Assessment of social transmission of threats in humans using observational fear conditioning


Across the human life span, fear is often acquired indirectly by observation of the emotional expressions of others. The observational fear conditioning protocol was previously developed as a laboratory model for investigating socially acquired threat responses. This protocol serves as a suitable alternative to the widely used Pavlovian fear conditioning, in which threat responses are acquired through direct experiences. In the observational fear conditioning protocol, the participant (observer) watches a demonstrator being presented with a conditioned stimulus (CS) paired with an aversive unconditioned stimulus (US). The expression of threat learning is measured as the conditioned response (CR) expressed by the observer in the absence of the demonstrator. CRs are commonly measured as skin conductance responses, but behavioral and neural measures have also been implemented. The experimental procedure is suitable for divergent populations, can be administered by a graduate student and takes 40 min. Similar protocols are used in animals, emphasizing its value as a translational tool for studying socioemotional learning.

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Figure 1: Design and outcome measures of the observational fear conditioning protocol.
Figure 2: Prototypical SCRs.


  1. 1

    LeDoux, J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155–184 (2000).

    CAS  Article  Google Scholar 

  2. 2

    Kandel, E.R., Dudai, Y. & Mayford, M.R. The molecular and systems biology of memory. Cell 157, 163–186 (2014).

    CAS  Article  Google Scholar 

  3. 3

    Askew, C. & Field, A.P. Vicarious learning and the development of fears in childhood. Behav. Res. Ther. 45, 2616–2627 (2007).

    Article  Google Scholar 

  4. 4

    Olsson, A. & Phelps, E.A. Social learning of fear. Nat. Neurosci. 10, 1095–1102 (2007).

    CAS  Article  Google Scholar 

  5. 5

    Mineka, S. & Ohman, A. Phobias and preparedness: the selective, automatic, and encapsulated nature of fear. Biol. Psychiatry 52, 927 (2002).

    Article  Google Scholar 

  6. 6

    Olsson, A., Nearing, K.I. & Phelps, E.A. Learning fears by observing others: the neural systems of social fear transmission. Soc. Cogn. Affect. Neurosci. 2, 3–11 (2007).

    Article  Google Scholar 

  7. 7

    Olsson, A. & Phelps, E.A. Learned fear of 'unseen' faces after Pavlovian, observational, and instructed fear. Psychol. Sci. 15, 822–828 (2004).

    Article  Google Scholar 

  8. 8

    Olsson, A. et al. Vicarious fear learning depends on empathic appraisals and trait empathy. Psychol. Sci. 27, 25–33 (2016).

    Article  Google Scholar 

  9. 9

    Golkar, A., Castro, V. & Olsson, A. Social learning of fear and safety is determined by the demonstrator's racial group. Biol. Lett. 11, 20140817 (2015).

    Article  Google Scholar 

  10. 10

    Golkar, A. & Olsson, A. Immunization against social fear learning. J. Exp. Psychol. Gen. 145, 665–671 (2016).

    Article  Google Scholar 

  11. 11

    Kleberg, J.L., Selbing, I., Lundqvist, D., Hofvander, B. & Olsson, A. Spontaneous eye movements and trait empathy predict vicarious learning of fear. Int. J. Psychophysiol. 98, 577–583 (2015).

    Article  Google Scholar 

  12. 12

    Olsson, A., Kopsida, E., Sorjonen, K. & Savic, I. Testosterone and estrogen impact social evaluations and vicarious emotions: a double-blind placebo-controlled study. Emotion 16, 515–523 (2016).

    Article  Google Scholar 

  13. 13

    Leadbeater, E. & Chittka, L. Social learning in insects — from miniature brains to consensus building. Curr. Biol. 17, R703–R713 (2007).

    CAS  Article  Google Scholar 

  14. 14

    Mineka, S., Davidson, M., Cook, M. & Keir, R. Observational conditioning of snake fear in rhesus monkeys. J. Abnorm. Psychol. 93, 355–372 (1984).

    CAS  Article  Google Scholar 

  15. 15

    Askew, C. & Field, A.P. The vicarious learning pathway to fear 40 years on. Clin. Psychol. Rev. 28, 1249–1265 (2008).

    Article  Google Scholar 

  16. 16

    Bandura, A. Social Learning Theory (General Learning Press, 1977).

  17. 17

    Rachman, S. The conditioning theory of fear-acquisition: a critical examination. Behav. Res. Ther. 15, 375–387 (1977).

    CAS  Article  Google Scholar 

  18. 18

    Raio, C.M. & Phelps, E.A. Brain Mapping: An Encyclopedic Reference (Elsevier, 2007).

  19. 19

    Boyd, R., Richerson, P.J. & Henrich, J. The cultural niche: why social learning is essential for human adaptation. Proc. Natl. Acad. Sci. USA 108, 10918–10925 (2011).

    CAS  Article  Google Scholar 

  20. 20

    Lindström, B., Selbing, I. & Olsson, A. Co-evolution of social learning and evolutionary preparedness in dangerous environments. PLoS One 11, e0160245 (2016).

    Article  Google Scholar 

  21. 21

    Gerull, F.C. & Rapee, R.M. Mother knows best: effects of maternal modelling on the acquisition of fear and avoidance behaviour in toddlers. Behav. Res. Ther. 40, 279–287 (2002).

    Article  Google Scholar 

  22. 22

    Busso, D.S., McLaughlin, K.A. & Sheridan, M.A. Media exposure and sympathetic nervous system reactivity predict PTSD symptoms after the Boston marathon bombings. Depress. Anxiety 31, 551–558 (2014).

    Article  Google Scholar 

  23. 23

    Comer, J.S., Furr, J.M., Beidas, R.S., Babyar, H.M. & Kendall, P.C. Media use and children's perceptions of societal threat and personal vulnerability. J. Clin. Child Adolesc. Psychol. 37, 622–630 (2008).

    Article  Google Scholar 

  24. 24

    Hoven, C.W. et al. Psychopathology among New York city public school children 6 months after September 11. Arch. Gen. Psychiatry 62, 545–552 (2005).

    Article  Google Scholar 

  25. 25

    Otto, M.W. et al. Posttraumatic stress disorder symptoms following media exposure to tragic events: impact of 9/11 on children at risk for anxiety disorders. J. Anxiety Disord. 21, 888–902 (2007).

    Article  Google Scholar 

  26. 26

    Pfefferbaum, B. et al. Media exposure in children one hundred miles from a terrorist bombing. Ann. Clin. Psychiatry 15, 1–8 (2003).

    Article  Google Scholar 

  27. 27

    Pfefferbaum, B. et al. Television exposure in children after a terrorist incident. Psychiatry 64, 202–211 (2001).

    CAS  Article  Google Scholar 

  28. 28

    Freedy, J.R., Resnick, H.S., Kilpatrick, D.G., Dansky, B.S. & Tidwell, R.P. The psychological adjustment of recent crime victims in the criminal justice system. J. Interpers. Violence 9, 450–468 (1994).

    Article  Google Scholar 

  29. 29

    Murphy, S.A. et al. PTSD among bereaved parents following the violent deaths of their 12- to 28-year-old children: a longitudinal prospective analysis. J. Traum. Stress 12, 273–291 (1999).

    CAS  Article  Google Scholar 

  30. 30

    Neria, Y. et al. The mental health consequences of disaster-related loss: findings from primary care one year after the 9/11 terrorist attacks. Psychiatry 71, 339–348 (2008).

    Article  Google Scholar 

  31. 31

    Neria, Y. et al. Prevalence and psychological correlates of complicated grief among bereaved adults 2.5–3.5 years after September 11th attacks. J. Traum. Stress 20, 251–262 (2007).

    Article  Google Scholar 

  32. 32

    Sutker, P.B., Uddo, M., Brailey, K., Vasterling, J.J. & Errera, P. Psychopathology in war-zone deployed and nondeployed Operation Desert Storm troops assigned graves registration duties. J. Abnorm. Psychol. 103, 383–390 (1994).

    CAS  Article  Google Scholar 

  33. 33

    Chang, C.-M. et al. Posttraumatic distress and coping strategies among rescue workers after an earthquake. J. Nerv. Ment. Dis. 191, 391–398 (2003).

    Article  Google Scholar 

  34. 34

    Breslau, N. & Kessler, R.C. The stressor criterion in DSM-IV posttraumatic stress disorder: an empirical investigation. Biol. Psychiatry 50, 699–704 (2001).

    CAS  Article  Google Scholar 

  35. 35

    Friedman, M.J., Resick, P.A., Bryant, R.A. & Brewin, C.R. Considering PTSD for DSM-5. Depress. Anxiety 28, 750–769 (2011).

    Article  Google Scholar 

  36. 36

    American Psychiatric Association & others Diagnostic and Statistical Manual of Mental Disorders (DSM) 5 (American Psychiatric Association, 2013).

  37. 37

    Phelps, E.A. et al. Activation of the left amygdala to a cognitive representation of fear. Nat. Neurosci. 4, 437–441 (2001).

    CAS  Article  Google Scholar 

  38. 38

    Schmitz, A. & Grillon, C. Assessing fear and anxiety in humans using the threat of predictable and unpredictable aversive events (the NPU-threat test). Nat. Protoc. 7, 527–532 (2012).

    CAS  Article  Google Scholar 

  39. 39

    Meffert, H., Brislin, S.J., White, S.F. & Blair, J.R. Prediction errors to emotional expressions: the roles of the amygdala in social referencing. Soc. Cogn. Affect. Neurosci. 10, 537–544 (2015).

    Article  Google Scholar 

  40. 40

    Hooker, C.I., Verosky, S.C., Miyakawa, A., Knight, R.T. & D'Esposito, M. The influence of personality on neural mechanisms of observational fear and reward learning. Neuropsychologia 46, 2709–2724 (2008).

    Article  Google Scholar 

  41. 41

    Helsen, K., Vlaeyen, J.W.S. & Goubert, L. Indirect acquisition of pain-related fear: an experimental study of observational learning using coloured cold metal bars. PLoS One 10, e0117236 (2015).

    Article  Google Scholar 

  42. 42

    Helsen, K., Goubert, L., Peters, M.L. & Vlaeyen, J.W.S. Observational learning and pain-related fear: an experimental study with colored cold pressor tasks. J. Pain 12, 1230–1239 (2011).

    Article  Google Scholar 

  43. 43

    Egorova, N. et al. Not seeing or feeling is still believing: conscious and non-conscious pain modulation after direct and observational learning. Sci. Rep. 5, 16809 (2015).

    CAS  Article  Google Scholar 

  44. 44

    Reynolds, G., Field, A.P. & Askew, C. Learning to fear a second-order stimulus following vicarious learning. Cogn. Emot. 31, 1–8 (2015).

    Google Scholar 

  45. 45

    Cameron, G., Schlund, M.W. & Dymond, S. Generalization of socially transmitted and instructed avoidance. Front. Behav. Neurosci. 9, 159 (2015).

  46. 46

    LeDoux, J. Rethinking the emotional brain. Neuron 73, 653–676 (2012).

    CAS  Article  Google Scholar 

  47. 47

    LeDoux, J.E. The slippery slope of fear. Trends Cogn. Sci. 17, 155–156 (2013).

    Article  Google Scholar 

  48. 48

    Cook, M. & Mineka, S. Selective associations in the observational conditioning of fear in rhesus monkeys. J. Exp. Psychol. Anim. Behav. Process. 16, 372–389 (1990).

    CAS  Article  Google Scholar 

  49. 49

    Cook, M. & Mineka, S. Second-order conditioning and overshadowing in the observational conditioning of fear in monkeys. Behav. Res. Ther. 25, 349–364 (1987).

    CAS  Article  Google Scholar 

  50. 50

    Mineka, S. & Cook, M. Mechanisms involved in the observational conditioning of fear. J. Exp. Psychol. Gen. 122, 23–38 (1993).

    CAS  Article  Google Scholar 

  51. 51

    Berger, S.M. Conditioning through vicarious instigation. Psychol. Rev. 69, 450–466 (1962).

    Article  Google Scholar 

  52. 52

    Hygge, S. Information about the model's unconditioned stimulus and response in vicarious classical conditioning. J. Pers. Soc. Psychol. 33, 764–771 (1976).

    CAS  Article  Google Scholar 

  53. 53

    Hygge, S. & Öhman, A. Conditioning of electrodermal responses through vicarious instigation and through perceived threat to a performer. Scand. J. Psychol. 17, 65–72 (1976).

    Article  Google Scholar 

  54. 54

    Golkar, A., Haaker, J., Selbing, I. & Olsson, A. Neural signals of vicarious extinction learning. Soc. Cogn. Affect. Neurosci. 11, 1541–1549 (2016).

    Article  Google Scholar 

  55. 55

    Golkar, A., Selbing, I., Flygare, O., Öhman, A. & Olsson, A. Other people as means to a safe end vicarious extinction blocks the return of learned fear. Psychol. Sci. 24, 2182–2190 (2013).

    Article  Google Scholar 

  56. 56

    Olsson, A. & Ochsner, K.N. The role of social cognition in emotion. Trends Cogn. Sci. 12, 65–71 (2008).

    Article  Google Scholar 

  57. 57

    Ohman, A. Nonconscious control of autonomic responses: a role for Pavlovian conditioning? Biol. Psychol. 27, 113–135 (1988).

    CAS  Article  Google Scholar 

  58. 58

    Prokasy, W.F. First interval skin conductance responses: conditioned or orienting responses? Psychophysiology 14, 360–367 (1977).

    CAS  Article  Google Scholar 

  59. 59

    Lonsdorf, T.B. et al. Don't fear ‘fear conditioning': methodological considerations for the design and analysis of studies on human fear acquisition, extinction, and return of fear. Neurosci. Biobehav. Rev. 77, 247–285 (2017).

    Article  Google Scholar 

  60. 60

    Henson, R. Efficient experimental design for fMRI. In Statistical Parametric Mapping: The Analysis of Functional Brain Images (eds. William Penny, Karl Friston, John Ashburner, Stefan Kiebel & Thomas Nichols) (Elsevier, 2007).

  61. 61

    Friston, K.J. et al. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 189–210 (1995).

    Article  Google Scholar 

  62. 62

    Haaker, J., Yi, J., Petrovic, P. & Olsson, A. Endogenous opioids regulate social threat learning in humans. Nat. Commun. (in the press).

  63. 63

    Lang, P.J., Bradley, M.M. & Cuthbert, B.N. Emotion, attention, and the startle reflex. Psychol. Rev. 97, 377–395 (1990).

    CAS  Article  Google Scholar 

  64. 64

    Blumenthal, T.D. et al. Committee report: guidelines for human startle eyeblink electromyographic studies. Psychophysiology 42, 1–15 (2005).

    Article  Google Scholar 

  65. 65

    Davis, M. Neural systems involved in fear-potentiated startle. Ann. N. Y. Acad. Sci. 563, 165–183 (1989).

    CAS  Article  Google Scholar 

  66. 66

    Lindner, K. et al. Fear-potentiated startle processing in humans: parallel fMRI and orbicularis EMG assessment during cue conditioning and extinction. Int. J. Psychophysiol. 98, 535–545 (2015).

    Article  Google Scholar 

  67. 67

    Grillon, C. & Davis, M. Fear-potentiated startle conditioning in humans: explicit and contextual cue conditioning following paired versus unpaired training. Psychophysiology 34, 451–458 (1997).

    CAS  Article  Google Scholar 

  68. 68

    Hamm, A.O. & Vaitl, D. Affective learning: awareness and aversion. Psychophysiology 33, 698–710 (1996).

    CAS  Article  Google Scholar 

  69. 69

    Bruchey, A.K., Jones, C.E. & Monfils, M.-H. Fear conditioning by-proxy: social transmission of fear during memory retrieval. Behav. Brain Res. 214, 80–84 (2010).

    Article  Google Scholar 

  70. 70

    Jones, C.E., Riha, P.D., Gore, A.C. & Monfils, M.-H. Social transmission of Pavlovian fear: fear-conditioning by-proxy in related female rats. Anim. Cogn. 17, 827–834 (2014).

    Article  Google Scholar 

  71. 71

    Jeon, D. et al. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat. Neurosci. 13, 482–488 (2010).

    CAS  Article  Google Scholar 

  72. 72

    Jeon, D. & Shin, H.-S. A mouse model for observational fear learning and the empathetic response. Curr. Protoc. Neurosci. Chapter 8, Unit 8.27 (2011).

  73. 73

    Debiec, J. & Sullivan, R.M. Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear. Proc. Natl. Acad. Sci. USA 111, 12222–12227 (2014).

    CAS  Article  Google Scholar 

  74. 74

    Knapska, E. et al. Between-subject transfer of emotional information evokes specific pattern of amygdala activation. Proc. Natl. Acad. Sci. USA 103, 3858–3862 (2006).

    CAS  Article  Google Scholar 

  75. 75

    Reynolds, G., Field, A.P. & Askew, C. Preventing the development of observationally learnt fears in children by devaluing the model's negative response. J. Abnorm. Child Psychol. 43, 1355–1367 (2015).

    Article  Google Scholar 

  76. 76

    Zhang, S., Mano, H., Ganesh, G., Robbins, T. & Seymour, B. Dissociable learning processes underlie human pain conditioning. Curr. Biol. 26, 52–58 (2016).

    Article  Google Scholar 

  77. 77

    Lundqvist, D., Flykt, A. & Öhman, A. The Karolinska Directed Emotional Faces-KDEF (CD-ROM from Department of Clinical Neuroscience, Psychology Section, Karolinska Institutet ISBN 91-630-7164-9 1998).

  78. 78

    Curtin, J.J., Lozano, D.L. & Allen, J.J. The psychophysiological laboratory. Handbook of Emotion Elicitation and Assessment 398–425 (Oxford University Press, 2007).

  79. 79

    Lykken, D.T. & Venables, P.H. Direct measurement of skin conductance: a proposal for standardization. Psychophysiology 8, 656–672 (1971).

    CAS  Article  Google Scholar 

  80. 80

    Boucsein, W. et al. Publication recommendations for electrodermal measurements. Psychophysiology 49, 1017–1034 (2012).

    Article  Google Scholar 

  81. 81

    Fowles, D.C. et al. Committee report. Publication recommendations for electrodermal measurements. Psychophysiology 18, 232–239 (1981).

    CAS  Article  Google Scholar 

  82. 82

    Mobbs, D. et al. A key role for similarity in vicarious reward. Science 324, 900 (2009).

    CAS  Article  Google Scholar 

  83. 83

    Behrens, T.E., Hunt, L.T., Woolrich, M.W. & Rushworth, M.F. Associative learning of social value. Nature 456, 245–249 (2008).

    CAS  Article  Google Scholar 

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This research was supported by the European Research Council (Independent Starting Grant 284366; Emotional Learning in Social Interaction to A.O.), the Knut and Alice Wallenberg Foundation (KAW 2014.0237 to A.O.), the German Research Foundation (Research Stipend HA 7470/1-1 to J.H.) and the Swedish Research Council (2015-00312 to A.G.).

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A.O. developed the original version of the observational fear conditioning protocol. A.G., I.S. and A.O. developed the current protocol, and all authors contributed to paradigm modifications. J.H. drafted the manuscript and all authors commented on the manuscript.

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Correspondence to Andreas Olsson.

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Haaker, J., Golkar, A., Selbing, I. et al. Assessment of social transmission of threats in humans using observational fear conditioning. Nat Protoc 12, 1378–1386 (2017).

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