Felt and Seen Pain Evoke the Same Local Patterns of Cortical Activity in Insular and Cingulate Cortex

The discovery of regions in the human brain (e.g., insula and cingulate cortex) that activate both under direct exposure to pain and when perceiving pain in others has been interpreted as a neural signature of empathy. However, this overlap raises the question of whether it may reflect a unique distributed population of bimodal neurons or, alternatively, the activity of intermingled but independent populations. We used fMRI on 28 female volunteers and used multivariate pattern analysis techniques to probe for more fine-grain spatial representations of seen and felt pain. Using a whole-brain approach, we found that only in the anterior insula (bilaterally) the distribution of cortical activity evoked by seeing another person's hand in pain was spatially similar to that of pain felt on one's own hand. Subsequent region of interest analyses also implicated the middle insula (right hemisphere) and the middle cingulate cortex. Furthermore, for the anterior insula, the spatial distribution of activity associated with one's pain also replicates that of the perception of negative but painless stimuli. Our data show how the neural representations of aversive events affecting oneself are also recruited when the same events affect others, and provide the stronger evidence thus far of a unique distributed cortical ensemble coding for aversive events regardless of the subject who is affected.

[1]  Lumy Sawaki,et al.  Roles of the Insular Cortex in the Modulation of Pain: Insights from Brain Lesions , 2009, The Journal of Neuroscience.

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

[3]  P. Vuilleumier,et al.  Effects of emotion regulation strategy on brain responses to the valence and social content of visual scenes , 2011, Neuropsychologia.

[4]  Hans P. Op de Beeck,et al.  Probing the mysterious underpinnings of multi-voxel fMRI analyses , 2010, NeuroImage.

[5]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[6]  A. Goldman,et al.  Is social cognition embodied? , 2009, Trends in Cognitive Sciences.

[7]  Angela R Laird,et al.  Brain activity associated with painfully hot stimuli applied to the upper limb: A meta‐analysis , 2005, Human brain mapping.

[8]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[9]  Alan C. Evans,et al.  An MRI-Based Probabilistic Atlas of Neuroanatomy , 1994 .

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

[11]  Ute Habel,et al.  Multidimensional assessment of empathic abilities: Neural correlates and gender differences , 2010, Psychoneuroendocrinology.

[12]  H. Karnath,et al.  Right insula for our sense of limb ownership and self-awareness of actions , 2010, Brain Structure and Function.

[13]  M. Peelen,et al.  Supramodal Representations of Perceived Emotions in the Human Brain , 2010, The Journal of Neuroscience.

[14]  Dimitri Van De Ville,et al.  Decoding of Emotional Information in Voice-Sensitive Cortices , 2009, Current Biology.

[15]  T. Singer,et al.  The role of anterior insular cortex in social emotions , 2010, Brain Structure and Function.

[16]  Markus Neuhäuser,et al.  Permutation Tests , 2011, International Encyclopedia of Statistical Science.

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

[18]  Franco Cauda,et al.  Different functions in the cingulate cortex, a meta-analytic connectivity modeling study , 2011, NeuroImage.

[19]  G. Fink,et al.  What Is the Position of an Arm Relative to the Body? Neural Correlates of Body Schema and Body Structural Description , 2009, The Journal of Neuroscience.

[20]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Vittorio Gallese,et al.  Emotional and Social Behaviors Elicited by Electrical Stimulation of the Insula in the Macaque Monkey , 2011, Current Biology.

[22]  J. Decety,et al.  Gender differences in the mu rhythm during empathy for pain: An electroencephalographic study , 2009, Brain Research.

[23]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[24]  Christian Keysers,et al.  Empathy for positive and negative emotions in the gustatory cortex , 2007, NeuroImage.

[25]  Claus Lamm,et al.  Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain , 2011, NeuroImage.

[26]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[27]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[28]  S. Quartz,et al.  Neural Differentiation of Expected Reward and Risk in Human Subcortical Structures , 2006, Neuron.

[29]  Peter Erhard,et al.  A common neural basis for receptive and expressive communication of pleasant facial affect , 2005, NeuroImage.

[30]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[31]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[32]  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.

[33]  H. Critchley,et al.  Neural Activity Relating to Generation and Representation of Galvanic Skin Conductance Responses: A Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[34]  Christian Keysers,et al.  Testing Simulation Theory with Cross-Modal Multivariate Classification of fMRI Data , 2008, PloS one.

[35]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[36]  E. Reiman,et al.  Thermosensory activation of insular cortex , 2000, Nature Neuroscience.

[37]  T. Singer,et al.  The Social Neuroscience of Empathy , 2009, Annals of the New York Academy of Sciences.

[38]  K. Wiech,et al.  Anterior Insula Integrates Information about Salience into Perceptual Decisions about Pain , 2010, The Journal of Neuroscience.

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

[40]  T. Singer,et al.  The empathic brain: how, when and why? , 2006, Trends in Cognitive Sciences.

[41]  L M Parsons,et al.  Imagined spatial transformation of one's body. , 1987, Journal of experimental psychology. General.

[42]  Philippe Kahane,et al.  Anatomofunctional organization of the insular cortex: A study using intracerebral electrical stimulation in epileptic patients , 2010, Epilepsia.

[43]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[44]  Christian Keysers,et al.  Somatosensation in social perception , 2010, Nature Reviews Neuroscience.

[45]  F. Tong,et al.  Decoding Seen and Attended Motion Directions from Activity in the Human Visual Cortex , 2006, Current Biology.

[46]  Matthew T. Kaufman,et al.  Distributed Neural Representation of Expected Value , 2005, The Journal of Neuroscience.

[47]  Claus Lamm,et al.  How Do We Empathize with Someone Who Is Not Like Us? A Functional Magnetic Resonance Imaging Study , 2010, Journal of Cognitive Neuroscience.

[48]  Jin Fan,et al.  Functional Dissociation of the Frontoinsular and Anterior Cingulate Cortices in Empathy for Pain , 2010, The Journal of Neuroscience.

[49]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[50]  Jeremy Freeman,et al.  Orientation Decoding Depends on Maps, Not Columns , 2011, The Journal of Neuroscience.

[51]  Alan C. Evans,et al.  Anatomical mapping of functional activation in stereotactic coordinate space , 1992, NeuroImage.

[52]  Alan C. Evans,et al.  Enhancement of MR Images Using Registration for Signal Averaging , 1998, Journal of Computer Assisted Tomography.

[53]  Stephen M. Smith,et al.  Meta-analysis of neuroimaging data: A comparison of image-based and coordinate-based pooling of studies , 2009, NeuroImage.

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

[55]  Jarrod A. Lewis-Peacock,et al.  Temporary Activation of Long-Term Memory Supports Working Memory , 2008, The Journal of Neuroscience.

[56]  P. Lang International Affective Picture System (IAPS) : Technical Manual and Affective Ratings , 1995 .

[57]  Jean Decety,et al.  Expertise Modulates the Perception of Pain in Others , 2007, Current Biology.

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

[59]  R. Davidson,et al.  The integration of negative affect, pain and cognitive control in the cingulate cortex , 2011, Nature Reviews Neuroscience.

[60]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

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

[62]  Patrik Vuilleumier,et al.  Processing social aspects of human gaze: A combined fMRI-DTI study , 2011, NeuroImage.

[63]  C. Keysers,et al.  Evidence for mirror systems in emotions , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[64]  P. Rainville Brain mechanisms of pain affect and pain modulation , 2002, Current Opinion in Neurobiology.

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

[66]  Guy Marchal,et al.  Automated multi-modality image registration based on information theory , 1995 .

[67]  A. T. Smith,et al.  The role of the human anterior insular cortex in time processing , 2010, Brain Structure and Function.

[68]  Justin L. Gardner,et al.  Executed and Observed Movements Have Different Distributed Representations in Human aIPS , 2008, The Journal of Neuroscience.

[69]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

[70]  J. Decety,et al.  Human Empathy Through the Lens of Social Neuroscience , 2006, TheScientificWorldJournal.

[71]  Bernhard E. Boser,et al.  A training algorithm for optimal margin classifiers , 1992, COLT '92.

[72]  K. Prkachin,et al.  Is pain the price of empathy? The perception of others' pain in patients with congenital insensitivity to pain. , 2006, Brain : a journal of neurology.