Neurocognitive evidence for mental imagery-driven hypoalgesic and hyperalgesic pain regulation

Mental imagery has the potential to influence perception by directly altering sensory, cognitive, and affective brain activity associated with imagined content. While it is well established that mental imagery can both exacerbate and alleviate acute and chronic pain, it is currently unknown how imagery mechanisms regulate pain perception. For example, studies to date have been unable to determine whether imagery effects depend upon a general redirection of attention away from pain or focused attentional mechanisms. To address these issues, we recorded subjective, behavioral and ERP responses using 64-channel EEG while healthy human participants applied a mental imagery strategy to decrease or increase pain sensations. When imagining a glove covering the forearm, participants reported decreased perceived intensity and unpleasantness, classified fewer high-intensity stimuli as painful, and showed a more conservative response bias. In contrast, when imagining a lesion on the forearm, participants reported increased pain intensity and unpleasantness, classified more low-intensity stimuli as painful, and displayed a more liberal response bias. Using a mass-univariate approach, we further showed differential modulation of the N2 potentials across conditions, with inhibition and facilitation respectively increasing and decreasing N2 amplitudes between 122 and 180 ms. Within this time window, source localization associated inhibiting vs. facilitating pain with neural activity in cortical regions involved in cognitive inhibitory control and in the retrieval of semantic information (i.e., right inferior frontal and temporal regions). In contrast, the main sources of neural activity associated with facilitating vs. inhibiting pain were identified in cortical regions typically implicated in salience processing and emotion regulation (i.e., left insular, inferior-middle frontal, supplementary motor and precentral regions). Overall, these findings suggest that the content of a mental image directly alters pain-related decision and evaluative processing to flexibly produce hypoalgesic and hyperalgesic outcomes.

[1]  M. Lloyd,et al.  Signal Detection Theory and the Psychophysics of Pain: An Introduction and Review , 1976, Psychosomatic medicine.

[2]  I Kojo,et al.  The mechanism of the psychophysiological effects of placebo. , 1988, Medical hypotheses.

[3]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[4]  Chantal Berna,et al.  How a Better Understanding of Spontaneous Mental Imagery Linked to Pain Could Enhance Imagery-Based Therapy in Chronic Pain , 2012, Journal of experimental psychopathology.

[5]  J. Kilner,et al.  Bias in a common EEG and MEG statistical analysis and how to avoid it , 2013, Clinical Neurophysiology.

[6]  Nikolaus Weiskopf,et al.  Anterolateral Prefrontal Cortex Mediates the Analgesic Effect of Expected and Perceived Control over Pain , 2006, The Journal of Neuroscience.

[7]  A. Mouraux,et al.  The pain matrix reloaded A salience detection system for the body , 2011, Progress in Neurobiology.

[8]  Chris McNorgan,et al.  A meta-analytic review of multisensory imagery identifies the neural correlates of modality-specific and modality-general imagery , 2012, Front. Hum. Neurosci..

[9]  G. Moseley,et al.  Graded motor imagery for pathologic pain , 2006, Neurology.

[10]  Seung-Schik Yoo,et al.  Neural substrates of tactile imagery: a functional MRI study , 2003, Neuroreport.

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

[12]  S. Kosslyn,et al.  Neural foundations of imagery , 2001, Nature Reviews Neuroscience.

[13]  Ana L. N. Fred,et al.  Unveiling the Biometric Potential of Finger-Based ECG Signals , 2011, Comput. Intell. Neurosci..

[14]  G. Rollman,et al.  Signal detection theory measurement of pain: A review and critique , 1977, Pain.

[15]  Karl J. Friston,et al.  Topological inference for EEG and MEG , 2010, 1011.2901.

[16]  B Bromm,et al.  Principal component analysis of pain-related cerebral potentials to mechanical and electrical stimulation in man. , 1982, Electroencephalography and clinical neurophysiology.

[17]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[18]  Angela R. Laird,et al.  Neural network of cognitive emotion regulation — An ALE meta-analysis and MACM analysis , 2014, NeuroImage.

[19]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[20]  J. B. Knight,et al.  Review and Critique , 1946, Geological Magazine.

[21]  Chantal Berna,et al.  Presence of Mental Imagery Associated with Chronic Pelvic Pain: A Pilot Study , 2011, Pain medicine.

[22]  P. Morris,et al.  Mental Imagery in Chronic Pain: Prevalence and Characteristics Running Head: Mental Imagery in Chronic Pain , 2014 .

[23]  James J. Gross,et al.  Emotion Regulation in Adulthood: Timing Is Everything , 2001 .

[24]  Vilfredo De Pascalis,et al.  Pain perception, somatosensory event-related potentials and skin conductance responses to painful stimuli in high, mid, and low hypnotizable subjects: effects of differential pain reduction strategies , 1999, PAIN®.

[25]  H. Philips,et al.  Imagery and pain: the prevalence, characteristics, and potency of imagery associated with pain. , 2011, Behavioural and cognitive psychotherapy.

[26]  Dirk Ostwald,et al.  Imaging tactile imagery: Changes in brain connectivity support perceptual grounding of mental images in primary sensory cortices , 2014, NeuroImage.

[27]  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.

[28]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Kelly Miller,et al.  Implementation of False Discovery Rate for Exploring Novel Paradigms and Trait Dimensions With ERPs , 2012, Developmental neuropsychology.

[30]  R. Kalisch The functional neuroanatomy of reappraisal: Time matters , 2009, Neuroscience & Biobehavioral Reviews.

[31]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[32]  K. Wiech,et al.  Neurocognitive aspects of pain perception , 2008, Trends in Cognitive Sciences.

[33]  Paul J Laurienti,et al.  The subjective experience of pain: where expectations become reality. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Neil A. Macmillan,et al.  Detection theory: A user's guide, 2nd ed. , 2005 .

[35]  Karl J. Friston,et al.  Evoked brain responses are generated by feedback loops , 2007, Proceedings of the National Academy of Sciences.

[36]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[37]  R. Dowman,et al.  SEP topographies elicited by innocuous and noxious sural nerve stimulation. II. Effects of stimulus intensity on topographic pattern and amplitude. , 1994, Electroencephalography and clinical neurophysiology.

[38]  Irene Tracey,et al.  Getting the pain you expect: mechanisms of placebo, nocebo and reappraisal effects in humans , 2010, Nature Medicine.

[39]  Matthew C. Keller,et al.  Increased sensitivity in neuroimaging analyses using robust regression , 2005, NeuroImage.

[40]  Nakia S. Gordon,et al.  Right-lateralized pain processing in the human cortex: an FMRI study. , 2006, Journal of neurophysiology.

[41]  Jennifer A. Silvers,et al.  Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. , 2014, Cerebral cortex.

[42]  A. Tellegen,et al.  Openness to absorbing and self-altering experiences ("absorption"), a trait related to hypnotic susceptibility. , 1974, Journal of abnormal psychology.

[43]  Karl J. Friston,et al.  EEG and MEG Data Analysis in SPM8 , 2011, Comput. Intell. Neurosci..

[44]  N. Bolger,et al.  Brain Mediators of Predictive Cue Effects on Perceived Pain , 2010, The Journal of Neuroscience.

[45]  Howard L Fields,et al.  Isolating the Modulatory Effect of Expectation on Pain Transmission: A Functional Magnetic Resonance Imaging Study , 2006, The Journal of Neuroscience.

[46]  G. Moseley,et al.  Graded motor imagery is effective for long-standing complex regional pain syndrome: a randomised controlled trial , 2004, Pain.

[47]  C Frith,et al.  Brain mechanisms associated with top-down processes in perception. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[48]  A. Gallace Multisensory Imagery , 2013, Springer New York.

[49]  Eduardo Martínez-Montes,et al.  False discovery rate and permutation test: An evaluation in ERP data analysis , 2010, Statistics in medicine.

[50]  A. D’Ausilio,et al.  An fMRI investigation on image generation in different sensory modalities: the influence of vividness. , 2009, Acta psychologica.

[51]  T. Nurmikko,et al.  Phantom limb pain, cortical reorganization and the therapeutic effect of mental imagery , 2008, Brain : a journal of neurology.

[52]  Mark H. Davis,et al.  A Multidimensional Approach to Individual Differences in Empathy , 1980 .

[53]  Brice A. Kuhl,et al.  Neural Systems Underlying the Suppression of Unwanted Memories , 2004, Science.

[54]  John Duncan,et al.  The role of the right inferior frontal gyrus: inhibition and attentional control , 2010, NeuroImage.

[55]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[56]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.