Pre-stimulus alpha power affects vertex N2–P2 potentials evoked by noxious stimuli

Abstract

It is well known that scalp potentials evoked by nonpainful visual and auditory stimuli are enhanced in amplitude when preceded by pre-stimulus low-amplitude alpha rhythms. This study tested the hypothesis that the same holds for the amplitude of vertex N2–P2 potentials evoked by brief noxious laser stimuli, an issue of interest for clinical perspective. EEG data were recorded in 10 subjects from 30 electrodes during laser noxious stimulation. The artifact-free vertex N2–P2 complex was spatially enhanced by surface Laplacian transformation. Pre-stimulus alpha power was computed at three alpha sub-bands according to subject's individual alpha frequency peak (i.e. about 6–8 Hz for alpha 1, 8–10 Hz for alpha 2 and 10–12 Hz for alpha 3 sub-band). Individual EEG single trials were divided in two sub-groups. The strong-alpha sub-group (high band power) included halfway of all EEG single trials, namely those having the highest pre-stimulus alpha power. Weak-alpha sub-group (low band power) included the remaining trials. Averaging procedure provided laser evoked potentials for both trial sub-groups. No significant effect was found for alpha 1 and alpha 2 sub-bands. Conversely, compared to strong-alpha 3 sub-group, weak-alpha 3 sub-group showed vertex N2–P2 potentials having significantly higher amplitude (p < 0.05). These results extend to the later phases of pain processing systems the notion that generation mechanisms of pre-stimulus alpha rhythms and (laser) evoked potentials are intrinsically related and subjected to fluctuating “noise”. That “noise” could explain the trial-by-trial variability of laser evoked potentials and perception.

Introduction

Several lines of evidence have found relationships between electroencephalographic (EEG) oscillations preceding nonpainful auditory or visual stimuli and the amplitude of averaged event-related potentials (ERPs) or evoked potentials (EPs) [11], [12], [15], [17], [37], [50], [51], [69], [70]. Pre-stimulus EEG oscillations at alpha band (about 10 Hz) would especially affect the amplitude of EPs or ERPs. Some studies have shown that lower the pre-stimulus alpha power, higher the amplitude of the ERPs or EPs [20], [27], [30], [64], [66]. The same was true for theta power (about 4–7 Hz) and EPs [13], [14], [16], [77]. Noteworthy, this kind of relationship does not held when the external stimulus is associated with specific attention demands. It has been shown a positive correlation between pre-stimulus alpha power and amplitude of N1 and P3 (N, negative; P, positive) components of the ERPs associated with the conscious perception of an infrequent stimulus (e.g., see ref. [36]).

The important relationship between the amplitude of pre-stimulus alpha oscillations and the amplitude of EPs is not surprising. Alpha oscillations dominate EEG activity in subjects at rest and reflect features of brain state that are important in relation to the subsequent cortical information processing. Alpha rhythms are strictly related to attentional level and cortical information processing in that enhancement or increase of alpha power reflects elaboration or inhibition of sensory stimuli [56], [63]. These oscillations usually range from 6 to 12 Hz and have been associated with different functional meanings as a function of frequency sub-band [18], [25], [55]. The amplitude of slow-frequency (8–10 Hz) alpha oscillations was related to attentional focus, whereas the amplitude of fast-frequency (10–12 Hz) alpha oscillations was related to cognitive resource allocation on specific sensory modalities [19], [32], [33], [41], [42], [46], [47], [48], [49], [73]. In general, lower is the amplitude of alpha rhythms, better is the information transfer (“gating”) through sensorimotor thalamo-cortical and cortico-cortical pathways [43], [63].

It can be hypothesized that the amplitude of pre-stimulus alpha oscillations, as a reflection of the functional state of thalamo-cortical and cortico-cortical channels, affects not only the cortical processing of nonpainful auditory and visual stimuli (as reported by the quoted papers of the first paragraph) but also the cortical processing of noxious stimuli. This issue is of extreme importance from the comparative evaluation of physiological substrate of painful versus nonpainful information processing and its possible clinical implication (i.e. neurophysiological concomitants of chronic pain). The present EEG study tested the hypothesis that the power of pre-stimulus alpha oscillations affects the cortical processing of sharp and localizable noxious stimuli as revealed by the amplitude of vertex N2–P2 complex evoked by laser stimulation, which has been frequently employed in previous experimental and clinical studies [3], [23]. With proper stimulation parameters, noxious laser stimuli mainly activate nociceptive A-delta and are experienced as sharp, localizable, and scalable; whereas, the use of different stimulation parameters activate C-fibers and induce a dull, hardly localizable pain [2], [21], [22], [80], [82], [84], [85], [86].