.H.
        • Fink A.
        • Stipacek A.
        • Neuper C.
        • Neubauer A.C.
        Intelligence and working memory systems: Evidence of neural efficiency in alpha band ERD.
        Brain Res Cogn Brain Res. 2004; 20: 212-225
        • Greenblatt R.E.
        Probabilistic reconstruction of multiple sources in the bioelectromagnetic inverse problem.
        Inverse Problems. 1993; 9: 271
        • He B.
        • Dai Y.
        • Astolfi L.
        • Babiloni F.
        • Yuan H.
        • Yang L.
        eConnectome: A MATLAB toolbox for mapping and imaging of brain functional connectivity.
        J Neurosci Methods. 2011; 195: 261-269
        • Huber M.T.
        • Bartling J.
        • Pachur D.
        • Woikowsky-Biedau S.
        • Lautenbacher S.
        EEG responses to tonic heat pain.
        Exp Brain Res. 2006; 173: 14-24
        • Iannetti G.D.
        • Hughes N.P.
        • Lee M.C.
        • Mouraux A.
        Determinants of laser-evoked EEG responses: Pain perception or stimulus saliency?.
        J Neurophysiol. 2008; 100: 815-828
        • Iannetti G.D.
        • Zambreanu L.
        • Wise R.G.
        • Buchanan T.J.
        • Huggins J.P.
        • Smart T.S.
        Pharmacological modulation of pain-related brain activity during normal and central sensitization states in humans.
        Proc Natl Acad Sci U S A. 2005; 102: 18195-18200
        • Inui K.
        • Tran T.D.
        • Hoshiyama M.
        • Kakigi R.
        Preferential stimulation of Adelta fibers by intra-epidermal needle electrode in humans.
        Pain. 2002; 96: 247-252
        • Inui K.
        • Tsuji T.
        • Kakigi R.
        Temporal analysis of cortical mechanisms for pain relief by tactile stimuli in humans.
        Cereb Cortex. 2006; 16: 355-365
        • Jung T.P.
        • Makeig S.
        • Westerfield M.
        • Townsend J.
        • Courchesne E.
        • Sejnowski T.J.
        Analysis and visualization of single-trial event-related potentials.
        Hum Brain Mapp. 2001; 14: 166-185
        • Klimesch W.
        • Doppelmayr M.
        • Hanslmayr S.
        Upper alpha ERD and absolute power: Their meaning for memory performance.
        Prog Brain Res. 2006; 159: 151-165
        • Koenig T.
        • Prichep L.
        • Lehmann D.
        • Sosa P.V.
        • Braeker E.
        • Kleinlogel H.
        Millisecond by millisecond, year by year: Normative EEG microstates and developmental stages.
        Neuroimage. 2002; 16: 41-48
        • Kolev V.
        • Yordanova J.
        • Schurmann M.
        • Basar E.
        Increased frontal phase-locking of event-related alpha oscillations during task processing.
        Int J Psychophysiol. 2001; 39: 159-165
        • Lange J.
        • Halacz J.
        • van Dijk H.
        • Kahlbrock N.
        • Schnitzler A.
        Fluctuations of prestimulus oscillatory power predict subjective perception of tactile simultaneity.
        Cereb Cortex. 2012; 22: 2564-2574
        • Laufs H.
        • Kleinschmidt A.
        • Beyerle A.
        • Eger E.
        • Salek-Haddadi A.
        • Preibisch C.
        EEG-correlated fMRI of human alpha activity.
        Neuroimage. 2003; 19: 1463-1476
        • Laufs H.
        • Krakow K.
        • Sterzer P.
        • Eger E.
        • Beyerle A.
        • Salek-Haddadi A.
        Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest.
        Proc Natl Acad Sci U S A. 2003; 100: 11053-11058
        • Legrain V.
        • Guerit J.M.
        • Bruyer R.
        • Plaghki L.
        Attentional modulation of the nociceptive processing into the human brain: Selective spatial attention, probability of stimulus occurrence, and target detection effects on laser evoked potentials.
        Pain. 2002; 99: 21-39
        • Legrain V.
        • Van Damme S.
        • Eccleston C.
        • Davis K.D.
        • Seminowicz D.A.
        • Crombez G.
        A neurocognitive model of attention to pain: Behavioral and neuroimaging evidence.
        Pain. 2009; 144: 230-232
        • Lehmann D.
        • Skrandies W.
        Reference-free identification of components of checkerboard-evoked multichannel potential fields.
        Electroencephalogr Clin Neurophysiol. 1980; 48: 609-621
        • Makeig S.
        • Jung T.
        • Bell A.
        • Ghahremani D.
        • Sejnowski T.
        Blind separation of auditory event-related brain responses into independent components.
        Proc Natl Acad Sci U S A. 1997; 94: 10979-10984
        • Martinovic J.
        • Busch N.
        High frequency oscillations as a correlate of visual perception.
        Int J Psychophysiol. 2011; 79: 32-38
        • May E.S.
        • Butz M.
        • Kahlbrock N.
        • Hoogenboom N.
        • Brenner M.
        • Schnitzler A.
        Pre- and post-stimulus alpha activity shows differential modulation with spatial attention during the processing of pain.
        Neuroimage. 2012; 62: 1965-1974
        • Michel C.M.
        • Murray M.M.
        • Lantz G.
        • Gonzalez S.
        • Spinelli L.
        • Grave de Peralta R.
        EEG source imaging.
        Clin Neurophysiol. 2004; 115: 2195-2222
        • Mitsis G.D.
        • Iannetti G.D.
        • Smart T.S.
        • Tracey I.
        • Wise R.G.
        Regions of interest analysis in pharmacological fMRI: How do the definition criteria influence the inferred result?.
        Neuroimage. 2008; 40: 121-132
        • Moosmann M.
        • Ritter P.
        • Krastel I.
        • Brink A.
        • Thees S.
        • Blankenburg F.
        Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy.
        Neuroimage. 2003; 20: 145-158
        • Mouraux A.
        • Guérit J.
        • Plaghki L.
        Non-phase locked electroencephalogram (EEG) responses to CO2 laser skin stimulations may reflect central interactions between a partial partial differential- and C-fibre afferent volleys.
        Clin Neurophysiol. 2003; 114: 710-722
        • Mouraux A.
        • Iannetti G.
        • Plaghki L.
        Low intensity intra-epidermal electrical stimulation can activate Adelta-nociceptors selectively.
        Pain. 2010; 150: 199-207
        • Mouraux A.
        • Iannetti G.D.
        Across-trial averaging of event-related EEG responses and beyond.
        Magn Reson Imaging. 2008; 26: 1041-1054
        • Mu Y.
        • Fan Y.
        • Mao L.
        • Han S.
        Event-related theta and alpha oscillations mediate empathy for pain.
        Brain Res. 2008; 1234: 128-136
        • Murray M.M.
        • Michel C.M.
        • Grave de Peralta R.
        • Ortigue S.
        • Brunet D.
        • Gonzalez Andino S.
        Rapid discrimination of visual and multisensory memories revealed by electrical neuroimaging.
        Neuroimage. 2004; 21: 125-135
        • Neuper C.
        • Pfurtscheller G.
        Event-related dynamics of cortical rhythms: Frequency-specific features and functional correlates.
        Int J Psychophysiol. 2001; 43: 41-58
        • Nir R.
        • 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.
        Clin Neurophysiol. 2011; 123: 605-612
        • Nir R.
        • Sinai A.
        • Raz E.
        • Sprecher E.
        • Yarnitsky D.
        Pain assessment by continuous EEG: Association between subjective perception of tonic pain and peak frequency of alpha oscillations during stimulation and at rest.
        Brain Res. 2010; 1344: 77-86
        • Ohara S.
        • Crone N.E.
        • Weiss N.
        • Lenz F.A.
        Attention to a painful cutaneous laser stimulus modulates electrocorticographic event-related desynchronization in humans.
        Clin Neurophysiol. 2004; 115: 1641-1652
        • Peng W.W.
        • Hu L.
        • Zhang Z.G.
        • Hu Y.
        Causality in the Association between P300 and alpha event-related desynchronization.
        PLoS ONE. 2012; 7: e34163
        • Pfurtscheller G.
        • Aranibar A.
        Event-related cortical desynchronization detected by power measurements of scalp EEG.
        Electroencephalogr Clin Neurophysiol. 1977; 42: 817-826
        • Pfurtscheller G.
        • Lopes da Silva F.H.
        Event-related EEG/MEG synchronization and desynchronization: Basic principles.
        Clin Neurophysiol. 1999; 110: 1842-1857
        • Ploner M.
        • Gross J.
        • Timmermann L.
        • Pollok B.
        • Schnitzler A.
        Oscillatory activity reflects the excitability of the human somatosensory system.
        Neuroimage. 2006; 32: 1231-1236
        • Ploner M.
        • Gross J.
        • Timmermann L.
        • Pollok B.
        • Schnitzler A.
        Pain suppresses spontaneous brain rhythms.
        Cereb Cortex. 2006; 16: 537-540
        • Polich J.
        Updating P300: An integrative theory of P3a and P3b.
        Clin Neurophysiol. 2007; 118: 2128-2148
        • Raij T.T.
        • Forss N.
        • Stancak A.
        • Hari R.
        Modulation of motor-cortex oscillatory activity by painful Adelta- and C-fiber stimuli.
        Neuroimage. 2004; 23: 569-573
        • Rogan J.C.
        • Keselman H.J.
        • Mendoza J.L.
        Analysis of repeated measurements.
        Br J Math Stat Psychol. 1979; 32: 269-286
        • Romei V.
        • Brodbeck V.
        • Michel C.
        • Amedi A.
        • Pascual-Leone A.
        • Thut G.
        Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas.
        Cereb Cortex. 2008; 18: 2010-2018
        • Sawaki R.
        • Katayama J.
        Stimulus context determines whether nontarget stimuli are processed as task-relevant or distractor information.
        Clin Neurophysiol. 2006; 117: 2532-2539
        • Tallon-Baudry C.
        • Bertrand O.
        • Delpuech C.
        • Permier J.
        Oscillatory gamma-band (30-70 Hz) activity induced by a visual search task in humans.
        J Neurosci. 1997; 17: 722-734
        • Valentini E.
        • Betti V.
        • Hu L.
        • Aglioti S.M.
        Hypnotic modulation of pain perception and of brain activity triggered by nociceptive laser stimuli.
        Cortex. 2012;
        • Van Winsum W.
        • Sergeant J.
        • Geuze R.
        The functional significance of event-related desynchronization of alpha rhythm in attentional and activating tasks.
        Electroencephalogr Clin Neurophysiol. 1984; 58: 519-524
        • Vazouras C.
        EEG source distribution localization using minimum-product and CRESO criteria for Tikhonov regularization.
        Conf Proc IEEE Eng Med Biol Soc. 2004; 6: 4457-4460
        • Yordanova J.
        • Kolev V.
        Event-related alpha oscillations are functionally associated with P300 during information processing.
        Neuroreport. 1998; 9: 3159-3164
        • Yordanova J.
        • Kolev V.
        • Polich J.
        P300 and alpha event-related desynchronization (ERD).
        Psychophysiology. 2001; 38: 143-152
        • Zhang Z.G.
        • Hu L.
        • Hung Y.S.
        • Mouraux A.
        • Iannetti G.D.
        Gamma-band oscillations in the primary somatosensory cortex - a direct and obligatory correlate of subjective pain intensity.
        J Neurosci. 2012; 32: 7429-7438