Organization of felt and seen pain responses in anterior cingulate cortex

Previous neuroimaging studies comparing pain observation with directly-experienced pain have shown conjoint activations in the cingulate cortex between felt and seen pain. However, whereas this phenomenon may be due to the functional-anatomical overlap of a shared neural substrate, it may also reflect neighboring but distinct activations for felt and seen pain respectively, the co-localization of which is made more likely in group-averaged, spatially-smoothed data. This study explores responses to felt and seen pain, and their spatial overlap, on unsmoothed data from single subjects. Significant activation for the statistical conjunction of felt and seen pain effects was present both at the group level and in six of the eleven individual subjects. However, although each subject showed distinct felt and seen pain areas in the cingulate, a conjunction between these activations was not found in every individual. Among those that showed a felt-seen pain conjunction, its location along the gyrus was variable and the conjunction always fell in a spatially intermediate location between the felt and seen pain activations. These results suggest that the BOLD signal conjunction originates from the intersection of adjacent and partially distinct activations--which do not necessarily always overlap-- rather than from a single neural population coding equally for felt and seen pain. This has implications for the interpretation of BOLD data in addressing "mirrorlike" activations in general, whether in action-related or pain-related areas.

[1]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[2]  Yu-Qing Cao,et al.  Voltage-gated calcium channels and pain , 2006, Pain.

[3]  C. L. Kwan,et al.  An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli , 2000, Pain.

[4]  S. Stone-Elander,et al.  Traumatic nociceptive pain activates the hypothalamus and the periaqueductal gray: a positron emission tomography study , 1996, Pain.

[5]  David Caplan,et al.  Cognitive conjunction and cognitive functions , 2004, NeuroImage.

[6]  Karl J. Friston,et al.  Multisubject fMRI Studies and Conjunction Analyses , 1999, NeuroImage.

[7]  W. Prinz,et al.  Relationships Between Perception and Action: Current Approaches , 1990 .

[8]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

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

[10]  R. Campbell,et al.  Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex , 2000, Current Biology.

[11]  C. Spence,et al.  Multisensory representation of limb position in human premotor cortex , 2003, Nature Neuroscience.

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

[13]  Marius V Peelen,et al.  The sight of others' pain modulates motor processing in human cingulate cortex. , 2007, Cerebral cortex.

[14]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[15]  J. Decety,et al.  To what extent do we share the pain of others? Insight from the neural bases of pain empathy , 2006, Pain.

[16]  Raymond J. Dolan,et al.  Levels of appraisal: A medial prefrontal role in high-level appraisal of emotional material , 2006, NeuroImage.

[17]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[18]  B. Vogt Pain and emotion interactions in subregions of the cingulate gyrus , 2005, Nature Reviews Neuroscience.

[19]  G. Aschersleben,et al.  The Theory of Event Coding (TEC): a framework for perception and action planning. , 2001, The Behavioral and brain sciences.

[20]  Ellen Poliakoff,et al.  Response-specific effects of pain observation on motor behavior , 2007, Cognition.

[21]  Karen D Davis,et al.  Interactions of pain intensity and cognitive load: the brain stays on task. , 2007, Cerebral cortex.

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

[23]  J. Dostrovsky,et al.  Pain-related neurons in the human cingulate cortex , 1999, Nature Neuroscience.

[24]  Karl J. Friston,et al.  Cognitive Conjunction: A New Approach to Brain Activation Experiments , 1997, NeuroImage.

[25]  W. Prinz A common-coding approach to perception and action , 1990 .

[26]  Claus Lamm,et al.  The Neural Substrate of Human Empathy: Effects of Perspective-taking and Cognitive Appraisal , 2007, Journal of Cognitive Neuroscience.

[27]  Avishai Henik,et al.  Are numbers special? The comparison systems of the human brain investigated by fMRI , 2005, Neuropsychologia.

[28]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[29]  Karen D. Davis,et al.  Altered Pain and Temperature Perception Following Cingulotomy and Capsulotomy in a Patient with Schizoaffective Disorder , 1995 .

[30]  B. Vogt,et al.  Pain Processing in Four Regions of Human Cingulate Cortex Localized with Co‐registered PET and MR Imaging , 1996, The European journal of neuroscience.

[31]  N. Kanwisher,et al.  The fusiform face area subserves face perception, not generic within-category identification , 2004, Nature Neuroscience.

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

[33]  P. Downing,et al.  Selectivity for the human body in the fusiform gyrus. , 2005, Journal of neurophysiology.

[34]  W. Prinz Perception and Action Planning , 1997 .

[35]  Peter W. R. Woodruff,et al.  Motivational-affective processing and the neural foundations of empathy , 2007 .

[36]  J. O'Doherty,et al.  Empathic neural responses are modulated by the perceived fairness of others , 2006, Nature.

[37]  G. Rizzolatti,et al.  A unifying view of the basis of social cognition , 2004, Trends in Cognitive Sciences.