The neural and computational systems of social learning

Abstract

Learning the value of stimuli and actions from others — social learning — adaptively contributes to individual survival and plays a key role in cultural evolution. We review research across species targeting the neural and computational systems of social learning in both the aversive and appetitive domains. Social learning generally follows the same principles as self-experienced value-based learning, including computations of prediction errors and is implemented in brain circuits activated across task domains together with regions processing social information. We integrate neural and computational perspectives of social learning with an understanding of behaviour of varying complexity, from basic threat avoidance to complex social learning strategies and cultural phenomena.

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Fig. 1: Schematic illustration of experimental procedures examining social threat and avoidance learning in rodents, monkeys and humans.
Fig. 2: Social threat learning partially shares neural mechanisms with self-experienced learning in both rodents and humans.
Fig. 3: Social reward learning partially shares neural mechanisms with self-experienced learning in both rodents and humans.

References

  1. 1.

    Bandura A. Social Learning Theory (Prentice-Hall, 1977).

  2. 2.

    Boyd, R., Richerson, P. J. & Henrich, J. The cultural niche: why social learning is essential for human adaptation. Proc. Natl. Acad. Sci. U.S.A. 108, 10918–10925 (2011). This review describes the central and adaptive role of social learning in human culture.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Debiec, J. & Olsson, A. Social fear learning: from animal models to human function. Trends Cogn. Sci. 21, 546–555 (2017).

    PubMed  PubMed Central  Google Scholar 

  4. 4.

    Schilbach, L. et al. Toward a second-person neuroscience. Behav. Brain Sci. 36, 393–414 (2013).

    PubMed  Google Scholar 

  5. 5.

    Kendal, R. L. et al. Social learning strategies: bridge-building between fields. Trends Cogn. Sci. 22, 651–665 (2018).

    PubMed  Google Scholar 

  6. 6.

    Apps, M. A. J., Rushworth, M. F. S. & Chang, S. W. C. The anterior cingulate gyrus and social cognition: tracking the motivation of others. Neuron 90, 692–707 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Falk, E. & Scholz, C. Persuasion, influence, and value: perspectives from communication and social neuroscience. Annu. Rev. Psychol. 69, 329–356 (2018).

    PubMed  Google Scholar 

  8. 8.

    Ruff, C. C. & Fehr, E. The neurobiology of rewards and values in social decision making. Nat. Rev. Neurosci. 15, 549–562 (2014).

    CAS  PubMed  Google Scholar 

  9. 9.

    Dayan, P. & Balleine, B. W. Reward, motivation, and reinforcement learning. Neuron 36, 285–298 (2002).

    CAS  PubMed  Google Scholar 

  10. 10.

    Sutton, R. S. & Barto, A. G. Reinforcement Learning: An Introduction (MIT Press, 1998).

  11. 11.

    Rescorla, R. A. & Wagner, A. R. in Classical Conditioning II: Current Research and Theory (eds. Black, A. H. & Prokasy, W. F.) 64–99 (Appleton-Century-Crofts, 1972).

  12. 12.

    Watkins, C. J. C. H. & Dayan, P. Q-learning. Mach. Learn. 8, 279–292 (1992).

    Google Scholar 

  13. 13.

    Dickinson, A. Actions and habits: the development of behavioural autonomy. Philos. Trans. R. Soc. B Biol. Sci. 308, 67–78 (1985).

    Google Scholar 

  14. 14.

    Dolan, R. J. & Dayan, P. Goals and habits in the brain. Neuron 80, 312–325 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Bach, D. R. & Dayan, P. Algorithms for survival: a comparative perspective on emotions. Nat. Rev. Neurosci. 18, 311–319 (2017).

    CAS  PubMed  Google Scholar 

  16. 16.

    Dayan, P., Niv, Y., Seymour, B. & Daw, D. N. The misbehavior of value and the discipline of the will. Neural Netw. 19, 1153–1160 (2006).

    PubMed  Google Scholar 

  17. 17.

    Bouton, M. E. Learning and Behavior: A Contemporary Synthesis (Sinauer Associates, 2007).

  18. 18.

    Miller, K., Shenhav, A. & Ludvig, E. Habits without values. Psychol Rev. 126, 292–311 (2019).

    PubMed  PubMed Central  Google Scholar 

  19. 19.

    Rangel, A., Camerer, C. & Montague, P. R. A framework for studying the neurobiology of value-based decision making. Nat. Rev. Neurosci. 9, 545–556 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Guitart-Masip, M., Duzel, E., Dolan, R. & Dayan, P. Action versus valence in decision making. Trends Cogn. Sci. 18, 194–202 (2014).

    PubMed  PubMed Central  Google Scholar 

  21. 21.

    Lindström, B., Golkar, A., Jangard, S., Tobler, P. N. & Olsson, A. Social to instrumental transfer of fear in human decision-making. Proc. Natl Acad. Sci. USA 116, 4732–4737 (2019). This study demonstrates how the interaction between Pavlovian and instrumental value systems in social learning can result in maladaptive decision making.

    PubMed  Google Scholar 

  22. 22.

    LeDoux, J. E., Cicchetti, P., Xagoraris, A. & Romanski, L. M. The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J. Neurosci. 10, 1062–1069 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Maren, S., Phan, K. L. & Liberzon, I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. 14, 417–428 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Sotres-Bayon, F. & Quirk, G. J. Prefrontal control of fear: more than just extinction. Curr. Opin. Neurobiol. 20, 231–235 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25.

    LeDoux, J. E., Iwata, J., Cicchetti, P. & Reis, D. J. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J. Neurosci. 8, 2517–2529 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Grahl, A., Onat, S. & Büchel, C. The periaqueductal gray and Bayesian integration in placebo analgesia. eLife 7, e32930 (2018).

    PubMed  PubMed Central  Google Scholar 

  27. 27.

    McNally, G. P., Johansen, J. P. & Blair, H. T. Placing prediction into the fear circuit. Trends Neurosci. 34, 283–292 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Haaker, J., Yi, J., Petrovic, P. & Olsson, A. Endogenous opioids regulate social threat learning in humans. Nat. Commun. 8, 15495 (2017). Using a pharmacological manipulation, this paper describes the role of the opioidergic system in social Pavlovian threat learning.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Gore, F. et al. Neural representations of unconditioned stimuli in basolateral amygdala mediate innate and learned responses. Cell 162, 134–145 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30.

    LaBar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E. & Phelps, E. A. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20, 937–945 (1998).

    CAS  PubMed  Google Scholar 

  31. 31.

    Phelps, E. A. & LeDoux, J. E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175–187 (2005).

    CAS  PubMed  Google Scholar 

  32. 32.

    Rajasethupathy, P. et al. Projections from neocortex mediate top-down control of memory retrieval. Nature 526, 653–659 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Alves, F. H. F. et al. Involvement of the insular cortex in the consolidation and expression of contextual fear conditioning. Eur. J. Neurosci. 38, 2300–2307 (2013).

    PubMed  Google Scholar 

  34. 34.

    Craig, A. D. How do you feel — now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59–70 (2009).

    CAS  PubMed  Google Scholar 

  35. 35.

    de la Vega, A., Chang, L. J., Banich, M. T., Wager, T. D. & Yarkoni, T. Large-scale meta-analysis of human medial frontal cortex reveals tripartite functional organization. J. Neurosci. 36, 6553–6562 (2016).

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    Lieberman, M. D. & Eisenberger, N. I. The dorsal anterior cingulate cortex is selective for pain: results from large-scale reverse inference. Proc. Natl Acad. Sci. USA 112, 15250–15255 (2015).

    CAS  PubMed  Google Scholar 

  37. 37.

    Shackman, A. J. et al. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat. Rev. Neurosci. 12, 154–167 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Fullana, M. A. et al. Neural signatures of human fear conditioning: an updated and extended meta-analysis of fMRI studies. Mol. Psychiatry 21, 500–508 (2016).

    CAS  PubMed  Google Scholar 

  39. 39.

    Dunsmoor, J. E., Niv, Y., Daw, N. & Phelps, E. A. Rethinking extinction. Neuron 88, 47–63 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Milad, M. R. & Quirk, G. J. Fear extinction as a model for translational neuroscience: ten years of progress. Annu. Rev. Psychol. 63, 129–151 (2012).

    PubMed  PubMed Central  Google Scholar 

  41. 41.

    Phelps, E. A., Delgado, M. R., Nearing, K. I. & LeDoux, J. E. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43, 897–905 (2004).

    CAS  PubMed  Google Scholar 

  42. 42.

    Fullana, M. A. et al. Fear extinction in the human brain: a meta-analysis of fMRI studies in healthy participants. Neurosci. Biobehav. Rev. 88, 16–25 (2018).

    PubMed  Google Scholar 

  43. 43.

    Gentry, R. N. & Roesch, M. R. Neural activity in ventral medial prefrontal cortex is modulated more before approach than avoidance during reinforced and extinction trial blocks. J. Neurosci. 38, 4584–4597 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Dunsmoor, J. E. et al. Role of human ventromedial prefrontal cortex in learning and recall of enhanced extinction. J. Neurosci. 39, 3264–3276 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Golkar, A., Haaker, J., Selbing, I. & Olsson, A. Neural signals of vicarious extinction learning. Soc. Cogn. Affect. Neurosci. 11, 1541–1549 (2016). The first imaging study on vicarious extinction learning, describing the role of the vmPFC in this social form of safety learning.

    PubMed  PubMed Central  Google Scholar 

  46. 46.

    Roitman, M. F., Wheeler, R. A. & Carelli, R. M. Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output. Neuron 45, 587–597 (2005).

    CAS  PubMed  Google Scholar 

  47. 47.

    Schultz, W., Apicella, P., Scarnati, E. & Ljungberg, T. Neuronal activity in monkey ventral striatum related to the expectation of reward. J. Neurosci. 12, 4595–4610 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Waelti, P., Dickinson, A. & Schultz, W. Dopamine responses comply with basic assumptions of formal learning theory. Nature 412, 43–48 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Hu, H. Reward and aversion. Annu. Rev. Neurosci. 39, 297–324 (2016).

    CAS  PubMed  Google Scholar 

  50. 50.

    Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B. & Uchida, N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482, 85–88 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Lammel, S. et al. Input-specific control of reward and aversion in the ventral tegmental area. Nature 491, 212–217 (2012). Study showing that distinct circuits within this structure can generate reward and aversion.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Everitt, B. J. et al. Associative processes in addiction and reward. The role of amygdala–ventral striatal subsystems. Ann. N. Y. Acad. Sci. 877, 412–438 (1999).

    CAS  PubMed  Google Scholar 

  53. 53.

    Stuber, G. D. et al. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475, 377–380 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Ramirez, S. et al. Activating positive memory engrams suppresses depression-like behaviour. Nature 522, 335–339 (2015). Study showing that optogenetic dissecting of a memory engram is possible.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Namburi, P. et al. A circuit mechanism for differentiating positive and negative associations. Nature 520, 675–678 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Janak, P. H. & Tye, K. M. From circuits to behaviour in the amygdala. Nature 517, 284–292 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Reekie, Y. L., Braesicke, K., Man, M. S. & Roberts, A. C. Uncoupling of behavioral and autonomic responses after lesions of the primate orbitofrontal cortex. Proc. Natl Acad. Sci. USA 105, 9787–9792 (2008).

    CAS  PubMed  Google Scholar 

  58. 58.

    Schoenbaum, G., Setlow, B., Saddoris, M. P. & Gallagher, M. Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39, 855–867 (2003).

    CAS  PubMed  Google Scholar 

  59. 59.

    Ferenczi, E. A. et al. Prefrontal cortical regulation of brainwide circuit dynamics and reward-related behavior. Science 351, aac9698 (2016).

    PubMed  PubMed Central  Google Scholar 

  60. 60.

    Otis, J. M. et al. Prefrontal cortex output circuits guide reward seeking through divergent cue encoding. Nature 543, 103–107 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Haber, S. N. & Knutson, B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26 (2009).

    PubMed Central  Google Scholar 

  62. 62.

    Delgado, M. R. Reward-related responses in the human striatum. Ann. N. Y. Acad. Sci. 1104, 70–88 (2007).

    PubMed  Google Scholar 

  63. 63.

    Amorapanth, P., LeDoux, J. E. & Nader, K. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat. Neurosci. 3, 74–79 (2000).

    CAS  PubMed  Google Scholar 

  64. 64.

    Killcross, S., Robbins, T. W. & Everitt, B. J. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 388, 377–380 (1997).

    CAS  PubMed  Google Scholar 

  65. 65.

    Wang, J., Bast, T., Wang, Y.-C. & Zhang, W.-N. Hippocampus and two-way active avoidance conditioning: contrasting effects of cytotoxic lesion and temporary inactivation. Hippocampus 25, 1517–1531 (2015).

    CAS  PubMed  Google Scholar 

  66. 66.

    Bravo-Rivera, C., Roman-Ortiz, C., Brignoni-Perez, E., Sotres-Bayon, F. & Quirk, G. J. Neural structures mediating expression and extinction of platform-mediated avoidance. J. Neurosci. 34, 9736–9742 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Parker, N. F. et al. Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target. Nat. Neurosci. 19, 845–854 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Moorman, D. E. & Aston-Jones, G. Prefrontal neurons encode context-based response execution and inhibition in reward seeking and extinction. Proc. Natl Acad. Sci. USA 112, 9472–9477 (2015).

    CAS  PubMed  Google Scholar 

  69. 69.

    Yin, H. H., Ostlund, S. B., Knowlton, B. J. & Balleine, B. W. The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci. 22, 513–523 (2005).

    PubMed  Google Scholar 

  70. 70.

    Balleine, B. W., Killcross, A. S. & Dickinson, A. The effect of lesions of the basolateral amygdala on instrumental conditioning. J. Neurosci. 23, 666–675 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Yin, H. H., Knowlton, B. J. & Balleine, B. W. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur. J. Neurosci. 19, 181–189 (2004).

    PubMed  Google Scholar 

  72. 72.

    Killcross, S. & Coutureau, E. Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb. Cortex 13, 400–408 (2003).

    PubMed  Google Scholar 

  73. 73.

    Gläscher, J., Hampton, A. N. & O’Doherty, J. P. Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. Cereb. Cortex 19, 483–495 (2009).

    PubMed  Google Scholar 

  74. 74.

    Miller, K. J., Botvinick, M. M. & Brody, C. D. Value representations in orbitofrontal cortex drive learning, not choice. bioRxiv https://doi.org/10.1101/245720 (2018).

    Article  Google Scholar 

  75. 75.

    Van Overwalle, F. A dissociation between social mentalizing and general reasoning. NeuroImage 54, 1589–1599 (2011).

    PubMed  Google Scholar 

  76. 76.

    Delgado, M. R. et al. Viewpoints: dialogues on the functional role of the ventromedial prefrontal cortex. Nat. Neurosci. 19, 1545–1552 (2016).

    CAS  PubMed  Google Scholar 

  77. 77.

    de Boer, L. et al. Dorsal striatal dopamine D1 receptor availability predicts an instrumental bias in action learning. Proc. Natl Acad. Sci. USA 116, 261–270 (2019).

    PubMed  Google Scholar 

  78. 78.

    O’Doherty, J. et al. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304, 452–454 (2004).

    PubMed  Google Scholar 

  79. 79.

    Laland, K. N. Social learning strategies. Anim. Learn. Behav. 32, 4–14 (2004). This review provides an integrated analysis of social learning strategies from the perspective of behavioural ecology.

    Google Scholar 

  80. 80.

    Debiec, J. & Sullivan, R. M. Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear. Proc. Natl. Acad. Sci. U.S.A. 111, 12222–12227 (2014). Study demonstrating intergenerational transmission of specific threat information in rodents.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. 81.

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

    PubMed  Google Scholar 

  82. 82.

    Hopwood, T. L. & Schutte, N. S. Psychological outcomes in reaction to media exposure to disasters and large-scale violence: a meta-analysis. Psychol. Violence 7, 316–327 (2017).

    Google Scholar 

  83. 83.

    Enquist, M., Eriksson, K. & Ghirlanda, S. Critical social learning: a solution to Rogers’s paradox of nonadaptive culture. Am. Anthropol. 109, 727–734 (2007).

    Google Scholar 

  84. 84.

    Rendell, L. et al. Why copy others? Insights from the social learning strategies tournament. Science 328, 208–213 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. 85.

    Joiner, J., Piva, M., Turrin, C. & Chang, S. W. C. Social learning through prediction error in the brain. NPJ Sci. Learn 2, 8 (2017).

    PubMed  PubMed Central  Google Scholar 

  86. 86.

    Amodio, D. M. & Frith, C. D. Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 7, 268–277 (2006).

    CAS  PubMed  Google Scholar 

  87. 87.

    Meyza, K. Z., Bartal, I. B.-A., Monfils, M. H., Panksepp, J. B. & Knapska, E. The roots of empathy: through the lens of rodent models. Neurosci. Biobehav. Rev. 76, 216–234 (2017).

    CAS  PubMed  Google Scholar 

  88. 88.

    Stanley, D. A. & Adolphs, R. Toward a neural basis for social behavior. Neuron 80, 816–826 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Zaki, J. Empathy: a motivated account. Psychol. Bull. 140, 1608–1647 (2014).

    PubMed  Google Scholar 

  90. 90.

    Callaghan, B. L. & Tottenham, N. The neuro-environmental loop of plasticity: a cross-species analysis of parental effects on emotion circuitry development following typical and adverse caregiving. Neuropsychopharmacology 41, 163–176 (2016).

    PubMed  Google Scholar 

  91. 91.

    Panksepp, J. B. & Lahvis, G. P. Differential influence of social versus isolate housing on vicarious fear learning in adolescent mice. Behav. Neurosci. 130, 206–211 (2016).

    PubMed  PubMed Central  Google Scholar 

  92. 92.

    Yusufishaq, S. & Rosenkranz, J. A. Post-weaning social isolation impairs observational fear conditioning. Behav. Brain Res. 242, 142–149 (2013).

    PubMed  PubMed Central  Google Scholar 

  93. 93.

    Inagaki, H. et al. Identification of a pheromone that increases anxiety in rats. Proc. Natl Acad. Sci. USA 111, 18751–18756 (2014).

    CAS  PubMed  Google Scholar 

  94. 94.

    Kim, E. J., Kim, E. S., Covey, E. & Kim, J. J. Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalization. PLoS ONE 5, e15077 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. 95.

    Knapska, E. et al. Between-subject transfer of emotional information evokes specific pattern of amygdala activation. Proc. Natl. Acad. Sci. U.S.A. 103, 3858–3862 (2006). The first rodent model of fear contagion, showing involvement of the amygdala.

    CAS  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Dezecache, G., Jacob, P. & Grèzes, J. Emotional contagion: its scope and limits. Trends Cogn. Sci. 19, 297–299 (2015).

    PubMed  Google Scholar 

  97. 97.

    Keum, S. & Shin, H.-S. Rodent models for studying empathy. Neurobiol. Learn. Mem. 135, 22–26 (2016).

    PubMed  Google Scholar 

  98. 98.

    Knapska, E., Mikosz, M., Werka, T. & Maren, S. Social modulation of learning in rats. Learn. Mem. 17, 35–42 (2010).

    PubMed  PubMed Central  Google Scholar 

  99. 99.

    Lamm, C., Decety, J. & Singer, T. Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. Neuroimage 54, 2492–2502 (2011).

    PubMed  Google Scholar 

  100. 100.

    de Waal, F. B. M. & Preston, S. D. Mammalian empathy: behavioural manifestations and neural basis. Nat. Rev. Neurosci. 18, 489–509 (2017).

    Google Scholar 

  101. 101.

    Masserman, J. H., Wechkin, S. & Terris, W. ‘Altruistic’ behavior in rhesus monkeys. Am. J. Psychiatry 121, 584–585 (1964).

    CAS  PubMed  Google Scholar 

  102. 102.

    Brass, M. & Heyes, C. Imitation: is cognitive neuroscience solving the correspondence problem? Trends Cogn. Sci. 9, 489–495 (2005).

    PubMed  Google Scholar 

  103. 103.

    Lanzetta, J. T. & Englis, B. G. Expectations of cooperation and competition and their effects on observers’ vicarious emotional responses. J. Pers. Soc. Psychol. 56, 543–554 (1989).

    Google Scholar 

  104. 104.

    Golkar, A. & Olsson, A. The interplay of social group biases in social threat learning. Sci. Rep. 7, 7685 (2017).

    PubMed  PubMed Central  Google Scholar 

  105. 105.

    Hein, G., Engelmann, J. B., Vollberg, M. C. & Tobler, P. N. How learning shapes the empathic brain. Proc. Natl Acad. Sci. USA 113, 80–85 (2016).

    CAS  PubMed  Google Scholar 

  106. 106.

    Lockwood, P. L., Apps, M. A. J., Valton, V., Viding, E. & Roiser, J. P. Neurocomputational mechanisms of prosocial learning and links to empathy. Proc. Natl Acad. Sci. USA 113, 9763–9768 (2016).

    CAS  PubMed  Google Scholar 

  107. 107.

    Burke, C. J., Tobler, P. N., Baddeley, M. & Schultz, W. Neural mechanisms of observational learning. Proc. Natl. Acad. Sci. U.S.A. 107, 14431–14436 (2010). This paper showed for the first time the neural correlates of observational learning during decision making, and pioneered the use of computational modelling in social learning research.

    CAS  PubMed  PubMed Central  Google Scholar 

  108. 108.

    Suzuki, S. et al. Learning to simulate others’ decisions. Neuron 74, 1125–1137 (2012).

    CAS  PubMed  Google Scholar 

  109. 109.

    Kilner, J. M., Friston, K. J. & Frith, C. D. Predictive coding: an account of the mirror neuron system. Cogn. Process. 8, 159–166 (2007).

    PubMed  PubMed Central  Google Scholar 

  110. 110.

    Dunne, S., D’Souza, A. & O’Doherty, J. P. The involvement of model-based but not model-free learning signals during observational reward learning in the absence of choice. J. Neurophysiol. 115, 3195–3203 (2016).

    PubMed  PubMed Central  Google Scholar 

  111. 111.

    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).

    PubMed  PubMed Central  Google Scholar 

  112. 112.

    Carlin, J. D. & Calder, A. J. The neural basis of eye gaze processing. Curr. Opin. Neurobiol. 23, 450–455 (2013).

    CAS  PubMed  Google Scholar 

  113. 113.

    Young, L., Camprodon, J. A., Hauser, M., Pascual-Leone, A. & Saxe, R. Disruption of the right temporoparietal junction with transcranial magnetic stimulation reduces the role of beliefs in moral judgments. Proc. Natl Acad. Sci. USA 107, 6753–6758 (2010).

    CAS  PubMed  Google Scholar 

  114. 114.

    Hill, C. A. et al. A causal account of the brain network computations underlying strategic social behavior. Nat. Neurosci. 20, 1142–1149 (2017).

    CAS  PubMed  Google Scholar 

  115. 115.

    Falk, E. B. et al. The neural correlates of persuasion: a common network across cultures and media. J. Cogn. Neurosci. 22, 2447–2459 (2010).

    PubMed  PubMed Central  Google Scholar 

  116. 116.

    Ong, D. C., Zaki, J. & Goodman, N. D. Computational models of emotion inference in theory of mind: a review and roadmap. Top. Cogn. Sci. 11, 338–357 (2018).

    PubMed  Google Scholar 

  117. 117.

    Saxe, R. & Houlihan, S. D. Formalizing emotion concepts within a Bayesian model of theory of mind. Curr. Opin. Psychol. 17, 15–21 (2017).

    PubMed  PubMed Central  Google Scholar 

  118. 118.

    Jeon, D. et al. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat. Neurosci. 13, 482–488 (2010). The first model of observational fear learning in rodents, shows the critical role of the ACC.

    CAS  PubMed  PubMed Central  Google Scholar 

  119. 119.

    Atsak, P. et al. Experience modulates vicarious freezing in rats: a model for empathy. PLoS ONE 6, e21855 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. 120.

    Pereira, A. G., Cruz, A., Lima, S. Q. & Moita, M. A. Silence resulting from the cessation of movement signals danger. Curr. Biol. 22, R627–628 (2012).

    CAS  PubMed  Google Scholar 

  121. 121.

    Chen, Q., Panksepp, J. B. & Lahvis, G. P. Empathy is moderated by genetic background in mice. PLoS ONE 4, e4387 (2009).

    PubMed  PubMed Central  Google Scholar 

  122. 122.

    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).

    PubMed  PubMed Central  Google Scholar 

  123. 123.

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

    CAS  PubMed  Google Scholar 

  124. 124.

    Reynolds, G., Field, A. P. & Askew, C. Learning to fear a second-order stimulus following vicarious learning. Cogn. Emot. 31, 572–579 (2017).

    PubMed  Google Scholar 

  125. 125.

    Hooker, C. I., Germine, L. T., Knight, R. T. & D’Esposito, M. Amygdala response to facial expressions reflects emotional learning. J. Neurosci. 26, 8915–8922 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. 126.

    Lindström, B., Haaker, J. & Olsson, A. A common neural network differentially mediates direct and social fear learning. NeuroImage 167, 121–129 (2018). This paper demonstrates that social and direct forms of Pavlovian threat learning are underpinned by a common neural network.

    PubMed  Google Scholar 

  127. 127.

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

    PubMed  Google Scholar 

  128. 128.

    Carrillo, M. et al. Emotional mirror neurons in the rat’s anterior cingulate cortex. Curr. Biol. 29, 1301–1312.e6 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  129. 129.

    Bissière, S. et al. The rostral anterior cingulate cortex modulates the efficiency of amygdala-dependent fear learning. Biol. Psychiatry 63, 821–831 (2008).

    PubMed  Google Scholar 

  130. 130.

    Allsop, S. A. et al. Corticoamygdala transfer of socially derived information gates observational learning. Cell 173, 1329–1342 (2018). This paper shows the role of a specific pathway (the ACC→BLA projection) in observational threat learning.

    CAS  PubMed  PubMed Central  Google Scholar 

  131. 131.

    Twining, R. C., Vantrease, J. E., Love, S., Padival, M. & Rosenkranz, J. A. An intra-amygdala circuit specifically regulates social fear learning. Nat. Neurosci. 20, 459–469 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. 132.

    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).

    PubMed  Google Scholar 

  133. 133.

    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).

    PubMed  PubMed Central  Google Scholar 

  134. 134.

    Terburg, D. et al. The basolateral amygdala is essential for rapid escape: a human and rodent study. Cell 175, 723–735.e16 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. 135.

    Wang, S. et al. The human amygdala parametrically encodes the intensity of specific facial emotions and their categorical ambiguity. Nat. Commun. 8, 14821 (2017).

    PubMed  PubMed Central  Google Scholar 

  136. 136.

    Eippert, F., Bingel, U., Schoell, E., Yacubian, J. & Buchel, C. Blockade of endogenous opioid neurotransmission enhances acquisition of conditioned fear in humans. J. Neurosci. 28, 5465–5472 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. 137.

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

    PubMed  Google Scholar 

  138. 138.

    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).

    PubMed  PubMed Central  Google Scholar 

  139. 139.

    Golkar, A., Selbing, I., Flygare, O., Öhman, A. & Olsson, A. Other people as means to a safe end. Psychol. Sci. 24, 2182–2190 (2013).

    PubMed  Google Scholar 

  140. 140.

    Chang, S. W. C., Winecoff, A. A. & Platt, M. L. Vicarious reinforcement in rhesus macaques (Macaca mulatta). Front. Neurosci. 5, 27 (2011).

    PubMed  PubMed Central  Google Scholar 

  141. 141.

    Kendal, R. et al. Chimpanzees copy dominant and knowledgeable individuals: implications for cultural diversity. Evol. Hum. Behav. 36, 65–72 (2015).

    PubMed  PubMed Central  Google Scholar 

  142. 142.

    Kavaliers, M., Colwell, D. D. & Choleris, E. Kinship, familiarity and social status modulate social learning about “micropredators” (biting flies) in deer mice. Behav. Ecol. Sociobiol. 58, 60–71 (2005).

    Google Scholar 

  143. 143.

    Goubert, L., Vlaeyen, J. W. S., Crombez, G. & Craig, K. D. Learning about pain from others: an observational learning account. J. Pain. 12, 167–174 (2011).

    PubMed  Google Scholar 

  144. 144.

    Fiske, S. T., Harris, L. T., Lee, T. L. & Russell, A. M. in Handbook of Prejudice, Stereotyping, and Discrimination (ed. Nelson, T. D.) 525–534 (Taylor & Francis, 2009).

  145. 145.

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

    Google Scholar 

  146. 146.

    Phelps, E. A. et al. Activation of the left amygdala to a cognitive representation of fear. Nat. Neurosci. 4, 437–441 (2001). The first study examining the brain responses to verbally instructed threat, highlighting the involvement of the amygdala in support of its conserved function across modes of learning.

    CAS  PubMed  Google Scholar 

  147. 147.

    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  PubMed  PubMed Central  Google Scholar 

  148. 148.

    Mechias, M.-L., Etkin, A. & Kalisch, R. A meta-analysis of instructed fear studies: implications for conscious appraisal of threat. NeuroImage 49, 1760–1768 (2010).

    PubMed  Google Scholar 

  149. 149.

    Dayan, P. & Berridge, K. C. Model-based and model-free Pavlovian reward learning: revaluation, revision, and revelation. Cogn. Affect. Behav. Neurosci. 14, 473–492 (2014).

    PubMed  PubMed Central  Google Scholar 

  150. 150.

    Atlas, L. Y., Doll, B. B., Li, J., Daw, N. D. & Phelps, E. A. Instructed knowledge shapes feedback-driven aversive learning in striatum and orbitofrontal cortex, but not the amygdala. eLife 5, e15192 (2016).

    PubMed  PubMed Central  Google Scholar 

  151. 151.

    Atlas, L. Y. & Phelps, E. A. Prepared stimuli enhance aversive learning without weakening the impact of verbal instructions. Learn. Mem. 25, 100–104 (2018).

    PubMed  PubMed Central  Google Scholar 

  152. 152.

    Costa, V. D., Bradley, M. M. & Lang, P. J. From threat to safety: instructed reversal of defensive reactions. Psychophysiology 52, 325–332 (2015).

    PubMed  Google Scholar 

  153. 153.

    Leadbeater, E. & Dawson, E. H. A social insect perspective on the evolution of social learning mechanisms. Proc. Natl Acad. Sci. USA 114, 7838–7845 (2017).

    CAS  PubMed  Google Scholar 

  154. 154.

    Dawson, E. H., Avarguès-Weber, A., Chittka, L. & Leadbeater, E. Learning by observation emerges from simple associations in an insect model. Curr. Biol. 23, 727–730 (2013).

    CAS  PubMed  Google Scholar 

  155. 155.

    Posadas-Andrews, A. & Roper, T. J. Social transmission of food-preferences in adult rats. Anim. Behav. 31, 265–271 (1983).

    Google Scholar 

  156. 156.

    Galef, B. G., Mason, J. R., Preti, G. & Bean, N. J. Carbon disulfide: a semiochemical mediating socially-induced diet choice in rats. Physiol. Behav. 42, 119–124 (1988).

    CAS  PubMed  Google Scholar 

  157. 157.

    Munger, S. D. et al. An olfactory subsystem that detects carbon disulfide and mediates food-related social learning. Curr. Biol. 20, 1438–1444 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. 158.

    Smith, C. A., East, B. S. & Colombo, P. J. The orbitofrontal cortex is not necessary for acquisition or remote recall of socially transmitted food preferences. Behav. Brain Res. 208, 243–249 (2010).

    PubMed  Google Scholar 

  159. 159.

    Carballo-Márquez, A., Vale-Martínez, A., Guillazo-Blanch, G. & Martí-Nicolovius, M. Muscarinic transmission in the basolateral amygdala is necessary for the acquisition of socially transmitted food preferences in rats. Neurobiol. Learn. Mem. 91, 98–101 (2009).

    PubMed  Google Scholar 

  160. 160.

    Ross, R. S., McGaughy, J. & Eichenbaum, H. Acetylcholine in the orbitofrontal cortex is necessary for the acquisition of a socially transmitted food preference. Learn. Mem. 12, 302–306 (2005).

    PubMed  PubMed Central  Google Scholar 

  161. 161.

    Wang, Y., Fontanini, A. & Katz, D. B. Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats. Learn. Mem. 13, 794–800 (2006).

    PubMed  PubMed Central  Google Scholar 

  162. 162.

    Kashtelyan, V., Lichtenberg, N. T., Chen, M. L., Cheer, J. F. & Roesch, M. R. Observation of reward delivery to a conspecific modulates dopamine release in ventral striatum. Curr. Biol. 24, 2564–2568 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  163. 163.

    Paton, J. J., Belova, M. A., Morrison, S. E. & Salzman, C. D. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439, 865–870 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  164. 164.

    Reynolds, S. M. & Berridge, K. C. Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste ‘liking’/‘disliking’ reactions, place preference/avoidance, and fear. J. Neurosci. 22, 7308–7320 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  165. 165.

    Kim, J., Pignatelli, M., Xu, S., Itohara, S. & Tonegawa, S. Antagonistic negative and positive neurons of the basolateral amygdala. Nat. Neurosci. 19, 1636–1646 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  166. 166.

    Morelli, S. A., Sacchet, M. D. & Zaki, J. Common and distinct neural correlates of personal and vicarious reward: a quantitative meta-analysis. NeuroImage 112, 244–253 (2015).

    PubMed  Google Scholar 

  167. 167.

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

    CAS  PubMed  PubMed Central  Google Scholar 

  168. 168.

    Morelli, S. A., Knutson, B. & Zaki, J. Neural sensitivity to personal and vicarious reward differentially relate to prosociality and well-being. Soc. Cogn. Affect. Neurosci. 13, 831–839 (2018).

    PubMed  PubMed Central  Google Scholar 

  169. 169.

    Singer, T. et al. Empathic neural responses are modulated by the perceived fairness of others. Nature 439, 466–469 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  170. 170.

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

    PubMed  PubMed Central  Google Scholar 

  171. 171.

    Bunch, G. B. & Zentall, T. R. Imitation of a passive avoidance response in the rat. Bull. Psychon. Soc. 15, 73–75 (1980).

    Google Scholar 

  172. 172.

    Del Russo, J. E. Observational learning of discriminative avoidance in hooded rats. Anim. Learn. Behav. 3, 76–80 (1975).

    Google Scholar 

  173. 173.

    Masuda, A. & Aou, S. Social transmission of avoidance behavior under situational change in learned and unlearned rats. PLoS ONE 4, e6794 (2009).

    PubMed  PubMed Central  Google Scholar 

  174. 174.

    Masuda, A. & Aou, S. Lesions of the medial prefrontal cortex enhance social modulation of avoidance. Behav. Brain Res. 217, 309–314 (2011).

    PubMed  Google Scholar 

  175. 175.

    Lindström, B. & Olsson, A. Mechanisms of social avoidance learning can explain the emergence of adaptive and arbitrary behavioral traditions in humans. J. Exp. Psychol. Gen. 144, 688–703 (2015).

    PubMed  Google Scholar 

  176. 176.

    Heyes, C. M. & Dawson, G. R. A demonstration of observational learning in rats using a bidirectional control. Q. J. Exp. Psychol. Sect. B Comp. Physiol. Psychol. 42, 59–71 (1990).

    CAS  Google Scholar 

  177. 177.

    Huang, I.-N., Koski, C. A. & DeQuardo, J. R. Observational learning of a bar-press by rats. J. Gen. Psychol. 108, 103–111 (1983).

    PubMed  Google Scholar 

  178. 178.

    Zentall, T. R. & Levine, J. M. Observational learning and social facilitation in the rat. Science 178, 1220–1221 (1972).

    CAS  PubMed  Google Scholar 

  179. 179.

    Bem, T., Jura, B., Bontempi, B. & Meyrand, P. Observational learning of a spatial discrimination task by rats: learning from the mistakes of others? Anim. Behav. 135, 85–96 (2018).

    Google Scholar 

  180. 180.

    Groesbeck, R. W. & Duerfeldt, P. H. Some relevant variables in observational learning of the rat. Psychon. Sci. 22, 41–43 (1971).

    Google Scholar 

  181. 181.

    Jurado-Parras, M. T., Gruart, A. & Delgado-García, J. M. Observational learning in mice can be prevented by medial prefrontal cortex stimulation and enhanced by nucleus accumbens stimulation. Learn. Mem. 19, 99–106 (2012).

    PubMed  Google Scholar 

  182. 182.

    Cooper, J. C., Dunne, S., Furey, T. & O’Doherty, J. P. Human dorsal striatum encodes prediction errors during observational learning of instrumental actions. J. Cogn. Neurosci. 24, 106–118 (2012).

    PubMed  Google Scholar 

  183. 183.

    Hill, M. R., Boorman, E. D. & Fried, I. Observational learning computations in neurons of the human anterior cingulate cortex. Nat. Commun. 7, 12722 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  184. 184.

    Apps, M. A. J. & Sallet, J. Social learning in the medial prefrontal cortex. Trends Cogn. Sci. 21, 151–152 (2017).

    PubMed  Google Scholar 

  185. 185.

    Chang, S. W. C., Gariépy, J.-F. & Platt, M. L. Neuronal reference frames for social decisions in primate frontal cortex. Nat. Neurosci. 16, 243–250 (2013). This study demonstrates the differentiated roles of sub-regions of the ACC in vicarious reward in primates.

    CAS  PubMed  Google Scholar 

  186. 186.

    Apps, M. A. J. & Ramnani, N. The anterior cingulate gyrus signals the net value of others’ rewards. J. Neurosci. 34, 6190–6200 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  187. 187.

    Lockwood, P. L., Apps, M. A. J., Roiser, J. P. & Viding, E. Encoding of vicarious reward prediction in anterior cingulate cortex and relationship with trait empathy. J. Neurosci. 35, 13720–13727 (2015). This study demonstrates that the gyrus of the anterior cingulate cortex (ACCg) is more responsive to vicarious than self-experienced reward, and related to trait empathy.

    CAS  PubMed  PubMed Central  Google Scholar 

  188. 188.

    Lockwood, P. L. et al. Association of callous traits with reduced neural response to others’ pain in children with conduct problems. Curr. Biol. 23, 901–905 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  189. 189.

    Hesslow, G. The current status of the simulation theory of cognition. Brain Res. 1428, 71–79 (2012).

    CAS  PubMed  Google Scholar 

  190. 190.

    Liljeholm, M., Molloy, C. J. & O’Doherty, J. P. Dissociable brain systems mediate vicarious learning of stimulus–response and action–outcome contingencies. J. Neurosci. 32, 9878–9886 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  191. 191.

    Williamson, R. A., Meltzoff, A. N. & Markman, E. M. Prior experiences and perceived efficacy influence 3-year-olds’ imitation. Dev. Psychol. 44, 275–285 (2008).

    PubMed  PubMed Central  Google Scholar 

  192. 192.

    Dorrance, B. R. & Zentall, T. R. Imitation of conditional discriminations in pigeons (Columba livia). J. Comp. Psychol. 116, 277–285 (2002).

    PubMed  Google Scholar 

  193. 193.

    Saggerson, A. L., George, D. N. & Honey, R. C. Imitative learning of stimulus–response and response–outcome associations in pigeons. J. Exp. Psychol. Anim. Behav. Process. 31, 289–300 (2005).

    CAS  PubMed  Google Scholar 

  194. 194.

    Duhan, D. F., Johnson, S. D., Wilcox, J. B. & Harrell, G. D. Influences on consumer use of word-of-mouth recommendation sources. J. Acad. Mark. Sci. 25, 283–295 (1997).

    Google Scholar 

  195. 195.

    Biele, G., Rieskamp, J., Krugel, L. K. & Heekeren, H. R. The neural basis of following advice. PLoS Biol. 9, e1001089 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  196. 196.

    Doll, B. B., Jacobs, W. J., Sanfey, A. G. & Frank, M. J. Instructional control of reinforcement learning: a behavioral and neurocomputational investigation. Brain Res. 1299, 74–94 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  197. 197.

    Li, J., Delgado, M. R. & Phelps, E. A. How instructed knowledge modulates the neural systems of reward learning. Proc. Natl Acad. Sci. USA 108, 55–60 (2011).

    CAS  PubMed  Google Scholar 

  198. 198.

    Fazio, R. H., Eiser, J. R. & Shook, N. J. Attitude formation through exploration: valence asymmetries. J. Pers. Soc. Psychol. 87, 293–311 (2004).

    PubMed  Google Scholar 

  199. 199.

    Staudinger, M. R. & Büchel, C. How initial confirmatory experience potentiates the detrimental influence of bad advice. NeuroImage 76, 125–133 (2013).

    PubMed  Google Scholar 

  200. 200.

    Bikhchandani, S., Hirshleifer, D. & Welch, I. Learning from the behavior of others: conformity, fads, and informational cascades. J. Econ. Perspect. 12, 151–170 (1998).

    Google Scholar 

  201. 201.

    Wood, L. A., Kendal, R. L. & Flynn, E. G. Whom do children copy? Model-based biases in social learning. Dev. Rev. 33, 341–356 (2013).

    Google Scholar 

  202. 202.

    Selbing, I. & Olsson, A. Beliefs about others’ abilities alter learning from observation. Sci. Rep. 7, 16173 (2017).

    PubMed  PubMed Central  Google Scholar 

  203. 203.

    Vostroknutov, A., Polonio, L. & Coricelli, G. The role of intelligence in social learning. Sci. Rep. 8, 6896 (2018).

    PubMed  PubMed Central  Google Scholar 

  204. 204.

    Collette, S., Pauli, W. M., Bossaerts, P. & O’Doherty, J. Neural computations underlying inverse reinforcement learning in the human brain. eLife 6, e29718 (2017).

    PubMed  PubMed Central  Google Scholar 

  205. 205.

    Ng, A. Y. & Russell, S. in Proceedings of the Seventeenth International Conference on Machine Learning (ed. Langley, P.) 663–670 (Morgan Kaufmann, 2000).

  206. 206.

    Heyes, C. Who knows? Metacognitive social learning strategies. Trends Cogn. Sci. 20, 204–213 (2016).

    PubMed  Google Scholar 

  207. 207.

    Jara-Ettinger, J. Theory of mind as inverse reinforcement learning. Curr. Opin. Behav. Sci. 29, 105–110 (2019).

    Google Scholar 

  208. 208.

    Efferson, C., Lalive, R., Richerson, P., McElreath, R. & Lubell, M. Conformists and mavericks: the empirics of frequency-dependent cultural transmission. Evol. Hum. Behav. 29, 56–64 (2008).

    Google Scholar 

  209. 209.

    Morgan, T. J. H., Rendell, L. E., Ehn, M., Hoppitt, W. & Laland, K. N. The evolutionary basis of human social learning. Proc. R. Soc. B Biol. Sci. 279, 653–662 (2012).

    CAS  Google Scholar 

  210. 210.

    Rendell, L. et al. Cognitive culture: theoretical and empirical insights into social learning strategies. Trends Cogn. Sci. 15, 68–76 (2011).

    PubMed  Google Scholar 

  211. 211.

    Kendal, R. L., Coolen, I. & Laland, K. N. The role of conformity in foraging when personal and social information conflict. Behav. Ecol. 15, 269–277 (2004).

    Google Scholar 

  212. 212.

    Pike, T. W. & Laland, K. N. Conformist learning in nine-spined sticklebacks’ foraging decisions. Biol. Lett. 6, 466–468 (2010).

    PubMed  PubMed Central  Google Scholar 

  213. 213.

    van de Waal, E., Borgeaud, C. & Whiten, A. Potent social learning and conformity shape a wild primate’s foraging decisions. Science 340, 483–485 (2013). This field study with vervet monkeys demonstrates social transmission of food preferences induced by aversive learning, which results in strong local food choice traditions.

    PubMed  Google Scholar 

  214. 214.

    van Leeuwen, E. J. C. & Haun, D. B. M. Conformity in nonhuman primates: fad or fact? Evol. Hum. Behav. 34, 1–7 (2013).

    Google Scholar 

  215. 215.

    Huang, T.-R., Hazy, T. E., Herd, S. A. & O’Reilly, R. C. Assembling old tricks for new tasks: a neural model of instructional learning and control. J. Cogn. Neurosci. 25, 843–851 (2013).

    PubMed  Google Scholar 

  216. 216.

    Wu, H., Luo, Y. & Feng, C. Neural signatures of social conformity: a coordinate-based activation likelihood estimation meta-analysis of functional brain imaging studies. Neurosci. Biobehav. Rev. 71, 101–111 (2016).

    PubMed  Google Scholar 

  217. 217.

    Klucharev, V., Hytönen, K., Rijpkema, M., Smidts, A. & Fernández, G. Reinforcement learning signal predicts social conformity. Neuron 61, 140–151 (2009).

    CAS  PubMed  Google Scholar 

  218. 218.

    Nook, E. C. & Zaki, J. Social norms shift behavioral and neural responses to foods. J. Cogn. Neurosci. 27, 1412–1426 (2015).

    PubMed  Google Scholar 

  219. 219.

    Suzuki, S., Adachi, R., Dunne, S., Bossaerts, P. & O’Doherty, J. P. Neural mechanisms underlying human consensus decision-making. Neuron 86, 591–602 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  220. 220.

    Parkinson, C. & Wheatley, T. The repurposed social brain. Trends Cogn. Sci. 19, 133–141 (2015).

    PubMed  Google Scholar 

  221. 221.

    Heyes, C. What’s social about social learning? J. Comp. Psychol. 126, 193–202 (2012). This review questions whether social learning involves any distinctly social processes, and argues that social learning is governed by domain-general learning processes.

    PubMed  Google Scholar 

  222. 222.

    Heyes, C. Enquire within: cultural evolution and cognitive science. Philos. Trans. R. Soc. B Biol. Sci. 373, 20170051 (2018).

    Google Scholar 

  223. 223.

    Heyes, C. & Pearce, J. M. Not-so-social learning strategies. Proc. R. Soc. B Biol. Sci. 282, 20141709 (2015).

    Google Scholar 

  224. 224.

    Lind, J., Ghirlanda, S. & Enquist, M. Social learning through associative processes: a computational theory. R. Soc. Open. Sci. 6, 181777 (2019). In this paper, the authors provide a theoretical reinforcement learning model that can account for many types of social learning in animals.

    PubMed  PubMed Central  Google Scholar 

  225. 225.

    Gee, D. G. et al. Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation. Proc. Natl Acad. Sci. USA 110, 15638–15643 (2013).

    CAS  PubMed  Google Scholar 

  226. 226.

    Chang, D.-J. & Debiec, J. Neural correlates of the mother-to-infant social transmission of fear. J. Neurosci. Res. 94, 526–534 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  227. 227.

    Sanders, J., Mayford, M. & Jeste, D. Empathic fear responses in mice are triggered by recognition of a shared experience. PLoS ONE 8, e74609 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  228. 228.

    Öhman, A. & Mineka, S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol. Rev. 108, 483–522 (2001).

    PubMed  Google Scholar 

  229. 229.

    Cohen, J. D. et al. Computational approaches to fMRI analysis. Nat. Neurosci. 20, 304–313 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  230. 230.

    O’Doherty, J. P., Hampton, A. & Kim, H. Model-based fMRI and its application to reward learning and decision making. Ann. N. Y. Acad. Sci. 1104, 35–53 (2007).

    PubMed  Google Scholar 

  231. 231.

    Diaconescu, A. O. et al. Hierarchical prediction errors in midbrain and septum during social learning. Soc. Cogn. Affect. Neurosci. 12, 618–634 (2017).

    PubMed  PubMed Central  Google Scholar 

  232. 232.

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

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank P. Tobler, K. Kondrakiewicz, T. Hensler, A. Walsh, and the reviewers for comments on an earlier version of the manuscript. A.O. was supported by the Knut and Alice Wallenberg Foundation (KAW 2014.0237), a European Research Council Starting Grant (284366; Emotional Learning in Social Interaction project) and a Consolidator Grant (2018-00877) from the Swedish Research Foundation (VR). B.L. was partially supported by Forte (COFAS2: 2014-2785 FOIP) and E.K. by a European Research Council Starting Grant (H 415148) and a National Science Centre grant (2015/19/B/HS6/02209).

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All authors contributed equally to all aspects of the manuscript.

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Correspondence to Andreas Olsson.

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Nature Reviews Neuroscience thanks R. Kendal, R. Adolphs and K. Tye for their contribution to the peer review of this work.

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Glossary

Social learning

Learning from others, for example through observation and instruction, which may or may not involve directly experienced or vicarious reinforcement.

Value-based learning

Learning about rewards and punishers, which promote the organization of behaviour for maximizing rewards and minimizing punishments

Optogenetics

The use of genetically encoded, light-activated proteins to modulate activity of specific neural circuits. Optogenetics allows for targeting specific cell types or projections to learn the causal relationship between their activity and behaviour.

Fear contagion

An individual’s fear and related behaviours directly trigger similar emotions and behaviours in others.

Vicarious reinforcement learning

Use of vicarious reinforcement as a stand in for directly experienced reinforcement in reinforcement learning algorithms.

Vicarious reinforcement

A motivating outcome, such as a reward or punishment, observed or otherwise known to be incurred by another individual.

Empathy

The sharing and understanding of the affective state of another individual.

Domain-general learning

Mechanisms contributing to many cognitive functions, across situations and tasks.

Vicarious learning

Learning from others without any directly experienced reinforcement. Sometimes used synonymously with ‘observational learning’.

Observational learning

Learning through observing the responses and behaviour of others, which may or may not involve reinforcement.

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Olsson, A., Knapska, E. & Lindström, B. The neural and computational systems of social learning. Nat Rev Neurosci 21, 197–212 (2020). https://doi.org/10.1038/s41583-020-0276-4

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