Changes of gamma-band oscillatory activity to tonic muscle pain

It is well know that phasic pain could induce suppression of alpha oscillations and enhancement of gamma oscillations. However, the cortical responses to tonic pain, especially tonic pain originating from deep tissue, which was proposed to better resemble the clinical pain, are not well understood. Here we aimed to investigate electroencephalographic (EEG) responses to tonic muscle pain. EEG signals and pain perceptions of three order-counterbalanced conditions: innocuous condition (A, infusion of isotonic saline), noxious conditions with low (B) and medium (C) intensities (infusion of hypertonic saline) were recorded from 43 subjects. We observed the enhancement of gamma oscillations in frontal-central region in condition C, as compared to either condition A or B. Positive relationship between the amplitude of gamma oscillations and pain intensity was also observed in frontal-central region. Therefore, we provide novel evidence for the encoding of frontal-central gamma oscillations in tonic pain processing.

[1]  M. Lindquist,et al.  An fMRI-based neurologic signature of physical pain. , 2013, The New England journal of medicine.

[2]  R. Treede,et al.  Human brain mechanisms of pain perception and regulation in health and disease , 2005, European journal of pain.

[3]  S. Makeig,et al.  Imaging human EEG dynamics using independent component analysis , 2006, Neuroscience & Biobehavioral Reviews.

[4]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[5]  S Seri,et al.  Quantitative EEG modifications during the Cold Water Pressor Test: hemispheric and hand differences. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[6]  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.

[7]  Lars Arendt-Nielsen,et al.  Different EEG topographic effects of painful and non-painful intramuscular stimulation in man , 2001, Experimental Brain Research.

[8]  J. Hsieh,et al.  Neuroimaging of Muscle Pain in Humans , 2009, Journal of the Chinese Medical Association : JCMA.

[9]  Joachim Gross,et al.  Prefrontal Gamma Oscillations Encode Tonic Pain in Humans , 2015, Cerebral cortex.

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

[11]  Edzard Ernst,et al.  Placebo Effects: Understanding the Mechanisms in Health and Disease , 2010 .

[12]  Miriam Kunz,et al.  Responses to tonic heat pain in the ongoing EEG under conditions of controlled attention , 2014, Somatosensory & motor research.

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

[14]  Christopher J James,et al.  Independent component analysis for biomedical signals , 2005, Physiological measurement.

[15]  R. Høifødt,et al.  The effect of experimenter gender on autonomic and subjective responses to pain stimuli , 2007, PAIN.

[16]  Alon Sinai,et al.  Tonic pain and continuous EEG: Prediction of subjective pain perception by alpha-1 power during stimulation and at rest , 2012, Clinical Neurophysiology.

[17]  Junshui Ma,et al.  Muscle artifacts in multichannel EEG: Characteristics and reduction , 2012, Clinical Neurophysiology.

[18]  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.

[19]  Lars Arendt-Nielsen,et al.  Dynamic changes and spatial correlation of EEG activities during cold pressor test in man , 2002, Brain Research Bulletin.

[20]  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.

[21]  S. Lautenbacher,et al.  EEG responses to tonic heat pain , 2006, Experimental Brain Research.

[22]  J. Cacioppo,et al.  Handbook of neuroscience for the behavioral sciences , 2009 .

[23]  H. Johansson,et al.  Changes in human regional cerebral blood flow following hypertonic saline induced experimental muscle pain: a positron emission tomography study , 2002, Neuroscience Letters.

[24]  J. Smith,et al.  Tonic changes in alpha power during immersion of the hand in cold water. , 1991, Electroencephalography and clinical neurophysiology.

[25]  Stephanie Schuckers,et al.  EEG indices of tonic pain-related activity in the somatosensory cortices , 2008, Clinical Neurophysiology.

[26]  Yang Tingzhong,et al.  Applicability of the Positive and Negative Affect Scale in Chinese , 2003 .

[27]  Richard J. Davidson,et al.  Validation of ICA-based myogenic artifact correction for scalp and source-localized EEG , 2010, NeuroImage.

[28]  Kemal S. Türker,et al.  Interference of tonic muscle activity on the EEG: a single motor unit study , 2014, Front. Hum. Neurosci..

[29]  Andrew C. N. Chen,et al.  Topographic brain measures of human pain and pain responsivity , 1989, Pain.

[30]  Ronald Melzack,et al.  The short-form McGill pain questionnaire , 1987, Pain.

[31]  Lars Arendt-Nielsen,et al.  Differential cerebral responses to aversive auditory arousal versus muscle pain: specific EEG patterns are associated with human pain processing , 2002, Experimental Brain Research.

[32]  C. Witton,et al.  Gamma oscillatory amplitude encodes stimulus intensity in primary somatosensory cortex , 2013, Front. Hum. Neurosci..

[33]  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.

[34]  Lars Arendt-Nielsen,et al.  Comparative EEG activation to skin pain and muscle pain induced by capsaicin injection. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  Andrew C. N. Chen,et al.  Brain and Human pain: Topographic EEG amplitude and coherence mapping , 2005, Brain Topography.

[36]  L. Arendt-Nielsen,et al.  In vivo model of muscle pain: Quantification of intramuscular chemical, electrical, and pressure changes associated with saline-induced muscle pain in humans , 1997, Pain.

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

[38]  A. J. Bell,et al.  INDEPENDENT COMPONENT ANALYSIS OF BIOMEDICAL SIGNALS , 2000 .

[39]  J. Palva,et al.  New vistas for alpha-frequency band oscillations. , 2007, Trends in neurosciences.

[40]  K. Shen,et al.  Frequency-domain EEG source analysis for acute tonic cold pain perception , 2012, Clinical Neurophysiology.

[41]  Yong Hu,et al.  Changes of Spontaneous Oscillatory Activity to Tonic Heat Pain , 2014, PloS one.

[42]  Domenica Le Pera,et al.  Long-lasting effect evoked by tonic muscle pain on parietal EEG activity in humans , 2000, Clinical Neurophysiology.

[43]  F. Prato,et al.  Measuring the neural response to continuous intramuscular infusion of hypertonic saline by perfusion MRI , 2012, Journal of magnetic resonance imaging : JMRI.

[44]  J. Ashton-Miller,et al.  A closed-loop system for maintaining constant experimental muscle pain in man , 1993, IEEE Transactions on Biomedical Engineering.

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

[46]  Thomas E. Nichols,et al.  Placebo Effects Mediated by Endogenous Opioid Activity on μ-Opioid Receptors , 2005, The Journal of Neuroscience.

[47]  J. Palva,et al.  New vistas for α-frequency band oscillations , 2007, Trends in Neurosciences.

[48]  C. Stohler,et al.  The effect of experimental muscle pain on the background electrical brain activity , 1992, Pain.

[49]  E. Whitham,et al.  Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20Hz are contaminated by EMG , 2007, Clinical Neurophysiology.

[50]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[51]  Han Ji MULTI-CENTERED LINGUISTIC ADAPTATION AND VALIDATION OF SHORT-FORM MCGILL PAIN QUESTIONNAIRE-2 , 2013 .