Advertisement

Research in Social Neuroscience: How Perceived Social Isolation, Ostracism, and Romantic Rejection Affect Our Brain

  • Stephanie CacioppoEmail author
  • John T. Cacioppo
Chapter

Abstract

Social exclusion has been defined broadly as the experience of being kept apart from others physically or emotionally. Our basic premise regarding the psychological study of social exclusion is that the brain is the key organ for forming, monitoring, maintaining, repairing, and replacing the salutary connections with others that Homo sapiens, as a social species, need to survive, reproduce, and leave a genetic legacy. Therefore, we focus here on functional magnetic resonance imaging (fMRI) studies of the neural correlates of perceptions of social isolation (i.e., loneliness), ostracism, and romantic rejection. Although this research suggests that the neural correlates may vary for these three forms of social exclusion, we discuss methodological and statistical issues that need to be addressed to determine the unique and common neural substrates across various forms of social exclusion.

Keywords

Romantic rejection Social isolation Loneliness Ostracism Social exclusion fMRI Electrical neuroimaging Neural markers Social threat Implicit attention 

References

  1. Adam, E. K., Hawkley, L. C., Kudielka, B. M., & Cacioppo, J. T. (2006). Day-to-day dynamics of experience-cortisol associations in a population-based sample of older adults. Proceedings of the National Academy of Sciences, 103, 17058–17063.CrossRefGoogle Scholar
  2. Aron, A., Fisher, H., Mashek, D. J., Strong, G., Li, H., & Brown, L. L. (2005). Reward, motivation, and emotion systems associated with early-stage intense romantic love. Journal of Neurophysiology, 94, 327–337.CrossRefPubMedGoogle Scholar
  3. Azevedo, F. A. C., Carvalho, L. R. B., Grinberg, L. T., Farfel, J. M., Ferretti, R. E. L., Leite, R. E. P., … Herculano-Houzel, S. (2009), Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. Journal of Comparative Neurology, 513, 532–541.Google Scholar
  4. Beadle, J. N., Brown, V., Keady, B., Tranel, D., & Paradiso, S. (2012). Trait empathy as a predictor of individual differences in perceived loneliness. Psychological Reports, 110, 3–15.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bickart, K. C., Hollenbeck, M. C., Barrett, L. F., & Dickerson, B. C. (2012). Intrinsic amygdala-cortical functional connectivity predicts social network size in humans. Journal of Neuroscience, 32, 14729–14741.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Button, K. S., Ioannidis, J. P., Mokrysz, C., Nosek, B. A., Flint, J., Robinson, E. S., & Munafò, M. R. (2013). Power failure: Why small sample size undermines the reliability of neuroscience. Nature Reviews Neuroscience, 14, 365–376.Google Scholar
  7. Cacioppo, J. T., & Cacioppo, S. (2013a). Minimal replicability, generalizability, and scientific advances in psychological science. European Journal of Personality, 27, 121–122.Google Scholar
  8. Cacioppo, J. T., & Cacioppo, S. (2013b). Social neuroscience. Perspectives on Psychological Science, 8, 668–670.CrossRefGoogle Scholar
  9. Cacioppo, J. T., Cacioppo, S., & Boomsma, D. I. (2014). Evolutionary mechanisms for loneliness. Cognition and Emotion, 28, 3–21.CrossRefPubMedGoogle Scholar
  10. Cacioppo, J. T., Cacioppo, S., Capitanio, J. P., & Cole, S. W. (2015). The neuroendocrinology of social isolation. Annual Review of Psychology, 66, 733–767.CrossRefPubMedGoogle Scholar
  11. Cacioppo, J. T., Cacioppo, S., Dulawa, S., & Palmer, A. (2014). Social neuroscience and its potential contribution to psychiatry. World Psychiatry, 13, 131–139.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cacioppo, J. T., Ernst, J. M., Burleson, M. H., McClintock, M. K., Malarkey, W. B., Hawkley, L. C., … Berntson, G. G. (2000). Lonely traits and concomitant physiological processes: The MacArthur Social Neuroscience Studies. International Journal of Psychophysiology, 35, 143–154.Google Scholar
  13. Cacioppo, J. T., Fowler, J. H., & Christakis, N. A. (2009). Alone in the crowd: The structure and spread of loneliness in a large social network. Journal of Personality and Social Psychology, 97, 977–991.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cacioppo, J. T., & Hawkley, L. C. (2009). Perceived social isolation and cognition. Trends in Cognitive Sciences, 13, 447–454.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cacioppo, J. T., Hawkley, L. C., & Berntson, G. G. (2003). The anatomy of loneliness. Current Directions in Psychological Science, 12, 71–74.CrossRefGoogle Scholar
  16. Cacioppo, J. T., Hawkley, L. C., Berntson, G. G., Ernst, J. M., Gibbs, A. C., Stickgold, R., & Hobson, J. A. (2002). Lonely days invade the nights: Social modulation of sleep efficiency. Psychological Science, 13, 384–387.Google Scholar
  17. Cacioppo, J. T., Hawkley, L. C., Ernst, J. M., Burleson, M., Berntson, G. G., Nouriani, B., & Spiegel, D. (2006). Loneliness within a nomological net: An evolutionary perspective. Journal of Research in Personality, 40, 1054–1085.Google Scholar
  18. Cacioppo, J. T., Norris, C. J., Decety, J., Monteleone, G., & Nusbaum, H. (2009). In the eye of the beholder: Individual differences in perceived social isolation predict regional brain activation to social stimuli. Journal of Cognitive Neuroscience, 21, 83–92.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Cacioppo, J. T., & Patrick, B. (2008). Loneliness: Human nature and the need for social connection. New York, NY: W. W. Norton & Company.Google Scholar
  20. Cacioppo, J. T., Tassinary, L. G., & Berntson, G. G. (in press). Handbook of Psychophysiology (4th ed.). New York, NY: Cambridge University Press.Google Scholar
  21. Cacioppo, S., Balogh, S., & Cacioppo, J. T. (2015). Implicit attention to negative social, in contrast to nonsocial, words in the Stroop task differs between individuals high and low in loneliness: Evidence from event-related brain microstates. Cortex, 70, 213–233.CrossRefPubMedGoogle Scholar
  22. Cacioppo, S., Bangee, M., Balogh, S., Cardenas-Iniguez, C., Qualter, P., & Cacioppo, J. T. (2015). Loneliness and implicit attention to social threat: A high performance electrical neuroimaging study. Cognitive Neuroscience. Advance online publication. doi:  10.1080/17588928.2015.1070136 Google Scholar
  23. Cacioppo, S., Bianchi-Demicheli, F., Frum, C., Pfaus, J. G., & Lewis, J. W. (2012). The common neural bases between sexual desire and love: A multilevel kernel density fMRI analysis. Journal of Sexual Medicine, 9, 1048–1054.CrossRefPubMedGoogle Scholar
  24. Cacioppo, S. & Cacioppo, J. T. (in press). Cognizance of the neuroimaging methods for studying the social brains. In S. S. Obhi & E. S. Cross (Eds.), Shared representations: Sensorimotor foundations of social life. Cambridge, UK: Cambridge University Press.Google Scholar
  25. Cacioppo, S., & Cacioppo, J. T. (2015). Dynamic spatiotemporal brain analyses using high-performance electrical neuroimaging, Part II: A step-by-step tutorial. Journal of Neuroscience Methods, 256, 184–197.CrossRefPubMedGoogle Scholar
  26. Cacioppo, S., Capitanio, J. P., & Cacioppo, J. T. (2014). Toward a neurology of loneliness. Psychological Bulletin, 140, 1464–1504.CrossRefPubMedGoogle Scholar
  27. Cacioppo, S., Frum, C., Asp, E., Weiss, R. M., Lewis, J. W., & Cacioppo, J. T. (2013). A quantitative meta-analysis of functional imaging studies of social rejection. Scientific Reports, 3, 2027.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Cole, S. W., Capitanio, J. P., Chun, K., Arevalo, J. M. G., Ma, J., & Cacioppo, J. T. (2015). Myeloid differentiation architecture of leukocyte transcriptome dynamics in perceived social isolation. Proceedings of the National Academy of Sciences, 112, 15142–15147.CrossRefGoogle Scholar
  29. Cooper, J. C., Dunne, S., Furey, T., & O’Doherty, J. P. (2014). The role of the posterior temporal and medial prefrontal cortices in mediating learning from romantic interest and rejection. Cerebral Cortex, 24, 2502–25011.CrossRefPubMedGoogle Scholar
  30. Davidson, R. J., & Cacioppo, J. T. (1992). New developments in the scientific study of emotion: An introduction to the special section. Psychological Science, 3, 21–22.CrossRefGoogle Scholar
  31. De Quervain, D. J. F., Fischbacher, U., Treyer, V., Schellhammer, M., Schnyder, U., Buck, A., & Fehr, E. (2004). The neural basis of altruistic punishment. Science, 305, 1254–1258.Google Scholar
  32. Delgado, M. R., Miller, M. M., Inati, S., & Phelps, E. A. (2005). An fMRI study of reward-related probability learning. NeuroImage, 24, 862–873.CrossRefPubMedGoogle Scholar
  33. Duck, S., Pond, K., & Leatham, G. (1994). Loneliness and the evaluation of relational events. Journal of Social and Personal Relationships, 11, 253–276.CrossRefGoogle Scholar
  34. Eisenberger, N. I. (2012). The pain of social disconnection: Examining the shared neural underpinnings of physical and social pain. Nature Reviews Neuroscience, 13, 421–434.CrossRefPubMedGoogle Scholar
  35. Eisenberger, N. I., & Cole, S. W. (2012). Social neuroscience and health: Neurophysiological mechanisms linking social ties with physical health. Nature Neuroscience, 15, 1–6.CrossRefGoogle Scholar
  36. Eisenberger, N. I., Liberman, M. D., & Williams, K. D. (2003). Does rejection hurt? An FMRI study of social exclusion. Science, 302, 290–292.CrossRefPubMedGoogle Scholar
  37. Fisher, H. E., Brown, L. L., Aron, A., Strong, G., & Mashek, D. (2010). Reward, addiction, and emotion regulation systems associated with rejection in love. Journal of Neurophysiology, 104, 51–60.CrossRefPubMedGoogle Scholar
  38. Fliessbach, K., Weber, B., Trautner, P., Dohmen, T., Sunde, U., Elger, C. E., & Falk, A. (2007). Social comparison affects reward-related brain activity in the human ventral striatum. Science, 318, 1305–1308.Google Scholar
  39. Gillath, O., Bunge, S. A., Shaver, P. R., Wendelken, C., & Mikulincer, M. (2005). Attachment-style differences in the ability to suppress negative thoughts: Exploring the neural correlates. NeuroImage, 28, 835–847.CrossRefPubMedGoogle Scholar
  40. Goossens, L., van Roekel, E., Verhagen, M., Cacioppo, J. T., Cacioppo, S., Maes, M., & Boomsma, D. I. (2015). The genetics of loneliness: Linking evolutionary theory to genome-wide genetics, epigenomics, and social science. Perspectives on Psychological Science, 10, 213–226.Google Scholar
  41. Grippo, A. J., Ihm, E., Wardwell, J., McNeal, N., Scotti, M. L., Moenk, D. A., … & Preihs, K. (2014). The effects of environmental enrichment on depressive and anxiety-relevant behaviors in socially isolated prairie voles. Psychosomatic Medicine, 76, 277–284.Google Scholar
  42. Hofer, M. A. (2009). Developmental neuroscience. In G. G. Berntson & J. T. Cacioppo (Eds.), Handbook of neuroscience for the behavioral sciences (pp. 12–31). Hoboken, NJ: John Wiley and Sons.Google Scholar
  43. Holt-Lunstad, J., Smith, T. B., Baker, M., Harris, T., & Stephenson, D. (2015). Loneliness and social isolation as risk factors for mortality: A meta-analytic review. Perspectives on Psychological Science, 10, 227–237.CrossRefPubMedGoogle Scholar
  44. Ioannou, C. C., Guttal, V., & Couzin, I. D. (2012). Predatory fish select for coordinated collective motion in virtual prey. Science, 337, 1212–1215.CrossRefPubMedGoogle Scholar
  45. Jones, W. H., Freemon, J. E., & Goswick, R. A. (1981). The persistence of loneliness: Self and other determinants. Journal of Personality, 49, 27–48.CrossRefGoogle Scholar
  46. Kanai, R., Bahrami, B., Duchaine, B., Janik, A., Banissy, M. J., & Rees, G. (2012). Brain structure links loneliness to social perception. Current Biology, 22, 1975–1979.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kanai, R., Bahrami, B., Roylance, R., & Rees, G. (2012). Online social network size is reflected in human brain structure. Proceedings of the Royal Society: Biological Science, 279, 1327–1334.CrossRefGoogle Scholar
  48. Kaushal, N., Nair, D., Gozal, D., & Ramesh, V. (2012). Socially isolated mice exhibit a blunted homeostatic sleep response to acute sleep deprivation compared to socially paired mice. Brain Research, 1454, 65–79.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kawamoto, T., Onoda, K., Nakashima, K. I., Nittono, H., Yamaguchi, S., & Ura, M. (2012). Is dorsal anterior cingulate activation in response to social exclusion due to expectancy violation? An fMRI study. Frontiers in Evolutionary Neuroscience, 4, 11.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Klumpp, H., Angstadt, M., & Phan, K. L. (2012). Insula reactivity and connectivity to anterior cingulate cortex when processing threat in generalized social anxiety disorder. Biological Psychology, 89, 273–276.CrossRefPubMedGoogle Scholar
  51. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International Affective Picture System (IAPS): Affective ratings of pictures and instruction manual (Technical Report A-8). Gainesville, FL: University of Florida.Google Scholar
  52. Lau, S., & Gruen, G. E. (1992). The social stigma of loneliness: Effect of target person’s and perceiver’s sex. Personality and Social Psychology Bulletin, 18, 182–189.CrossRefGoogle Scholar
  53. Leyton, M. (2007). Conditioned and sensitized responses to stimulant drugs in humans. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 31, 1601–1613.CrossRefPubMedGoogle Scholar
  54. Luo, Y., Hawkley, L. C., Waite, L. J., & Cacioppo, J. T. (2012). Loneliness, health, and mortality in old age: A national longitudinal study. Social Science & Medicine, 74, 907–914.CrossRefGoogle Scholar
  55. Mendoza, S. P., & Mason, W. A. (1986). Contrasting responses to intruders and to involuntary separation by monogamous and polygynous New World monkeys. Physiology & Behavior, 38, 795–801.CrossRefGoogle Scholar
  56. O’Doherty, J. P. (2004). Reward representations and reward-related learning in the human brain: Insights from neuroimaging. Current Opinion in Neurobiology, 14, 769–776.CrossRefPubMedGoogle Scholar
  57. Peplau, L. A., Russell, D., & Heim, M. (1979). The experience of loneliness. In I. H. Frieze, D. Bar-Tal, & J. S. Carroll (Eds.), New approaches to social problems: Applications of attribution theory (pp. 53–78). San Francisco, CA: Jossey-Bass.Google Scholar
  58. Powers, K. E., Wagner, D. D., Norris, C. J., & Heatherton, T. F. (2013). Socially excluded individuals fail to recruit medial prefrontal cortex for negative social scenes. Social Cognitive and Affective Neuroscience, 8, 151–157.CrossRefPubMedGoogle Scholar
  59. Rilling, J., Gutman, D., Zeh, T., Pagnoni, G., Berns, G., & Kilts, C. (2002). A neural basis for social cooperation. Neuron, 35, 395–504.CrossRefPubMedGoogle Scholar
  60. Riva, P., Williams, K. D., & Gallucci, M. (2014). The relationship between fear of social and physical threat and its effect on social distress and physical pain perception. Pain, 155, 485–493.CrossRefPubMedGoogle Scholar
  61. Rotenberg, K. (1994). Loneliness and interpersonal trust. Journal of Social and Clinical Psychology, 13, 152–173.CrossRefGoogle Scholar
  62. Rotenberg, K. J., Gruman, J. A., & Ariganello, M. (2002). Behavioral confirmation of the loneliness stereotype. Basic and Applied Social Psychology, 24, 81–89.CrossRefGoogle Scholar
  63. Rotenberg, K. J., & Kmill, J. (1992). Perception of lonely and non-lonely persons as a function of individual differences in loneliness. Journal of Social and Personal Relationships, 9, 325–330.CrossRefGoogle Scholar
  64. Rotge, J., Lemogne, C., Hinfray, S., Huguet, P., Grynszpan, O., Tartour, … Fossati, P. (2015). A meta-analysis of the anterior cingulate contribution to social pain. Social Cognitive and Affective Neuroscience, 10, 19–27.Google Scholar
  65. Sandrone, S., Bacigaluppi, M., Galloni, M. R., & Martino, G. (2012). Angelo Mosso (1846–1910). Journal of Neurology, 259, 2513–2514.CrossRefPubMedGoogle Scholar
  66. Sarter, M., Berntson, G. G., & Cacioppo, J. T. (1996). Brain imaging and cognitive neuroscience: Toward strong inference in attributing function to structure. American Psychologist, 51, 13–21.CrossRefPubMedGoogle Scholar
  67. Seymour, B., Daw, N., Dayan, P., Singer, T., & Dolan, R. (2007). Differential encoding of losses and gains in the human striatum. Journal of Neuroscience, 27, 4826–4831.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Somerville, L. H., Heatherton, T. F., & Kelley, W. M. (2006). Anterior cingulate cortex responds differentially to expectancy violation and social rejection. Nature Neuroscience, 9, 1007–1008.CrossRefPubMedGoogle Scholar
  69. Wang, Z., Faith, M., Patterson, F., Tang, K., Kerrin, K., Wileyto, E. P., … Lerman, C. (2007). Neural substrates of abstinence-induced cigarette cravings in chronic smokers. Journal of Neuroscience, 27, 14035–14040.Google Scholar
  70. Weiss, R. S. (1973). Loneliness: The experience of emotional and social isolation. Cambridge, MA: MIT Press.Google Scholar
  71. Woo, C. W., Koban, L., Kross, E., Lindquist, M. A., Banich, M. T., Ruzic, L., … Wager, T. D. (2014). Separate neural representations for physical pain and social rejection. Nature Communications, 5, 5380. Google Scholar
  72. Yamada, M., & Decety, J. (2009). Unconscious affective processing and empathy: An investigation of subliminal priming on the detection of painful facial expressions. Pain, 143, 71–75.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.The University of ChicagoChicagoUSA

Personalised recommendations