Human brain oscillatory activity phase‐locked to painful electrical stimulations: A multi‐channel EEG study

The main aims of this study were 1) a fine spatial analysis of electroencephalographic (EEG) oscillations after galvanic painful stimulation (nonpainful stimulation as a reference) and 2) a comparative evaluation of phase‐ and nonphase‐locked component of these EEG oscillations. Preliminary surface Laplacian transformation of EEG data (31 channels) reduced head volume conductor effects. EEG phase values were computed by FFT analysis and the statistical evaluation of these values was performed by Rayleigh test (P < 0.05). About 50% of the EEG single trials presented statistically the same FFT phase value of the evoked EEG oscillations (phase‐locked single trials), indicating a preponderant phase‐locked compared to nonphase‐locked component. The remaining single trials showed random FFT phase values (nonphase‐locked single trials), indicating a preponderant nonphase‐locked compared to phase‐locked component. Compared to nonpainful stimulation, painful stimulation increased phase‐locked theta to gamma band responses in the contralateral hemisphere and decreased the phase‐locked beta band response in the ipsilateral hemisphere. Furthermore, nonphase‐locked alpha band response decreased in the ipsilateral fronto‐central area. In conclusion, both decreased and increased EEG oscillatory responses to galvanic painful stimulation would occur in parallel in different cortical regions and in the phase‐ and nonphase‐locked EEG data sets. This enriches the actual debate on the mapping of event‐related oscillatory activity of human brain. Hum. Brain Mapping 15:112–123, 2002. © 2002 Wiley‐Liss, Inc.

[1]  Barrie W. Jervis,et al.  A Fundamental Investigation of the Composition of Auditory Evoked Potentials , 1983, IEEE Transactions on Biomedical Engineering.

[2]  L. Kaufman,et al.  Modulation of Spontaneous Brain Activity during Mental Imagery , 1990, Journal of Cognitive Neuroscience.

[3]  R. Kakigi,et al.  Pain-related somatosensory evoked magnetic fields. , 1995, Electroencephalography and clinical neurophysiology.

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

[5]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[6]  B Bromm,et al.  Pre-stimulus/post-stimulus relations in EEG spectra and their modulations by an opioid and an antidepressant. , 1989, Electroencephalography and clinical neurophysiology.

[7]  B. MCA. SAVERS,et al.  The Mechanism of Auditory Evoked EEG Responses , 1974, Nature.

[8]  Andrew C. N. Chen,et al.  Topology of EEG Coherence Changes May Reflect Differential Neural Network Activation in Cold and Pain Perception , 2004, Brain Topography.

[9]  Lars Arendt-Nielsen,et al.  Laser-evoked potentials in human pain - II. Cerebral generators , 1998 .

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

[11]  A. Urbano,et al.  Improved realistic Laplacian estimate of highly-sampled EEG potentials by regularization techniques. , 1998, Electroencephalography and clinical neurophysiology.

[12]  M. Brandt,et al.  Pre-stimulus spectral EEG patterns and the visual evoked response. , 1991, Electroencephalography and clinical neurophysiology.

[13]  M. Brandt,et al.  The effect of the phase of prestimulus alpha activity on the averaged visual evoked response. , 1991, Electroencephalography and clinical neurophysiology.

[14]  Ben H. Jansen,et al.  A neurophysiologically-based mathematical model of flash visual evoked potentials , 2004, Biological Cybernetics.

[15]  M. Brandt,et al.  The relationship between prestimulus-alpha amplitude and visual evoked potential amplitude. , 1991, The International journal of neuroscience.

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

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

[18]  F Cincotti,et al.  Mapping of early and late human somatosensory evoked brain potentials to phasic galvanic painful stimulation , 2001, Human brain mapping.

[19]  J. W. Kuhlman,et al.  Functional topography of the human mu rhythm. , 1978, Electroencephalography and clinical neurophysiology.

[20]  E. Chudler,et al.  The assessment of pain by cerebral evoked potentials , 1983, Pain.

[21]  W. J. Nowack Neocortical Dynamics and Human EEG Rhythms , 1995, Neurology.

[22]  J. Lorenz,et al.  Neurophysiological evaluation of pain. , 1998, Electroencephalography and clinical neurophysiology.

[23]  Andrew C. N. Chen Human brain measures of clinical pain: a review I. Topographic mappings , 1993, Pain.

[24]  Juliana Yordanova,et al.  Analysis of phase-locking is informative for studying event-related EEG activity , 1997, Biological Cybernetics.

[25]  G Pfurtscheller,et al.  Mapping of event-related desynchronization and type of derivation. , 1988, Electroencephalography and clinical neurophysiology.

[26]  G. Pfurtscheller,et al.  Event-related synchronization of mu rhythm in the EEG over the cortical hand area in man , 1994, Neuroscience Letters.

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

[28]  A. Urbano,et al.  Spline Laplacian estimate of EEG potentials over a realistic magnetic resonance-constructed scalp surface model. , 1996, Electroencephalography and clinical neurophysiology.

[29]  F. D. Silva The Rhythmic Slow Activity (Theta) of the Limbic Cortex: An Oscillation in Search of a Function , 1992 .

[30]  W. Klimesch Brain Function and Oscillations, Vol. II: Integrative Brain Function. Neurophysiology and Cognitive Processes, edited by Erol Basar , 1999, Trends in Cognitive Sciences.

[31]  Andrew C. N. Chen,et al.  Laser-evoked potentials in human pain: I. Use and possible misuse , 1998 .

[32]  L. Arendt-Nielsen Characteristics, detection, and modulation of laser‐evoked vertex potentials , 1994, Acta anaesthesiologica Scandinavica. Supplementum.

[33]  P. Roland Cortical representation of pain , 1992, Trends in Neurosciences.

[34]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.