Separate neural representations for physical pain and social rejection

Nature Communications

Volumn 5, Issue , 2014, Pages

  Woo, Choong Wan ^a   Koban, Leonie ^a   Kross, Ethan ^b   Lindquist, Martin A ^c   Banich, Marie T ^a   Ruzic, Luka ^a   Andrews Hanna, Jessica R ^a   Wager, Tor D ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLASSIFICATION; DATA SET; IMAGING METHOD; NEUROLOGY;

ACCURACY; ADULT; ANTERIOR CINGULATE; ARTICLE; BRAIN REGION; CLASSIFIER; CONNECTOME; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; PAIN; SOCIAL REJECTION; BRAIN; FUNCTIONAL NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN MEASUREMENT; PATHOPHYSIOLOGY; SOCIAL DISTANCE; YOUNG ADULT;

BRAIN; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; PAIN; PAIN MEASUREMENT; SOCIAL DISTANCE; YOUNG ADULT;

EID: 84922890367     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6380     Document Type: Article

References (70)

1. MacDonald, G. & Leary, M. R. Why does social exclusion hurt? The relationship between social and physical pain. Psychol. Bull. 131, 202-223 (2005).
2. Eisenberger, N. I., Lieberman, M. D. & Williams, K. D. Does rejection hurt? An fMRI study of social exclusion. Science 302, 290-292 (2003).
3. Eisenberger, N. I. The pain of social disconnection: examining the shared neural underpinnings of physical and social pain. Nat. Rev. Neurosci. 13, 421-434 (2012).
4. Kross, E., Berman, M. G., Mischel, W., Smith, E. E. & Wager, T. D. Social rejection shares somatosensory representations with physical pain. Proc. Natl Acad. Sci. USA 108, 6270-6275 (2011).
5. Novembre, G., Zanon, M. & Silani, G. Empathy for social exclusion involves the sensory-discriminative component of pain: a within-subject fMRI study. Soc. Cogn. Affect Neurosci. doi: 10.1093/scan/nsu038 (2014).
6. Holt-Lunstad, J., Smith, T. B. & Layton, J. B. Social relationships and mortality risk: a meta-Analytic review. PLoS Med. 7, e1000316 (2010).
7. Keller, M. C., Neale, M. C. & Kendler, K. S. Association of different adverse life events with distinct patterns of depressive symptoms. Am. J. Psychiatry. 164, 1521-1529 quiz 1622 (2007).
8. Cacioppo, J. T. & Hawkley, L. C. Perceived social isolation and cognition. Trends Cogn. Sci. 13, 447-454 (2009).
9. Barrett, L. F. & Wager, T. D. The structure of emotion-Evidence from neuroimaging studies. Curr. Dir. Psychol. Sci. 15, 79-83 (2006).
10. Cohen, S. & Janicki-Deverts, D. Can we improve our physical health by altering our social networks? Perspect. Psychol. Sci. 4, 375-378 (2009).
11. DeWall, C. N. et al. Acetaminophen reduces social pain: behavioral and neural evidence. Psychol. Sci. 21, 931-937 (2010).
12. Panksepp, J., Nelson, E. & Bekkedal, M. Brain systems for the mediation of social separation-distress and social-reward. Evolutionary antecedents and neuropeptide intermediaries. Ann. N.Y. Acad. Sci. 807, 78-100 (1997).
13. Hsu, D. T. et al. Response of the mu-opioid system to social rejection and acceptance. Mol. Psychiatry 18, 1211-1217 (2013).
14. Craig, A. D. How do you feel-now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59-70 (2009).
15. Etkin, A. & Wager, T. D. Functional neuroimaging of anxiety: a meta-Analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 164, 1476-1488 (2007).
16. Rainville, P., Duncan, G. H., Price, D. D., Carrier, B. & Bushnell, M. C. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277, 968-971 (1997).
17. Peelen, M. V., Wiggett, A. J. & Downing, P. E. Patterns of fMRI activity dissociate overlapping functional brain areas that respond to biological motion. Neuron 49, 815-822 (2006).
18. Peelen, M. V. & Downing, P. E. Using multi-voxel pattern analysis of fMRI data to interpret overlapping functional activations. Trends Cogn. Sci. 11, 4-5 (2007).
19. Iannetti, G. D., Salomons, T. V., Moayedi, M., Mouraux, A. & Davis, K. D. Beyond metaphor: contrasting mechanisms of social and physical pain. Trends Cogn. Sci. 17, 371-378 (2013).
20. Wager, T. D. et al. in Handbook of Emotions Ch. 15 (eds Lewis, M., Haviland-Jones, J. M. & Barrett, L. F.) 249-271 (Guilford, 2008).
21. Dosenbach, N. U. et al. A core system for the implementation of task sets. Neuron 50, 799-812 (2006).
22. Yarkoni, T., Poldrack, R. A., Nichols, T. E., Van Essen, D. C. & Wager, T. D. Large-scale automated synthesis of human functional neuroimaging data. Nat. Methods 8, 665-670 (2011).
23. Egner, T. Surprise! A unifying model of dorsal anterior cingulate function? Nat. Neurosci. 14, 1219-1220 (2011).
24. Seeley, W. W. et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 27, 2349-2356 (2007).
25. Kvitsiani, D. et al. Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature 498, 363-366 (2013).
26. Sikes, R. W. & Vogt, B. A. Nociceptive neurons in area 24 of rabbit cingulate cortex. J. Neurophysiol. 68, 1720-1732 (1992).
27. Shidara, M. & Richmond, B. J. Anterior cingulate: single neuronal signals related to degree of reward expectancy. Science 296, 1709-1711 (2002).
28. Sheth, S. A. et al. Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation. Nature 488, 218-221 (2012).
29. Haxby, J. V. et al. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293, 2425-2430 (2001).
30. Sternberg, S. Separate modifiability, mental modules, and the use of pure and composite measures to reveal them. Acta Psychol. 106, 147-246 (2001).
31. Kamitani, Y. & Tong, F. Decoding the visual and subjective contents of the human brain. Nat. Neurosci. 8, 679-685 (2005).
32. Wager, T. D. et al. An fMRI-based neurologic signature of physical pain. New Engl J. Med. 368, 1388-1397 (2013).
33. Pennebaker, J. W., Chung, C. K., Ireland, M., Gonzales, A. & Booth, R. J. The development and psychometric properties of LIWC2007. LIWC. Net (2007).
34. Vapnik, V. The Nature of Statistical Learning Theory (Springer-Verlag, 1995).
35. Hastie, T., Tibshirani, R. & Friedman, J. The Elements of Statistical Learning: Data Mining, Inference, and Prediction 2nd edn (Springer, 2009).
36. Apkarian, A. V., Bushnell, M. C., Treede, R. D. & Zubieta, J. K. Human brain mechanisms of pain perception and regulation in health and disease. Eur. J. Pain 9, 463-484 (2005).
37. Bushnell, M. C., Ceko, M. & Low, L. A. Cognitive and emotional control of pain and its disruption in chronic pain. Nat. Rev. Neurosci. 14, 502-511 (2013).
38. Denny, B. T., Kober, H., Wager, T. D. & Ochsner, K. N. A meta-Analysis of functional neuroimaging studies of self-And other judgments reveals a spatial gradient for mentalizing in medial prefrontal cortex. J. Cogn. Neurosci. 24, 1742-1752 (2012).
39. Amodio, D. M. & Frith, C. D. Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 7, 268-277 (2006).
40. Wager, T. D., Davidson, M. L., Hughes, B. L., Lindquist, M. A. & Ochsner, K. N. Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59, 1037-1050 (2008).
41. Urry, H. L., van Reekum, C. M., Johnstone, T. & Davidson, R. J. Individual differences in some (but not all) medial prefrontal regions reflect cognitive demand while regulating unpleasant emotion. Neuroimage 47, 852-863 (2009).
42. Willis, W. D. & Westlund, K. N. Neuroanatomy of the pain system and of the pathways that modulate pain. J. Clin. Neurophysiol. 14, 2-31 (1997).
43. Kriegeskorte, N., Mur, M. & Bandettini, P. Representational similarity analysis-connecting the branches of systems neuroscience. Front. Sys. Neurosci. 2, 4 (2008).
44. Corradi-Dell'Acqua, C., Hofstetter, C. & Vuilleumier, P. Felt and seen pain evoke the same local patterns of cortical activity in insular and cingulate cortex. J. Neurosci. 31, 17996-18006 (2011).
45. Kriegeskorte, N., Goebel, R. & Bandettini, P. Information-based functional brain mapping. Proc. Natl Acad. Sci. USA 103, 3863-3868 (2006).
46. Craddock, R. C., James, G. A., Holtzheimer, 3rd P. E., Hu, X. P. & Mayberg, H. S. A whole brain fMRI atlas generated via spatially constrained spectral clustering. Hum. Brain Mapp. 33, 1914-1928 (2012).
47. Eisenberger, N. I. & Cole, S. W. Social neuroscience and health: neurophysiological mechanisms linking social ties with physical health. Nat. Neurosci. 15, 669-674 (2012).
48. Shmuel, A., Chaimow, D., Raddatz, G., Ugurbil, K. & Yacoub, E. Mechanisms underlying decoding at 7 T: Ocular dominance columns, broad structures, and macroscopic blood vessels in V1 convey information on the stimulated eye. Neuroimage 49, 1957-1964 (2010).
49. Logothetis, N. K. What we can do and what we cannot do with fMRI. Nature 453, 869-878 (2008).
50. Chaimow, D., Yacoub, E., Ugurbil, K. & Shmuel, A. Modeling and analysis of mechanisms underlying fMRI-based decoding of information conveyed in cortical columns. Neuroimage 56, 627-642 (2011).
51. Fisher, H. E., Brown, L. L., Aron, A., Strong, G. & Mashek, D. Reward, addiction, and emotion regulation systems associated with rejection in love. J. Neurophysiol. 104, 51-60 (2010).
52. Way, B. M., Taylor, S. E. & Eisenberger, N. I. Variation in the mu-opioid receptor gene (OPRM1) is associated with dispositional and neural sensitivity to social rejection. Proc. Natl Acad. Sci. USA 106, 15079-15084 (2009).
53. Butler, R. K. & Finn, D. P. Stress-induced analgesia. Prog. Neurobiol. 88, 184-202 (2009).
54. Kehoe, P. & Blass, E. M. Opioid-mediation of separation distress in 10-day-old rats: reversal of stress with maternal stimuli. Dev. Psychobiol. 19, 385-398 (1986).
55. DeWall, C. N. & Baumeister, R. F. Alone but feeling no pain: Effects of social exclusion on physical pain tolerance and pain threshold, affective forecasting, and interpersonal empathy. J. Pers. Soc. Psychol. 91, 1-15 (2006).
56. Anderson, B. J. Paracetamol (Acetaminophen): mechanisms of action. Paediatr. Anaesth. 18, 915-921 (2008).
57. Kapur, S., Phillips, A. G. & Insel, T. R. Why has it taken so long for biological psychiatry to develop clinical tests and what to do about it? Mol. Psychiatr. 17, 1174-1179 (2012).
58. Landa, A., Peterson, B. S. & Fallon, B. A. Somatoform pain: a developmental theory and translational research review. Psychosom. Med. 74, 717-727 (2012).
59. Singh, I. & Rose, N. Biomarkers in psychiatry. Nature 460, 202-207 (2009).
60. Vogt, B. A. Pain and emotion interactions in subregions of the cingulate gyrus. Nat. Rev. Neurosci. 6, 533-544 (2005).
61. Davis, T. & Poldrack, R. A. Measuring neural representations with fMRI: practices and pitfalls. Ann. N.Y. Acad. Sci. 1296, 108-134 (2013).
62. Williams, K. D., Cheung, C. K. T. & Choi, W. Cyberostracism: effects of being ignored over the Internet. J. Pers. Soc. Psychol. 79, 748-762 (2000).
63. Ayduk, O., Mischel, W. & Downey, G. Attentional mechanisms linking rejection to hostile reactivity: the role of 'hot' versus 'cool' focus. Psychol. Sci. 13, 443-448 (2002).
64. Kross, E., Davidson, M., Weber, J. & Ochsner, K. Coping with emotions past: the neural bases of regulating affect associated with negative autobiographical memories. Biol. Psychiat. 65, 361-366 (2009).
65. Wager, T. D. et al. Placebo-induced changes in fMRI in the anticipation and experience of pain. Science 303, 1162-1167 (2004).
66. Op de Beeck, H. P. Against hyperacuity in brain reading: spatial smoothing does not hurt multivariate fMRI analyses? Neuroimage 49, 1943-1948 (2010).
67. Whitfield-Gabrieli, S. & Nieto-Castanon, A. Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2, 125-141 (2012).
68. Lindquist, K. A., Wager, T. D., Kober, H., Bliss-Moreau, E. & Barrett, L. F. The brain basis of emotion: a meta-Analytic review. Behav. Brain Sci. 35, 121-143 (2012).
69. Wager, T. D., Keller, M. C., Lacey, S. C. & Jonides, J. Increased sensitivity in neuroimaging analyses using robust regression. Neuroimage 26, 99-113 (2005).
70. Amunts, K. et al. Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat. Embryol. (Berl). 210, 343-352 (2005).