An fMRI Study Exploring the Overlap and Differences between Neural Representations of Physical and Recalled Pain

Implementing a recall paradigm without hypnosis, we use functional MRI (fMRI) to explore and compare nociceptive and centrally-driven pain experiences. We posit that a trace of a recent nociceptive event can be used to create sensory-re-experiencing of pain that can be qualified in terms of intensity and vividness. Fifteen healthy volunteers received three levels of thermal stimuli (warm, low pain and high pain) and subsequently were asked to recall and then rate this experience. Neuroimaging results reveal that recalling a previous sensory experience activates an extensive network of classical pain processing structures except the contralateral posterior insular cortex. Nociceptive-specific activation of this structure and the rated intensity difference between physical and recalled pain events allow us to investigate the link between the quality of the original nociceptive stimulus and the mental trace, as well as the differences between the accompanying neural responses. Additionally, by incorporating the behavioural ratings, we explored which brain regions were separately responsible for generating either an accurate or vivid recall of the physical experience. Together, these observations further our understanding of centrally-mediated pain experiences and pain memory as well as the potential relevance of these factors in the maintenance of chronic pain.

[1]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[2]  Stephen Morley,et al.  Vivid memory for ‘everyday’ pains , 1993, Pain.

[3]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[4]  E. Brodie,et al.  Memory for labor pain: context and quality , 1996, Pain.

[5]  J. Decety Do imagined and executed actions share the same neural substrate? , 1996, Brain research. Cognitive brain research.

[6]  Fred A Lenz,et al.  Pain sensitivity alterations as a function of lesion location in the parasylvian cortex , 1999, Pain.

[7]  Ravi S. Menon,et al.  Dissociating pain from its anticipation in the human brain. , 1999, Science.

[8]  A. Hartley,et al.  Locating and fractionating working memory using functional neuroimaging: Storage, maintenance, and executive functions , 2000, Microscopy research and technique.

[9]  Chiang-shan Ray Li,et al.  Impairment of motor imagery in putamen lesions in humans , 2000, Neuroscience Letters.

[10]  G. Glover,et al.  Basal ganglia involvement in memory‐guided movement sequencing , 2000, Neuroreport.

[11]  C. Degueldre,et al.  Neural Mechanisms of Antinociceptive Effects of Hypnosis , 2000, Anesthesiology.

[12]  E A Maguire,et al.  Neuroimaging studies of autobiographical event memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[13]  A. Halpern,et al.  Cerebral Substrates of Musical Imagery , 2001, Annals of the New York Academy of Sciences.

[14]  P. Matthews,et al.  Exacerbation of Pain by Anxiety Is Associated with Activity in a Hippocampal Network , 2001, The Journal of Neuroscience.

[15]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[16]  A. Lundervold,et al.  Common pathways in mental imagery and pain perception: an fMRI study of a subject with an amputated arm. , 2001, Scandinavian journal of psychology.

[17]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[18]  F. Mauguière,et al.  Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. , 2002, Cerebral cortex.

[19]  S. Clare,et al.  Imaging how attention modulates pain in humans using functional MRI. , 2002, Brain : a journal of neurology.

[20]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[21]  Justin A. Harris,et al.  Transient Storage of a Tactile Memory Trace in Primary Somatosensory Cortex , 2002, The Journal of Neuroscience.

[22]  Michael D. Robinson,et al.  Belief and feeling: evidence for an accessibility model of emotional self-report. , 2002, Psychological bulletin.

[23]  S. Minoshima,et al.  Keeping pain out of mind: the role of the dorsolateral prefrontal cortex in pain modulation. , 2003, Brain : a journal of neurology.

[24]  S. Kosslyn,et al.  When is early visual cortex activated during visual mental imagery? , 2003, Psychological bulletin.

[25]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[26]  M. Bensafi,et al.  Olfactomotor activity during imagery mimics that during perception , 2003, Nature Neuroscience.

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

[28]  E. Phelps Human emotion and memory: interactions of the amygdala and hippocampal complex , 2004, Current Opinion in Neurobiology.

[29]  Pierre Rainville,et al.  Rapid deterioration of pain sensory-discriminative information in short-term memory , 2004, Pain.

[30]  A. Apkarian,et al.  Cortical pathophysiology of chronic pain. , 2004, Novartis Foundation symposium.

[31]  Daniela Montaldi,et al.  Recalling spatial information as a component of recently and remotely acquired episodic or semantic memories: an fMRI study. , 2004, Neuropsychology.

[32]  V. Andrew Stenger,et al.  Cerebral activation during hypnotically induced and imagined pain , 2004, NeuroImage.

[33]  D. V. Kuiken A meta-analysis of the effect of guided imagery practice on outcomes. , 2004 .

[34]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[35]  Debra M Van Kuiken A Meta-Analysis of the Effect of Guided Imagery Practice on Outcomes , 2004, Journal of holistic nursing : official journal of the American Holistic Nurses' Association.

[36]  R. Treede,et al.  Human brain mechanisms of pain perception and regulation in health and disease , 2005, European journal of pain.

[37]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.

[38]  Kevin S. LaBar,et al.  Co-activation of the amygdala, hippocampus and inferior frontal gyrus during autobiographical memory retrieval , 2005, Neuropsychologia.

[39]  R. Hari,et al.  Brain correlates of subjective reality of physically and psychologically induced pain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[40]  A. Meltzoff,et al.  Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain , 2006, Neuropsychologia.

[41]  E. Brodie,et al.  Analgesia through the looking‐glass? A randomized controlled trial investigating the effect of viewing a ‘virtual’ limb upon phantom limb pain, sensation and movement , 2007, European journal of pain.

[42]  Pierre Rainville,et al.  Memory Traces of Pain in Human Cortex , 2007, The Journal of Neuroscience.

[43]  T. Nurmikko,et al.  Retrieving autobiographical memories of painful events activates the anterior cingulate cortex and inferior frontal gyrus. , 2007, The journal of pain : official journal of the American Pain Society.

[44]  I. Tracey,et al.  The insula: A multidimensional integration site for pain , 2007, Pain.

[45]  Koji Inui,et al.  Inner experience of pain: imagination of pain while viewing images showing painful events forms subjective pain representation in human brain. , 2006, Cerebral cortex.

[46]  François Mauguière,et al.  Human SII and posterior insula differently encode thermal laser stimuli. , 2006, Cerebral cortex.

[47]  H. Krämer,et al.  Illusion of pain: pre-existing knowledge determines brain activation of 'imagined allodynia'. , 2008, The journal of pain : official journal of the American Pain Society.

[48]  C. Keysers,et al.  A Common Anterior Insula Representation of Disgust Observation, Experience and Imagination Shows Divergent Functional Connectivity Pathways , 2008, PloS one.

[49]  Tania Singer,et al.  University of Zurich Zurich Open Repository and Archive I Feel How You Feel but Not Always: the Empathic Brain and Its I Feel How You Feel but Not Always: the Empathic Brain and Its Modulation , 2009 .

[50]  M. Baliki,et al.  Towards a theory of chronic pain , 2009, Progress in Neurobiology.

[51]  U. Baumgärtner,et al.  Explicit episodic memory for sensory-discriminative components of capsaicin-induced pain: Immediate and delayed ratings , 2009, Pain.

[52]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[53]  G. Hesslow The current status of the simulation theory of cognition , 2012, Brain Research.

[54]  R. Gollub,et al.  The use of functional neuroimaging to evaluate psychological and other non-pharmacological treatments for clinical pain , 2012, Neuroscience Letters.