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

Journal name:
Nature Protocols
Year published:
Published online


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.

At a glance


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

    (a) General design of the observational fear conditioning protocol, depicting the observer (participant) in shaded gray, first watching the demonstrator's responses to the CS–US pairings (observational learning stage), and then being exposed to the CS (direct-expression stage). (b) The specific timing of the CS (yellow and blue areas) and US onsets (the shaded area refers to the presentation of the observational US while the CS is present; the expression of discomfort by the demonstrator might be longer) and (c) prototypical resulting SCR during the presentation of the CS+ and CS. Permission for the outlined experiment was obtained from the Regional Ethical Review Board Stockholm (

  2. Prototypical SCRs.
    Figure 2: Prototypical SCRs.

    (a) SCRs to the observational CSs, including the SCR to the observational US. (b) SCRs to the direct CS presentations. Black dashed lines illustrate the scoring of the amplitude as the difference between peak and foot point after the stimulus onset. Circles demark the foot point and peak. Obs, observational.

  3. This figure illustrates the prototypical placement of electrodes
    Supplementary Fig. 1: This figure illustrates the prototypical placement of electrodes


  1. Illustration of the observational learning stage.
    Video 1: Illustration of the observational learning stage.
  2. Illustration of the direct-expression stage.
    Video 2: Illustration of the direct-expression stage.


  1. LeDoux, J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155184 (2000).
  2. Kandel, E.R., Dudai, Y. & Mayford, M.R. The molecular and systems biology of memory. Cell 157, 163186 (2014).
  3. Askew, C. & Field, A.P. Vicarious learning and the development of fears in childhood. Behav. Res. Ther. 45, 26162627 (2007).
  4. Olsson, A. & Phelps, E.A. Social learning of fear. Nat. Neurosci. 10, 10951102 (2007).
  5. Mineka, S. & Ohman, A. Phobias and preparedness: the selective, automatic, and encapsulated nature of fear. Biol. Psychiatry 52, 927 (2002).
  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, 311 (2007).
  7. Olsson, A. & Phelps, E.A. Learned fear of 'unseen' faces after Pavlovian, observational, and instructed fear. Psychol. Sci. 15, 822828 (2004).
  8. Olsson, A. et al. Vicarious fear learning depends on empathic appraisals and trait empathy. Psychol. Sci. 27, 2533 (2016).
  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).
  10. Golkar, A. & Olsson, A. Immunization against social fear learning. J. Exp. Psychol. Gen. 145, 665671 (2016).
  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, 577583 (2015).
  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, 515523 (2016).
  13. Leadbeater, E. & Chittka, L. Social learning in insects — from miniature brains to consensus building. Curr. Biol. 17, R703R713 (2007).
  14. Mineka, S., Davidson, M., Cook, M. & Keir, R. Observational conditioning of snake fear in rhesus monkeys. J. Abnorm. Psychol. 93, 355372 (1984).
  15. Askew, C. & Field, A.P. The vicarious learning pathway to fear 40 years on. Clin. Psychol. Rev. 28, 12491265 (2008).
  16. Bandura, A. Social Learning Theory (General Learning Press, 1977).
  17. Rachman, S. The conditioning theory of fear-acquisition: a critical examination. Behav. Res. Ther. 15, 375387 (1977).
  18. Raio, C.M. & Phelps, E.A. Brain Mapping: An Encyclopedic Reference (Elsevier, 2007).
  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, 1091810925 (2011).
  20. Lindström, B., Selbing, I. & Olsson, A. Co-evolution of social learning and evolutionary preparedness in dangerous environments. PLoS One 11, e0160245 (2016).
  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, 279287 (2002).
  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, 551558 (2014).
  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, 622630 (2008).
  24. Hoven, C.W. et al. Psychopathology among New York city public school children 6 months after September 11. Arch. Gen. Psychiatry 62, 545552 (2005).
  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, 888902 (2007).
  26. Pfefferbaum, B. et al. Media exposure in children one hundred miles from a terrorist bombing. Ann. Clin. Psychiatry 15, 18 (2003).
  27. Pfefferbaum, B. et al. Television exposure in children after a terrorist incident. Psychiatry 64, 202211 (2001).
  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, 450468 (1994).
  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, 273291 (1999).
  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, 339348 (2008).
  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, 251262 (2007).
  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, 383390 (1994).
  33. Chang, C.-M. et al. Posttraumatic distress and coping strategies among rescue workers after an earthquake. J. Nerv. Ment. Dis. 191, 391398 (2003).
  34. Breslau, N. & Kessler, R.C. The stressor criterion in DSM-IV posttraumatic stress disorder: an empirical investigation. Biol. Psychiatry 50, 699704 (2001).
  35. Friedman, M.J., Resick, P.A., Bryant, R.A. & Brewin, C.R. Considering PTSD for DSM-5. Depress. Anxiety 28, 750769 (2011).
  36. American Psychiatric Association & others Diagnostic and Statistical Manual of Mental Disorders (DSM) 5 (American Psychiatric Association, 2013).
  37. Phelps, E.A. et al. Activation of the left amygdala to a cognitive representation of fear. Nat. Neurosci. 4, 437441 (2001).
  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, 527532 (2012).
  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, 537544 (2015).
  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, 27092724 (2008).
  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).
  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, 12301239 (2011).
  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).
  44. Reynolds, G., Field, A.P. & Askew, C. Learning to fear a second-order stimulus following vicarious learning. Cogn. Emot. 31, 18 (2015).
  45. Cameron, G., Schlund, M.W. & Dymond, S. Generalization of socially transmitted and instructed avoidance. Front. Behav. Neurosci. 9, 159 (2015).
  46. LeDoux, J. Rethinking the emotional brain. Neuron 73, 653676 (2012).
  47. LeDoux, J.E. The slippery slope of fear. Trends Cogn. Sci. 17, 155156 (2013).
  48. Cook, M. & Mineka, S. Selective associations in the observational conditioning of fear in rhesus monkeys. J. Exp. Psychol. Anim. Behav. Process. 16, 372389 (1990).
  49. Cook, M. & Mineka, S. Second-order conditioning and overshadowing in the observational conditioning of fear in monkeys. Behav. Res. Ther. 25, 349364 (1987).
  50. Mineka, S. & Cook, M. Mechanisms involved in the observational conditioning of fear. J. Exp. Psychol. Gen. 122, 2338 (1993).
  51. Berger, S.M. Conditioning through vicarious instigation. Psychol. Rev. 69, 450466 (1962).
  52. Hygge, S. Information about the model's unconditioned stimulus and response in vicarious classical conditioning. J. Pers. Soc. Psychol. 33, 764771 (1976).
  53. Hygge, S. & Öhman, A. Conditioning of electrodermal responses through vicarious instigation and through perceived threat to a performer. Scand. J. Psychol. 17, 6572 (1976).
  54. Golkar, A., Haaker, J., Selbing, I. & Olsson, A. Neural signals of vicarious extinction learning. Soc. Cogn. Affect. Neurosci. 11, 15411549 (2016).
  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, 21822190 (2013).
  56. Olsson, A. & Ochsner, K.N. The role of social cognition in emotion. Trends Cogn. Sci. 12, 6571 (2008).
  57. Ohman, A. Nonconscious control of autonomic responses: a role for Pavlovian conditioning? Biol. Psychol. 27, 113135 (1988).
  58. Prokasy, W.F. First interval skin conductance responses: conditioned or orienting responses? Psychophysiology 14, 360367 (1977).
  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, 247285 (2017).
  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. Friston, K.J. et al. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 189210 (1995).
  62. Haaker, J., Yi, J., Petrovic, P. & Olsson, A. Endogenous opioids regulate social threat learning in humans. Nat. Commun. (in the press).
  63. Lang, P.J., Bradley, M.M. & Cuthbert, B.N. Emotion, attention, and the startle reflex. Psychol. Rev. 97, 377395 (1990).
  64. Blumenthal, T.D. et al. Committee report: guidelines for human startle eyeblink electromyographic studies. Psychophysiology 42, 115 (2005).
  65. Davis, M. Neural systems involved in fear-potentiated startle. Ann. N. Y. Acad. Sci. 563, 165183 (1989).
  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, 535545 (2015).
  67. Grillon, C. & Davis, M. Fear-potentiated startle conditioning in humans: explicit and contextual cue conditioning following paired versus unpaired training. Psychophysiology 34, 451458 (1997).
  68. Hamm, A.O. & Vaitl, D. Affective learning: awareness and aversion. Psychophysiology 33, 698710 (1996).
  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, 8084 (2010).
  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, 827834 (2014).
  71. Jeon, D. et al. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat. Neurosci. 13, 482488 (2010).
  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. 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, 1222212227 (2014).
  74. Knapska, E. et al. Between-subject transfer of emotional information evokes specific pattern of amygdala activation. Proc. Natl. Acad. Sci. USA 103, 38583862 (2006).
  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, 13551367 (2015).
  76. Zhang, S., Mano, H., Ganesh, G., Robbins, T. & Seymour, B. Dissociable learning processes underlie human pain conditioning. Curr. Biol. 26, 5258 (2016).
  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. Curtin, J.J., Lozano, D.L. & Allen, J.J. The psychophysiological laboratory. Handbook of Emotion Elicitation and Assessment 398425 (Oxford University Press, 2007).
  79. Lykken, D.T. & Venables, P.H. Direct measurement of skin conductance: a proposal for standardization. Psychophysiology 8, 656672 (1971).
  80. Boucsein, W. et al. Publication recommendations for electrodermal measurements. Psychophysiology 49, 10171034 (2012).
  81. Fowles, D.C. et al. Committee report. Publication recommendations for electrodermal measurements. Psychophysiology 18, 232239 (1981).
  82. Mobbs, D. et al. A key role for similarity in vicarious reward. Science 324, 900 (2009).
  83. Behrens, T.E., Hunt, L.T., Woolrich, M.W. & Rushworth, M.F. Associative learning of social value. Nature 456, 245249 (2008).

Download references

Author information

  1. These authors contributed equally to this work.

    • Jan Haaker,
    • Armita Golkar &
    • Ida Selbing


  1. Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.

    • Jan Haaker,
    • Armita Golkar,
    • Ida Selbing &
    • Andreas Olsson


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.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Author details

Supplementary information

Additional data