Learning fears by observing others: the neural systems of social fear transmission - PubMed (original) (raw)
Learning fears by observing others: the neural systems of social fear transmission
Andreas Olsson et al. Soc Cogn Affect Neurosci. 2007 Mar.
Abstract
Classical fear conditioning has been used as a model paradigm to explain fear learning across species. In this paradigm, the amygdala is known to play a critical role. However, classical fear conditioning requires first-hand experience with an aversive event, which may not be how most fears are acquired in humans. It remains to be determined whether the conditioning model can be extended to indirect forms of learning more common in humans. Here we show that fear acquired indirectly through social observation, with no personal experience of the aversive event, engages similar neural mechanisms as fear conditioning. The amygdala was recruited both when subjects observed someone else being submitted to an aversive event, knowing that the same treatment awaited themselves, and when subjects were subsequently placed in an analogous situation. These findings confirm the central role of the amygdala in the acquisition and expression of observational fear learning, and validate the extension of cross-species models of fear conditioning to learning in a human sociocultural context. Our findings also provides new insights into the relationship between learning from, and empathizing with, fearful others. This study suggests that indirectly attained fears may be as powerful as fears originating from direct experiences.
Figures
Fig. 1
(A) A snap-shot from the movie presented to subjects during the observation stage, depicting the learning model facing a computer screen that displayed the CS+ and CS−. To each of the three shocks paired with a CS+, the model displayed signs of distress (e.g. lowering the eyebrows, raising the cheeks and twisting the right hand indicating the administration of the shock). (B) Mean skin conductance response (SCR) during the test stage to the CS+ (blue bar) and the CS− (yellow bar) and during the observation stage to the model's response to the shock (red bar) and CS− (yellow bar). Error bars show standard error.
Fig. 2
Amygdala activation at P < 0.005, uncorrected, during (A) the test stage for the contrast between CS+ vs CS− (x, y, z = −20, −2, −9 and 19, −2, −7 for the left and right amygdala, respectively) and (B) the observation stage for the contrast between CS+ and US combined vs the CS− (x, y, z = −28, −5, −12 and 23, −2, −10 for the left and right amygdala, respectively). (C) Shows the regions commonly activated in (a) and (b) (P < 0.05, uncorrected; x, y, z = −20, −9, −13 and 19, −6, −10 for the left and right amygdala, respectively). Region of interest (ROI) time courses for amygdala activation (percent signal change) in the (D) left and (E) right amygdala to the CS+ (blue line) and CS− (green line) during the test stage, and the (F) left and (G) right amygdala to the CS+ (blue line), US (red line) and CS− (green line) during the observation stage. ROIs were extracted from the CS+ vs CS− contrast during the test stage, with a _P_-threshold of P < 0.005, uncorrected. Error bars show standard error.
Comment in
- Learning to fear what others have feared before.
Ochsner K. Ochsner K. Soc Cogn Affect Neurosci. 2007 Mar;2(1):1-2. doi: 10.1093/scan/nsm007. Soc Cogn Affect Neurosci. 2007. PMID: 20336855 Free PMC article. No abstract available.
Similar articles
- Social learning of fear.
Olsson A, Phelps EA. Olsson A, et al. Nat Neurosci. 2007 Sep;10(9):1095-102. doi: 10.1038/nn1968. Nat Neurosci. 2007. PMID: 17726475 Review. - Neural correlates of biased social fear learning and interaction in an intergroup context.
Molapour T, Golkar A, Navarrete CD, Haaker J, Olsson A. Molapour T, et al. Neuroimage. 2015 Nov 1;121:171-83. doi: 10.1016/j.neuroimage.2015.07.015. Epub 2015 Jul 10. Neuroimage. 2015. PMID: 26166625 Free PMC article. - A common neural network differentially mediates direct and social fear learning.
Lindström B, Haaker J, Olsson A. Lindström B, et al. Neuroimage. 2018 Feb 15;167:121-129. doi: 10.1016/j.neuroimage.2017.11.039. Epub 2017 Nov 21. Neuroimage. 2018. PMID: 29170069 - An exploration of amygdala-prefrontal mechanisms in the intergenerational transmission of learned fear.
Silvers JA, Callaghan BL, VanTieghem M, Choy T, O'Sullivan K, Tottenham N. Silvers JA, et al. Dev Sci. 2021 May;24(3):e13056. doi: 10.1111/desc.13056. Epub 2020 Nov 10. Dev Sci. 2021. PMID: 33103280 Free PMC article. - Extending animal models of fear conditioning to humans.
Delgado MR, Olsson A, Phelps EA. Delgado MR, et al. Biol Psychol. 2006 Jul;73(1):39-48. doi: 10.1016/j.biopsycho.2006.01.006. Epub 2006 Feb 10. Biol Psychol. 2006. PMID: 16472906 Review.
Cited by
- Observation of others' painful heat stimulation involves responses in the spinal cord.
Tinnermann A, Büchel C, Haaker J. Tinnermann A, et al. Sci Adv. 2021 Mar 31;7(14):eabe8444. doi: 10.1126/sciadv.abe8444. Print 2021 Mar. Sci Adv. 2021. PMID: 33789899 Free PMC article. - Human fear neurobiology reimagined: Can brain-derived biotypes predict fear-based disorders after trauma?
McClellan France J, Jovanovic T. McClellan France J, et al. Neurosci Biobehav Rev. 2023 Jan;144:104988. doi: 10.1016/j.neubiorev.2022.104988. Epub 2022 Dec 5. Neurosci Biobehav Rev. 2023. PMID: 36470327 Free PMC article. Review. - Observational learning of threat-related attentional bias.
Grégoire L, Dubravac M, Moore K, Kim N, Anderson BA. Grégoire L, et al. Cogn Emot. 2024 Aug;38(5):789-800. doi: 10.1080/02699931.2024.2317917. Epub 2024 Feb 27. Cogn Emot. 2024. PMID: 38411172 - The neurobiology of safety and threat learning in infancy.
Debiec J, Sullivan RM. Debiec J, et al. Neurobiol Learn Mem. 2017 Sep;143:49-58. doi: 10.1016/j.nlm.2016.10.015. Epub 2016 Nov 4. Neurobiol Learn Mem. 2017. PMID: 27826033 Free PMC article. Review. - Functional overlap of top-down emotion regulation and generation: an fMRI study identifying common neural substrates between cognitive reappraisal and cognitively generated emotions.
Otto B, Misra S, Prasad A, McRae K. Otto B, et al. Cogn Affect Behav Neurosci. 2014 Sep;14(3):923-38. doi: 10.3758/s13415-013-0240-0. Cogn Affect Behav Neurosci. 2014. PMID: 24430617
References
- Adolphs R. Cognitive neuroscience of human social behavior. Nature Neuroscience. 2003;4:165–78. - PubMed
- Amodio DM, Frith CD. Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience. 2006;7:268–77. - PubMed
- Bandura A. Social Learning Theory. New York: General Learning Press; 1977.
- Berger S. Conditioning through vicarious instigation. Psychological Review. 1962;69:450–66. - PubMed
- Botvinick M, Jha AP, Bylsma LM, Fabian SA, Solomon PE, Prkachin KM. Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. Neuroimage. 2005;25:312–19. - PubMed
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources