Single-trial time–frequency analysis of electrocortical signals: Baseline correction and beyond

Event-related desynchronization (ERD) and synchronization (ERS) of electrocortical signals (e.g., electroencephalogram [EEG] and magnetoencephalogram) reflect important aspects of sensory, motor, and cognitive cortical processing. The detection of ERD and ERS relies on time-frequency decomposition of single-trial electrocortical signals, to identify significant stimulus-induced changes in power within specific frequency bands. Typically, these changes are quantified by expressing post-stimulus EEG power as a percentage of change relative to pre-stimulus EEG power. However, expressing post-stimulus EEG power relative to pre-stimulus EEG power entails two important and surprisingly neglected issues. First, it can introduce a significant bias in the estimation of ERD/ERS magnitude. Second, it confuses the contribution of pre- and post-stimulus EEG power. Taking the human electrocortical responses elicited by transient nociceptive stimuli as an example, we demonstrate that expressing ERD/ERS as the average percentage of change calculated at single-trial level introduces a positive bias, resulting in an overestimation of ERS and an underestimation of ERD. This bias can be avoided using a single-trial baseline subtraction approach. Furthermore, given that the variability in ERD/ERS is not only dependent on the variability in post-stimulus power but also on the variability in pre-stimulus power, an estimation of the respective contribution of pre- and post-stimulus EEG variability is needed. This can be achieved using a multivariate linear regression (MVLR) model, which could be optimally estimated using partial least square (PLS) regression, to dissect and quantify the relationship between behavioral variables and pre- and post-stimulus EEG activities. In summary, combining single-trial baseline subtraction approach with PLS regression can be used to achieve a correct detection and quantification of ERD/ERS.

[1]  Marina Schmid,et al.  An Introduction To The Event Related Potential Technique , 2016 .

[2]  C. Jun,et al.  Performance of some variable selection methods when multicollinearity is present , 2005 .

[3]  G. Pfurtscheller,et al.  Event-related cortical desynchronization detected by power measurements of scalp EEG. , 1977, Electroencephalography and clinical neurophysiology.

[4]  S. Kay Fundamentals of statistical signal processing: estimation theory , 1993 .

[5]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[6]  Claudia Plant,et al.  Decoding an individual's sensitivity to pain from the multivariate analysis of EEG data. , 2012, Cerebral cortex.

[7]  J. Schoffelen,et al.  Prestimulus Oscillatory Activity in the Alpha Band Predicts Visual Discrimination Ability , 2008, The Journal of Neuroscience.

[8]  I. Tracey,et al.  Similar nociceptive afferents mediate psychophysical and electrophysiological responses to heat stimulation of glabrous and hairy skin in humans , 2006, The Journal of physiology.

[9]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[10]  S Makeig,et al.  Blind separation of auditory event-related brain responses into independent components. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[11]  S. Wold,et al.  PLS-regression: a basic tool of chemometrics , 2001 .

[12]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[13]  Hervé Abdi,et al.  Partial least squares methods: partial least squares correlation and partial least square regression. , 2013, Methods in molecular biology.

[14]  A Mouraux,et al.  Across-trial averaging of event-related EEG responses and beyond. , 2008, Magnetic resonance imaging.

[15]  A. Schnitzler,et al.  Normal and pathological oscillatory communication in the brain , 2005, Nature Reviews Neuroscience.

[16]  N. Crone,et al.  Attention to a painful cutaneous laser stimulus modulates electrocorticographic event-related desynchronization in humans , 2004, Clinical Neurophysiology.

[17]  S. Luck An Introduction to the Event-Related Potential Technique , 2005 .

[18]  A. Schnitzler,et al.  Pain Suppresses Spontaneous Brain Rhythms , 2006 .

[19]  A. Kleinschmidt,et al.  Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Gian Domenico Iannetti,et al.  Laser guns and hot plates , 2005, Pain.

[21]  A. Stancák,et al.  Desynchronization of cortical rhythms following cutaneous stimulation: effects of stimulus repetition and intensity, and of the size of corpus callosum , 2003, Clinical Neurophysiology.

[22]  Joachim Gross,et al.  Neurophysiological coding of traits and states in the perception of pain. , 2011, Cerebral cortex.

[23]  Li Hu,et al.  A time-varying source connectivity approach to reveal human somatosensory information processing , 2012, NeuroImage.

[24]  Jaroslaw Zygierewicz,et al.  On the statistical significance of event-related EEG desynchronization and synchronization in the time-frequency plane , 2004, IEEE Transactions on Biomedical Engineering.

[25]  A. Mouraux,et al.  Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? , 2008, Journal of neurophysiology.

[26]  Claudio Del Percio,et al.  Distraction affects frontal alpha rhythms related to expectancy of pain: An EEG study , 2006, NeuroImage.

[27]  T. Sejnowski,et al.  Analysis and visualization of single‐trial event‐related potentials , 2001, Human brain mapping.

[28]  C. Büchel,et al.  Functional Dissociation of Ongoing Oscillatory Brain States , 2012, PloS one.

[29]  James H. Torrie,et al.  Principles and procedures of statistics: a biometrical approach (2nd ed) , 1980 .

[30]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[31]  Viktor Witkovsky,et al.  S171 GAMMA OSCILLATIONS ARE INVOLVED IN THE SENSORIMOTOR TRANSFORMATION OF PAIN , 2011 .

[32]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[34]  G Pfurtscheller,et al.  Event-related beta synchronization after wrist, finger and thumb movement. , 1998, Electroencephalography and clinical neurophysiology.

[35]  G. Pfurtscheller Event-related synchronization (ERS): an electrophysiological correlate of cortical areas at rest. , 1992, Electroencephalography and clinical neurophysiology.

[36]  Lihua Mao,et al.  Event-related theta and alpha oscillations mediate empathy for pain , 2008, Brain Research.

[37]  Arnaud Delorme,et al.  Single-Trial Normalization for Event-Related Spectral Decomposition Reduces Sensitivity to Noisy Trials , 2011, Front. Psychology.

[38]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[39]  A. Mouraux,et al.  Gamma-Band Oscillations in the Primary Somatosensory Cortex—A Direct and Obligatory Correlate of Subjective Pain Intensity , 2012, The Journal of Neuroscience.

[40]  C. Tallon-Baudry,et al.  How Ongoing Fluctuations in Human Visual Cortex Predict Perceptual Awareness: Baseline Shift versus Decision Bias , 2009, The Journal of Neuroscience.

[41]  Lars Arendt-Nielsen,et al.  Anticipatory electroencephalography alpha rhythm predicts subjective perception of pain intensity. , 2006, The journal of pain : official journal of the American Pain Society.

[42]  S. Makeig Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. , 1993, Electroencephalography and clinical neurophysiology.

[43]  Yong Hu,et al.  Functional features of nociceptive-induced suppression of alpha band electroencephalographic oscillations. , 2013, The journal of pain : official journal of the American Pain Society.

[44]  A Mouraux,et al.  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. , 2003, Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology.

[45]  Yong Hu,et al.  Causality in the Association between P300 and Alpha Event-Related Desynchronization , 2012, PloS one.

[46]  Joachim Gross,et al.  Gamma Oscillations in Human Primary Somatosensory Cortex Reflect Pain Perception , 2007, PLoS biology.

[47]  A Mouraux,et al.  Non-phase locked electroencephalogram (EEG) responses to CO2 laser skin stimulations may reflect central interactions between A∂- and C-fibre afferent volleys , 2003, Clinical Neurophysiology.

[48]  Arne D. Ekstrom,et al.  Prestimulus theta activity predicts correct source memory retrieval , 2011, Proceedings of the National Academy of Sciences.

[49]  C. Neuper,et al.  Event-related dynamics of brain oscillations , 2006 .