Attentional processes and cognitive performance during expectancy of painful galvanic stimulations: a high-resolution EEG study

Abstract

In the present high-resolution electroencephalographic (EEG) study, an omitted-stimulus paradigm induced a strong expectancy for a predictable painful stimulation (nonpainful in the control condition). During the expectancy of pain, concurrent cognitive demands were superimposed. The aim was to investigate the effects on primary sensorimotor and central midline areas of the competition among concurrent attentional processes related to cognition and pain expectancy, as indexed by behavioral performance and EEG data. A main issue was whether cognitive performance decreases, due to a re-allocation of attentional resources on primary sensorimotor and midline areas for the anticipation of pain. Behavioral results showed no differences in the cognitive (working memory) performance during the expectancy of nonpainful versus painful stimulations. In parallel, anticipatory event-related potentials (ERPs) were negligible in line with a low emotional reactivity/alertness as revealed by heart rate deceleration (HRD), skin conductance response (SCR), and low-band (6–10 Hz) alpha EEG oscillations. In contrast, high-band alpha EEG oscillations (10–12 Hz) over the contralateral primary sensorimotor cortex decreased more during the expectancy of painful compared to nonpainful stimuli, in line with an increased anticipatory preparation of the somatosensory channel. These findings provide further evidence on the fact that attentional processes at the basis of cognition can be defended by the anticipation of pain, at least when the incoming painful stimuli are repetitive and predictable. This happens even if the brain increases preparatory processes of the specific sensory channel to be targeted by the painful stimulus.

Introduction

Attentional processes modulate regional blood flow of nociceptive cortical areas not only during pain experience but also in an anticipatory phase [1], [2], [3], [4], [5], [6], [7], [8]. The anticipation of pain influences primary somatosensory area, which is mainly devoted to sensory discrimination [3], [9], [10], [11], [12]. Other regions affected by the anticipation of pain are the midline cingulate areas, which are engaged in affective/cognitive aspects of pain experience, selection of proper viscero-sensorimotor/behavioral responses, and event memorization [2], [3], [6], [7], [9], [10], [11], [12], [13], [14].

The relationships among concurrent pain experience and cognition are poorly understood. A bulk of previous evidence have shown that pain or anticipation of pain may subtract attentional resources from cognitive operations [15], [16], [17], [18], [19], [20], as a function of task complexity, endogenous variations in hormone level (i.e. menstrual cycle), and individual differences in reactivity to stressful agents [21], [22], [23]. A neurophysiological correlate of pain is the decrease of a midline positive electroencephalographic (EEG) potential evoked by a novel stimulus, which would indicate a decrement of attentional resources for cognitive processes [24], [25], [26]. On the contrary, other studies have shown that cognitive demands can distract from pain perception [7], [12], [27], [28]. Basically, the underlying mechanism would be a modulation of orbitofrontal and anterior cingulate areas accompanied by a reduced activation of brainstem opioid network including amygdala, periaqueductal gray, parabrachial nucleus, and centromedial medulla [7], [12], [27], [29].

In the present high-resolution EEG study, an omitted-stimulus paradigm induced a strong expectancy for a predictable painful stimulation (nonpainful in the control condition). During the expectancy of pain, concurrent cognitive demands were superimposed. The aim was to investigate the effects on primary sensorimotor and midline cortical areas, including supplementary motor area, frontal areas and cingulate gyrus, of the competition among concurrent attentional processes related to cognition and pain expectancy, as indexed by behavioral performance and EEG data. A main issue was whether cognitive performance decreases due to a re-allocation of attentional resources on primary sensorimotor and midline areas for the anticipation of pain.

The rationale for the neurophysiological approach is that synaptic concomitants of anticipatory attentional processes can be roughly but directly indexed by two EEG parameters. First index is EEG oscillatory activity at extended alpha band (6–12 Hz). Lower the amplitude of the alpha oscillations, better the information transfer (“gating”) through sensorimotor thalamocortical and cortico-cortical pathways [30], [31]. The second index is obtained by the averaging of the EEG oscillations across single trials, in the period between warning and imperative go stimuli [32], [33]. The averaging procedure produces slow negative event-related potentials (ERPs) or contingent negative variation (CNV), which denote affective-motivational cortical processes other than preparatory sensorimotor processes [34], [35]. When no motor response is required, CNV is termed stimulus-preceding negativity (SPN; [32], [33]). Both CNV and SPN reflect anticipatory cortical excitability [32].