Neural Mechanisms of Attentional Switching Between Pain and a Visual Illusion Task: A Laser Evoked Potential Study

Brain Topography https://doi.org/10.1007/s10548-017-0613-8 ORIGINAL PAPER Neural Mechanisms of Attentional Switching Between Pain and a Visual Illusion Task: A Laser Evoked Potential Study Andrej Stancak1,2 · Nicholas Fallon1 · Alessandra Fenu1 · Katerina Kokmotou1,2 · Vicente Soto1 · Stephanie Cook1 Received: 5 June 2017 / Accepted: 11 December 2017 © The Author(s) 2017. This article is an open access publication Abstract Previous studies demonstrated that pain induced by a noxious stimulus during a distraction task is affected by both stimulus-driven and goal-directed processes which interact and change over time. The purpose of this exploratory study was to analyse associations of aspects of subjective pain experience and engagement with the distracting task with attentionsensitive components of noxious laser-evoked potentials (LEPs) on a single-trial basis. A laser heat stimulus was applied to the dorsum of the left hand while subjects either viewed the Rubin vase-face illusion (RVI), or focused on their pain and associated somatosensory sensations occurring on their stimulated hand. Pain-related sensations occurring with every laser stimulus were evaluated using a set of visual analogue scales. Factor analysis was used to identify the principal dimensions of pain experience. LEPs were correlated with subjective aspects of pain experience on a single-trial basis using a multiple linear regression model. A positive LEP component at the vertex electrodes in the interval 294–351 ms (P2) was smaller during focusing on RVI than during focusing on the stimulated hand. Single-trial amplitude variations of the P2 component correlated with changes in Factor 1, representing essential aspects of pain, and inversely with both Factor 2, accounting for anticipated pain, and the number of RVI figure reversals. A source dipole located in the posterior region of the cingulate cortex was the strongest contributor to the attention-related single-trial variations of the P2 component. Instantaneous amplitude variations of the P2 LEP component during switching attention towards pain in the presence of a distracting task are related to the strength of pain experience, engagement with the task, and the level of anticipated pain. Results provide neurophysiological underpinning for the use of distraction analgesia acute pain relief. Keywords EEG · P2 · Distraction analgesia · Source dipole model · Single-trial analysis Introduction Pain has been shown to be reduced while attention is directed to a stimulus occurring in a different sensory modality or consumed in an engaging cognitive task (Miron et al. 1989). Although earlier studies pointed to certain limitations in effects of distraction on pain intensity (Leventhal 1992; McCaul et al. 1992), the phenomenon of distraction-induced analgesia proved to be robust enough to alleviate acute procedural pain using video games (Seyrek et al. 1984), * Andrej Stancak 1 Department of Psychological Sciences, University of Liverpool, Liverpool L69 7ZA, UK 2 Institute for Risk and Uncertainty, University of Liverpool, Liverpool, UK immersive virtual reality (Hoffman et al. 2011, 2004b), or watching TV (Bellieni et al. 2006). Since pain signals potential or actual tissue damage, it easily captures attention and therefore disrupts ongoing cognitive or sensory processing (Eccleston and Crombez 1999). Balancing pain experience with concurrent cognitive or sensory activities requires a switch mechanism which operates automatically on a scale of hundreds of milliseconds and also takes into account instantaneous demands and motivational values of parallel tasks. The time interval following switching attention towards pain has been suggested to allow the background pain to invade the conscious mind and disrupt the cognitive performance further in chronic pain patients (Attridge et al. 2016; Vlaeyen et al. 2016). Pain intensity and performance in a distracting task have been shown to interact in a dose-dependent manner with the largest pain reduction and the largest disruption of performance occurring at the highest levels of both (Romero et al. 2013). 13 Vol.:(0123456789) Brain Topography Previous fMRI studies, reviewed recently in Torta et al. (2017), pointed to a network of regions associated with pain reduction during attentional distraction, such as anterior cingulate cortex (Bantick et al. 2002; Buffington et al. 2005), anterior insula (Peyron et al. 1999), and thalamus and somatosensory cortex (Hoffman et al. 2004a). Focusing attention to the location of a noxious stimulus or pain unpleasantness has been shown to activate different brain networks known as medial and lateral pain system (Kulkarni et al. 2005). More recently, Kucyi et al. (2013) demonstrated that a salience network featured by anterior insula, dorsolateral prefrontal cortex and temporal-parietal junction were active when subjects spontaneously allocated larger attention to pain than to unrelated thoughts. However, BOLD-fMRI recordings cannot resolve brain activation patterns on a scale of hundreds of milliseconds which is the time scale at which instantaneous switching between pain and a parallel cognitive process would occur. Electroencephalographic LEPs, offering a temporal resolution on a scale of milliseconds, have been employed to analyse the cortical spatio-temporal patterns associated with attentional modulation of pain. Distraction of attention compared to focusing on pain has been shown to decrease the LEP components at centro-parietal midline electrodes in the latency interval of N2 and more often of the P2 component (Beydoun et al. 1993; Boyle et al. 2008; Friederich et al. 2001; García-Larrea et al. 1997; Kanda et al. 1996; Ohara et al. 2004; Schlereth et al. 2003; Siedenberg and Treede 1996). Positive centro-parietal components at latencies longer than 300 ms also encoded novelty and saliency effects in attentional oddball experiments (Legrain et al. 2003, 2002, 2009a; Siedenberg and Treede 1996; Zaslansky et al. 1996). The positive P2 LEP component reflects salience and novelty of noxious stimuli, and is also affected by the amount of cognitive load associated with a distracter (Legrain et al. 2012). Allocation of attentional resources to pain in the presence of a goal-directed activity can be viewed as a dynamic interplay of the automatic, stimulus-driven, bottom up processes and goal-directed, intentional, top-down processes (Legrain et al. 2012, 2009b; Torta et al. 2017). Formation of pain experience reflects perceptual decision making in which prior information, such as anticipated pain intensity, plays a role (Wiech et al. 2014). To understand the rules and neural mechanisms which determine how pain experience changes during attentional distraction, in which both the pain experience and the engagement with the cognitive task vary over time, a single-trial analysis of subjective responses, task performance data, and cortical response is required. Perceptu (...truncated)