Elsevier

NeuroImage

Volume 66, 1 February 2013, Pages 469-478
NeuroImage

Crossmodal bias of visual input on pain perception and pain-induced beta activity

https://doi.org/10.1016/j.neuroimage.2012.10.040Get rights and content

Abstract

In our environment, acute pain is often accompanied by input from other sensory modalities, like visual stimuli, which can facilitate pain processing. To date, it is not well understood how these inputs influence the perception and processing of pain. Previous studies on integrative processing between sensory modalities other than pain have shown that multisensory response gains are strongest when the constituent unimodal stimuli are minimally effective in evoking responses. This finding has been termed the principle of inverse effectiveness (IE). In this high-density electroencephalography study, we investigated the influence of Gabor patches of low and high contrast levels on the perception and processing of spatially and temporally aligned painful electrical stimuli of low and high intensities. Subjective pain ratings, event-related potentials (ERPs) and oscillatory responses served as dependent measures. In line with the principle of IE, stronger crossmodal biasing effects of visual input on subjective pain ratings were found for low compared to high intensity painful stimuli. This effect was paralleled by stronger bimodal interactions in right-central ERPs (150–200 ms) for low compared to high intensity pain stimuli. Moreover, an enhanced suppression of medio-central beta-band activity (12–24 Hz, 200–400 ms) was found for low compared to high intensity pain stimuli. Our findings possibly reflect a facilitation of stimulus processing that serves to enhance response readiness of the sensorimotor system following painful stimulation. Taken together, our study demonstrates that multisensory processing between visual and painful stimuli follows the principle of IE and suggests a role for beta-band oscillations in the crossmodal modulation of pain.

Highlights

► Multisensory gain often is largest when unisensory inputs alone evoke low responses. ► We examined this principle of inverse effectiveness (IE) in human pain processing. ► Pain intensity ratings, event-related potentials and EEG beta-band responses followed the principle of IE. ► Multisensory integration of pain obeys similar rules as other sensory modalities.

Introduction

Acute pain often signals threat and potential damage to the individual, making fast and accurate processing of nociceptive input crucial for our survival. In our environment, pain often occurs together with information from other sensory modalities. Recent studies have shown that semantically meaningful visual stimuli, like emotional facial expressions (Senkowski et al., 2011a) or a needle pricking a hand (Höfle et al., 2012), influence the perception and processing of pain. Despite the high ecological relevance of pain, to date there is no detailed account of the interaction between nociception and vision, and how this interaction may be shaped by basic stimulus properties, such as stimulus intensity.

Research on multisensory integration has demonstrated that combining information across two or more sensory modalities often facilitates behavioral performance (Rach et al., 2011, Senkowski et al., 2011b) as well as neural responses (Stein and Stanford, 2008). A frequently observed effect in behavioral data is that perceived intensities of bimodal stimuli are increased compared to the perceived intensities of the corresponding unimodal stimuli (Frassinetti et al., 2002, Nasri et al., 2011, Odgaard et al., 2004, Stein et al., 1996). Stein et al. (1996) found that the presentation of a brief tone increases the perceived intensity of a concurrently presented flash. Similarly, Odgaard et al. (2004) demonstrated that bursts of white noise presented together with a light are perceived as being louder than noise presented alone. Paralleling these behavioral findings, human neurophysiological studies have shown enhanced neural activity in response to bimodal compared to the corresponding unimodal stimuli (Giard and Peronnet, 1999, Gondan et al., 2005, Murray et al., 2005, Talsma and Woldorff, 2005).

A hallmark of multisensory processing is that the magnitude of behavioral facilitation, as well as the modulation of neural activity, is often inversely related to the intensity of the presented stimuli. Bimodal stimuli more frequently lead to stronger facilitation effects when the constituent unimodal stimuli are low in intensity compared to when they are high in intensity (Corneil et al., 2002, Diederich and Colonius, 2004, Rach et al., 2011). This so called principle of inverse effectiveness (IE) was first shown in single neuron recordings from the cat superior colliculus (Stein and Meredith, 1993) and has recently been demonstrated in a number of human behavioral and neurophysiological studies (Cappe et al., 2012, Senkowski et al., 2011b, Stevenson and James, 2009, Stevenson et al., 2012; but see Ross et al., 2007). Whether IE also applies to the interaction of painful and visual stimuli is thus far unknown.

A candidate neural mechanism that could be crucial for integrative processing of visual and painful stimuli is neural synchrony. Human electroencephalography (EEG) and magnetoencephalography (MEG) studies have highlighted the critical role of synchronized oscillatory activity in both pain processing (Hauck et al., 2008) and multisensory integration (Kayser et al., 2008, Senkowski et al., 2008). Pain processing under various experimental conditions has been shown to suppress oscillatory beta-band activity (BBA; 13–30 Hz) (Mancini et al., in review, Ploner et al., 2006, Raij et al., 2004, Senkowski et al., 2011a), in addition to modulations of low-frequency activity (2–12 Hz) (Domnick et al., 2009, Mouraux et al., 2003) and high-frequency gamma-band activity (GBA; 30–100 Hz) (Gross et al., 2007, Hauck et al., 2007, Tiemann et al., 2010). The close relationship between pain processing and oscillatory responses indicates that the principle of IE, if applicable for integrative processing between painful and visual stimuli, may be reflected in modulations of oscillatory activity. In this EEG study, we investigated whether behavioral and neural interactions between visual and painful stimuli follow the principle of IE. We presented subjects with unimodal visual, unimodal painful and bimodal visual-painful stimuli of high and low intensities, while recording ERPs, oscillatory responses and subjective pain ratings.

Section snippets

Participants

Sixteen right-handed, paid volunteers participated in the study. Three participants had to be excluded because more than 50% of trials including painful stimulation had to be removed due to extensive muscle artifacts in their EEG data. The remaining thirteen participants (8 female, 20–31 years of age) had normal or corrected to normal vision and reported no history of neurological or psychiatric illness. All applied procedures were approved by the Ethics Commission of the Medical Association of

Behavioral data

ANOVAs were calculated for intensity and unpleasantness ratings using the factors condition (bimodal vs. combined unimodal) and stimulation (PhighVhigh, PlowVhigh, PhighVlow, and PlowVlow). The ANOVA for intensity ratings (Table 1) revealed significant main effects of condition (F1,12 = 17.38, p  0.001), stimulation (F3,12 = 25.19, p  0.001), as well as a significant interaction between these factors (F3,36 = 23.02, p  0.001). A two-way follow-up ANOVA was conducted on difference values (PV  P) using the

Discussion

In this study, we investigated the effect of stimulus intensity on multisensory processing between spatially and temporally aligned painful and visual stimuli. As a main result, we found that the crossmodal bias of visual stimuli on pain intensity ratings and neural processing in BBA and ERPs follows the principle of IE.

Conclusion

Our study shows that multisensory processing of visual-painful stimuli in pain intensity ratings, BBA, and ERPs follows the principle of IE. We provide evidence that integrative processing between painful and visual stimuli works in a similar way as previously reported for multisensory processing of stimuli from other sensory modalities. Moreover, our study demonstrates that spatially and temporally aligned basic visual stimuli can bias the perception of pain, even though they do not contain

Acknowledgments

We would like to thank Roger Zimmermann for help with the preparation of the experimental setup and Karin Deazle and Benjamin Asanov for recruitment of participants and help with data recordings. This study was supported by grants from the German Research Foundation (DFG) (SE 1859/1-2, D.S.; SFB TRR 58 B04, A.K.E.) and the European Union (ERC-2010-StG-20091209, D.S.; ERC-2010-AdG-269716, A.K.E.).

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