Neural substrates underlying evaluation of pain in actions depicted in words

Previous research has shown that evaluation of pain shown in pictures is mediated by a cortical circuit consisting of the primary and secondary somatosensory cortex (SI and SII), the anterior cingulate cortex (ACC), and the insula. SI and SII subserve the sensory-discriminative component of pain processing whereas ACC and the insula mediate the affective-motivational aspect of pain processing. The current work investigated the neural correlates of evaluation of pain depicted in words. Subjects were scanned using functional magnetic resonance imaging (fMRI) while reading words or phrases depicting painful or neutral actions. Subjects were asked to rate pain intensity of the painful actions depicted in words or counting the number of Chinese characters in the words. Relative to the counting task, rating pain intensity induced activations in SII, the insula, the right middle frontal gyrus, the left superior temporal sulcus and the left middle occipital gyrus. Our results suggest that both the sensory-discriminative and affective-motivational components of the pain matrix are engaged in the processing of pain depicted in words.

[1]  Volkmar Glauche,et al.  Somatotopic organization of human somatosensory cortices for pain: a single trial fMRI study , 2004, NeuroImage.

[2]  G. Pagnoni,et al.  Does Anticipation of Pain Affect Cortical Nociceptive Systems? , 2002, The Journal of Neuroscience.

[3]  Anthony K. P. Jones,et al.  The cortical representation of pain , 1999, PAIN.

[4]  Richard F. Martin,et al.  Nociceptive responses of trigeminal neurons in SII-7b cortex of awake monkeys , 1989, Brain Research.

[5]  Y. Lamour,et al.  Rat somatosensory (SmI) cortex: I. Characteristics of neuronal responses to noxious stimulation and comparison with responses to non-noxious stimulation , 2004, Experimental Brain Research.

[6]  D. Price.  Psychological and neural mechanisms of the affective dimension of pain. , 2000, Science.

[7]  Smith Ge,et al.  The Cortical Representation of the Macula. , 1930 .

[8]  Andrew N. Meltzoff,et al.  How do we perceive the pain of others? A window into the neural processes involved in empathy , 2005, NeuroImage.

[9]  D. Kenshalo,et al.  Responses of primate SI cortical neurons to noxious stimuli. , 1983, Journal of neurophysiology.

[10]  Riitta Hari,et al.  The compassionate brain: humans detect intensity of pain from another's face. , 2006, Cerebral cortex.

[11]  Alan C. Evans,et al.  Functional imaging of an illusion of pain , 1996, Nature.

[12]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Gaspare Galati,et al.  Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain , 2005, Nature Neuroscience.

[14]  J. Stroop.  Studies of interference in serial verbal reactions. , 1992 .

[15]  P. Petrovic,et al.  Placebo and Opioid Analgesia-- Imaging a Shared Neuronal Network , 2002, Science.

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

[17]  M. Bushnell,et al.  Pain affect encoded in human anterior cingulate but not somatosensory cortex. , 1997, Science.

[18]  Xiaosi Gu,et al.  Attention and reality constraints on the neural processes of empathy for pain , 2007, NeuroImage.

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

[20]  F. Birklein,et al.  The unpleasantness of tonic pain is encoded by the insular cortex , 2005, Neurology.

[21]  Jian Kong,et al.  Using fMRI to dissociate sensory encoding from cognitive evaluation of heat pain intensity , 2006, Human brain mapping.

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

[23]  M. Osaka,et al.  A word expressing affective pain activates the anterior cingulate cortex in the human brain: an fMRI study , 2004, Behavioural Brain Research.

[24]  Salvatore Maria Aglioti,et al.  Empathy for pain and touch in the human somatosensory cortex. , 2007, Cerebral cortex.

[25]  G. Pellegrino,et al.  Vicarious responses to pain in anterior cingulate cortex: Is empathy a multisensory issue? , 2004, Cognitive, affective & behavioral neuroscience.

[26]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[27]  Karl Magnus Petersson,et al.  A Regression Analysis Study of the Primary Somatosensory Cortex during Pain , 2002, NeuroImage.

[28]  K. Davis,et al.  The neural circuitry of pain as explored with functional MRI , 2000, Neurological research.

[29]  H. Burton,et al.  Somatic submodality distribution within the second somatosensory (SII), 7b, retroinsular, postauditory, and granular insular cortical areas of M. fascicularis , 1980, The Journal of comparative neurology.

[30]  Salvatore Maria Aglioti,et al.  Stimulus-driven modulation of motor-evoked potentials during observation of others' pain , 2006, NeuroImage.

[31]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[32]  S. Stone-Elander,et al.  Pain-related cerebral activation is altered by a distracting cognitive task , 2000, Pain.

[33]  Krish D. Singh,et al.  fMRI of Thermal Pain: Effects of Stimulus Laterality and Attention , 2002, NeuroImage.

[34]  Patrizia Baraldi,et al.  Functional activity mapping of the mesial hemispheric wall during anticipation of pain , 2003, NeuroImage.

[35]  Resolving a paradox of pain , 1996, Nature.

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

[37]  B. Krauss,et al.  A Comparative fMRI Study of Cortical Representations for Thermal Painful, Vibrotactile, and Motor Performance Tasks , 1999, NeuroImage.

[38]  Roland Peyron,et al.  Role of Operculoinsular Cortices in Human Pain Processing: Converging Evidence from PET, fMRI, Dipole Modeling, and Intracerebral Recordings of Evoked Potentials , 2002, NeuroImage.