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

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 (150-200ms) for low compared to high intensity pain stimuli. Moreover, an enhanced suppression of medio-central beta-band activity (12-24Hz, 200-400ms) 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.

[1]  Brigitte Röder,et al.  Multisensory processing in the redundant-target effect: A behavioral and event-related potential study , 2005, Perception & psychophysics.

[2]  A. Engel,et al.  Attention to Painful Stimulation Enhances γ-Band Activity and Synchronization in Human Sensorimotor Cortex , 2007, The Journal of Neuroscience.

[3]  John J. Foxe,et al.  Multisensory interactions in early evoked brain activity follow the principle of inverse effectiveness , 2011, NeuroImage.

[4]  Robert Oostenveld,et al.  Enhanced EEG gamma-band activity reflects multisensory semantic matching in visual-to-auditory object priming , 2008, NeuroImage.

[5]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[6]  R Kakigi,et al.  Pain-Related somatosensory evoked potentials. , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[7]  John J. Foxe,et al.  Crossmodal binding through neural coherence: implications for multisensory processing , 2008, Trends in Neurosciences.

[8]  Sidney S. Simon,et al.  Merging of the Senses , 2008, Front. Neurosci..

[9]  B. Bromm,et al.  The intracutaneous stimulus: a new pain model for algesimetric studies. , 1984, Methods and findings in experimental and clinical pharmacology.

[10]  John J. Foxe,et al.  Grabbing your ear: rapid auditory-somatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment. , 2005, Cerebral cortex.

[11]  M. Murray,et al.  Looming Signals Reveal Synergistic Principles of Multisensory Integration , 2012, The Journal of Neuroscience.

[12]  M. Woldorff,et al.  Distortion of ERP averages due to overlap from temporally adjacent ERPs: analysis and correction. , 2007, Psychophysiology.

[13]  Joachim Gross,et al.  Gamma oscillations as a neuronal correlate of the attentional effects of pain , 2010, PAIN.

[14]  N. Bolognini,et al.  Enhancement of visual perception by crossmodal visuo-auditory interaction , 2002, Experimental Brain Research.

[15]  A. Diederich,et al.  Bimodal and trimodal multisensory enhancement: Effects of stimulus onset and intensity on reaction time , 2004, Perception & psychophysics.

[16]  G. Pfurtscheller,et al.  ERD/ERS patterns reflecting sensorimotor activation and deactivation. , 2006, Progress in brain research.

[17]  Marty G. Woldorff,et al.  Selective Attention and Multisensory Integration: Multiple Phases of Effects on the Evoked Brain Activity , 2005, Journal of Cognitive Neuroscience.

[18]  Joachim Gross,et al.  Gamma Oscillations in Human Primary Somatosensory Cortex Reflect Pain Perception , 2007, PLoS biology.

[19]  S A Hillyard,et al.  An analysis of audio-visual crossmodal integration by means of event-related potential (ERP) recordings. , 2002, Brain research. Cognitive brain research.

[20]  Viviana Betti,et al.  Seeing the pain of others while being in pain: A laser-evoked potentials study , 2008, NeuroImage.

[21]  V. Legrain,et al.  Involuntary orienting of attention to nociceptive events: neural and behavioral signatures. , 2009, Journal of neurophysiology.

[22]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[23]  A. Mouraux,et al.  Gamma-Band Oscillations in the Primary Somatosensory Cortex—A Direct and Obligatory Correlate of Subjective Pain Intensity , 2012, The Journal of Neuroscience.

[24]  Hauke R. Heekeren,et al.  What Happens in Between? Human Oscillatory Brain Activity Related to Crossmodal Spatial Cueing , 2008, PloS one.

[25]  N. Logothetis,et al.  Visual modulation of neurons in auditory cortex. , 2008, Cerebral cortex.

[26]  Daniel Senkowski,et al.  Good times for multisensory integration: Effects of the precision of temporal synchrony as revealed by gamma-band oscillations , 2007, Neuropsychologia.

[27]  Ryan A. Stevenson,et al.  Audiovisual integration in human superior temporal sulcus: Inverse effectiveness and the neural processing of speech and object recognition , 2009, NeuroImage.

[28]  Hans Colonius,et al.  On quantifying multisensory interaction effects in reaction time and detection rate , 2011, Psychological research.

[29]  A. Schnitzler,et al.  Differential coding of pain intensity in the human primary and secondary somatosensory cortex. , 2001, Journal of neurophysiology.

[30]  Laura Busse,et al.  The ERP omitted stimulus response to “no-stim” events and its implications for fast-rate event-related fMRI designs , 2003, NeuroImage.

[31]  Lawrence E Marks,et al.  Brighter noise: Sensory enhancement of perceived loudness by concurrent visual stimulation , 2004, Cognitive, affective & behavioral neuroscience.

[32]  Riitta Hari,et al.  Modulation of motor-cortex oscillatory activity by painful Aδ- and C-fiber stimuli , 2004, NeuroImage.

[33]  U. Noppeney,et al.  Superadditive responses in superior temporal sulcus predict audiovisual benefits in object categorization. , 2010, Cerebral cortex.

[34]  A Mouraux,et al.  Non-phase locked electroencephalogram (EEG) responses to CO2 laser skin stimulations may reflect central interactions between A∂- and C-fibre afferent volleys , 2003, Clinical Neurophysiology.

[35]  T. Stanford,et al.  Multisensory integration: current issues from the perspective of the single neuron , 2008, Nature Reviews Neuroscience.

[36]  A J Van Opstal,et al.  Auditory-visual interactions subserving goal-directed saccades in a complex scene. , 2002, Journal of neurophysiology.

[37]  John J. Foxe,et al.  Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. , 2002, Brain research. Cognitive brain research.

[38]  Claudia Plant,et al.  Decoding an individual's sensitivity to pain from the multivariate analysis of EEG data. , 2012, Cerebral cortex.

[39]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[40]  A. Mouraux,et al.  Low intensity intra-epidermal electrical stimulation can activate Aδ-nociceptors selectively , 2010, PAIN.

[41]  J. Lorenz,et al.  Neurophysiological evaluation of pain. , 1998, Electroencephalography and clinical neurophysiology.

[42]  Daniel Senkowski,et al.  Gamma-Band Activity as a Signature for Cross-Modal Priming of Auditory Object Recognition by Active Haptic Exploration , 2011, The Journal of Neuroscience.

[43]  Aina Puce,et al.  Inverse Effectiveness and Multisensory Interactions in Visual Event-Related Potentials with Audiovisual Speech , 2012, Brain Topography.

[44]  M. Giard,et al.  Auditory-Visual Integration during Multimodal Object Recognition in Humans: A Behavioral and Electrophysiological Study , 1999, Journal of Cognitive Neuroscience.

[45]  B. Stein,et al.  Enhancement of Perceived Visual Intensity by Auditory Stimuli: A Psychophysical Analysis , 1996, Journal of Cognitive Neuroscience.

[46]  A. Mouraux,et al.  Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. , 2009, Journal of neurophysiology.

[47]  Febo Cincotti,et al.  Human brain oscillatory activity phase‐locked to painful electrical stimulations: A multi‐channel EEG study , 2002, Human brain mapping.

[48]  A. Mouraux,et al.  Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? , 2008, Journal of neurophysiology.

[49]  F. Varela,et al.  Neuromagnetic imaging of cortical oscillations accompanying tactile stimulation. , 2003, Brain research. Cognitive brain research.

[50]  Riitta Hari,et al.  Oscillatory motor cortex–muscle coupling during painful laser and nonpainful tactile stimulation , 2005, NeuroImage.

[51]  P. Haggard,et al.  Changes in cortical oscillations linked to multisensory modulation of nociception , 2013, The European journal of neuroscience.

[52]  A. Engel,et al.  Emotional Facial Expressions Modulate Pain-Induced Beta and Gamma Oscillations in Sensorimotor Cortex , 2011, The Journal of Neuroscience.

[53]  Robert Oostenveld,et al.  Tactile stimulation accelerates behavioral responses to visual stimuli through enhancement of occipital gamma-band activity , 2009, Vision Research.

[54]  Anthony K. P. Jones,et al.  Pain processing during three levels of noxious stimulation produces differential patterns of central activity , 1997, Pain.

[55]  John J. Foxe,et al.  Multisensory processing and oscillatory activity: analyzing non-linear electrophysiological measures in humans and simians , 2007, Experimental Brain Research.

[56]  John J. Foxe,et al.  Do you see what I am saying? Exploring visual enhancement of speech comprehension in noisy environments. , 2006, Cerebral cortex.

[57]  Ryan A. Stevenson,et al.  Visuo-haptic Neuronal Convergence Demonstrated with an Inversely Effective Pattern of BOLD Activation , 2012, Journal of Cognitive Neuroscience.

[58]  J. Maisog,et al.  Pain intensity processing within the human brain: a bilateral, distributed mechanism. , 1999, Journal of neurophysiology.

[59]  Michael Hauck,et al.  C-fiber-related EEG-oscillations induced by laser radiant heat stimulation of capsaicin-treated skin , 2009, Journal of pain research.

[60]  Thierry Thomas-Danguin,et al.  Cross-modal interactions between taste and smell: Odour-induced saltiness enhancement depends on salt level , 2011 .

[61]  N. Holmes The law of inverse effectiveness in neurons and behaviour: Multisensory integration versus normal variability , 2007, Neuropsychologia.

[62]  Michael Hauck,et al.  Role of Synchronized Oscillatory Brain Activity for Human Pain Perception , 2008, Reviews in the neurosciences.

[63]  P. Mitra,et al.  Analysis of dynamic brain imaging data. , 1998, Biophysical journal.

[64]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[65]  Michael Hauck,et al.  Viewing a needle pricking a hand that you perceive as yours enhances unpleasantness of pain , 2012, PAIN®.

[66]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[67]  Joachim Gross,et al.  Pain suppresses spontaneous brain rhythms. , 2005, Cerebral cortex.