Human brain oscillatory activity phase-locked to painful electrical stimulations: a multi-channel EEG study

Abstract

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.

Figure 1

Raster and histogram graphs illustrating the phase (FFT) of bandpassed (theta, alpha, beta 1, beta 2, and gamma) EEG oscillations after galvanic nonpainful and (moderate and slight) painful stimulations at left wrist (i.e., overlying median nerve stimulation). The EEG oscillations refer to an electrode position (FC2), in which the phase‐locked EEG oscillations were maximum in a representative subject. The FFT phase values (degrees) are illustrated for each single trial in the raster. The histograms (last three rows) plot the number of single trials within 50 bins of 7.2°, obtained dividing the 0–360° phase range by 50.

Figure 2

Most representative waveforms of spatially‐enhanced somatosensory evoked potentials (SEPs) to the nonpainful stimulations in a representative subject (Subject 2). Electrode sites are labeled according to 10‐20 system.

Figure 3

Across‐subjects grand average waveforms of spatially enhanced SEPs, which are located at right frontal (F4 electrode site of 10‐20 system), central (C4), and parietal (PC6) leads contralateral to the nonpainful stimulations. These waveforms refer to the SEPs obtained averaging separately phase‐locked (thick black traces) and nonphase‐locked (thin gray traces) single trials.

Figure 4

T‐values color maps plotting the results of an explorative statistical comparison of spectral ratios for the phase‐locked moderate painful vs. nonpainful stimulations and for the nonphase‐locked moderate painful vs. nonpainful stimulations. Color scale (256 hues): maximum negative and positive t‐values are coded in white and violet, respectively. Negative t‐values (white‐red) indicate a lower spectral density for the moderate painful stimulation than the nonpainful stimulations. Vice‐versa for the positive t‐values (violet‐blue).

Figure 5

Maps illustrating the linear correlation (r‐values) between phase‐ and nonphase‐locked spectral ratio data for the moderate painful vs. nonpainful stimulations. Color scale (256 hues): maximum negative and positive r‐values (±1) are coded in white and violet, respectively.