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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References
Bandura A. Social Learning Theory (Prentice-Hall, 1977).
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.
Debiec, J. & Olsson, A. Social fear learning: from animal models to human function. Trends Cogn. Sci. 21, 546–555 (2017).
Schilbach, L. et al. Toward a second-person neuroscience. Behav. Brain Sci. 36, 393–414 (2013).
Kendal, R. L. et al. Social learning strategies: bridge-building between fields. Trends Cogn. Sci. 22, 651–665 (2018).
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).
Falk, E. & Scholz, C. Persuasion, influence, and value: perspectives from communication and social neuroscience. Annu. Rev. Psychol. 69, 329–356 (2018).
Ruff, C. C. & Fehr, E. The neurobiology of rewards and values in social decision making. Nat. Rev. Neurosci. 15, 549–562 (2014).
Dayan, P. & Balleine, B. W. Reward, motivation, and reinforcement learning. Neuron 36, 285–298 (2002).
Sutton, R. S. & Barto, A. G. Reinforcement Learning: An Introduction (MIT Press, 1998).
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).
Watkins, C. J. C. H. & Dayan, P. Q-learning. Mach. Learn. 8, 279–292 (1992).
Dickinson, A. Actions and habits: the development of behavioural autonomy. Philos. Trans. R. Soc. B Biol. Sci. 308, 67–78 (1985).
Dolan, R. J. & Dayan, P. Goals and habits in the brain. Neuron 80, 312–325 (2013).
Bach, D. R. & Dayan, P. Algorithms for survival: a comparative perspective on emotions. Nat. Rev. Neurosci. 18, 311–319 (2017).
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).
Bouton, M. E. Learning and Behavior: A Contemporary Synthesis (Sinauer Associates, 2007).
Miller, K., Shenhav, A. & Ludvig, E. Habits without values. Psychol Rev. 126, 292–311 (2019).
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).
Guitart-Masip, M., Duzel, E., Dolan, R. & Dayan, P. Action versus valence in decision making. Trends Cogn. Sci. 18, 194–202 (2014).
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.
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).
Maren, S., Phan, K. L. & Liberzon, I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. 14, 417–428 (2013).
Sotres-Bayon, F. & Quirk, G. J. Prefrontal control of fear: more than just extinction. Curr. Opin. Neurobiol. 20, 231–235 (2010).
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).
Grahl, A., Onat, S. & Büchel, C. The periaqueductal gray and Bayesian integration in placebo analgesia. eLife 7, e32930 (2018).
McNally, G. P., Johansen, J. P. & Blair, H. T. Placing prediction into the fear circuit. Trends Neurosci. 34, 283–292 (2011).
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.
Gore, F. et al. Neural representations of unconditioned stimuli in basolateral amygdala mediate innate and learned responses. Cell 162, 134–145 (2015).
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).
Phelps, E. A. & LeDoux, J. E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175–187 (2005).
Rajasethupathy, P. et al. Projections from neocortex mediate top-down control of memory retrieval. Nature 526, 653–659 (2015).
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).
Craig, A. D. How do you feel — now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59–70 (2009).
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).
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).
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).
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).
Dunsmoor, J. E., Niv, Y., Daw, N. & Phelps, E. A. Rethinking extinction. Neuron 88, 47–63 (2015).
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).
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).
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).
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).
Dunsmoor, J. E. et al. Role of human ventromedial prefrontal cortex in learning and recall of enhanced extinction. J. Neurosci. 39, 3264–3276 (2019).
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.
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).
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).
Waelti, P., Dickinson, A. & Schultz, W. Dopamine responses comply with basic assumptions of formal learning theory. Nature 412, 43–48 (2001).
Hu, H. Reward and aversion. Annu. Rev. Neurosci. 39, 297–324 (2016).
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).
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.
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).
Stuber, G. D. et al. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475, 377–380 (2011).
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.
Namburi, P. et al. A circuit mechanism for differentiating positive and negative associations. Nature 520, 675–678 (2015).
Janak, P. H. & Tye, K. M. From circuits to behaviour in the amygdala. Nature 517, 284–292 (2015).
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).
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).
Ferenczi, E. A. et al. Prefrontal cortical regulation of brainwide circuit dynamics and reward-related behavior. Science 351, aac9698 (2016).
Otis, J. M. et al. Prefrontal cortex output circuits guide reward seeking through divergent cue encoding. Nature 543, 103–107 (2017).
Haber, S. N. & Knutson, B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26 (2009).
Delgado, M. R. Reward-related responses in the human striatum. Ann. N. Y. Acad. Sci. 1104, 70–88 (2007).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Killcross, S. & Coutureau, E. Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb. Cortex 13, 400–408 (2003).
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).
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).
Van Overwalle, F. A dissociation between social mentalizing and general reasoning. NeuroImage 54, 1589–1599 (2011).
Delgado, M. R. et al. Viewpoints: dialogues on the functional role of the ventromedial prefrontal cortex. Nat. Neurosci. 19, 1545–1552 (2016).
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).
O’Doherty, J. et al. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304, 452–454 (2004).
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.
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.
Askew, C. & Field, A. P. Vicarious learning and the development of fears in childhood. Behav. Res. Ther. 45, 2616–2627 (2007).
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).
Enquist, M., Eriksson, K. & Ghirlanda, S. Critical social learning: a solution to Rogers’s paradox of nonadaptive culture. Am. Anthropol. 109, 727–734 (2007).
Rendell, L. et al. Why copy others? Insights from the social learning strategies tournament. Science 328, 208–213 (2010).
Joiner, J., Piva, M., Turrin, C. & Chang, S. W. C. Social learning through prediction error in the brain. NPJ Sci. Learn 2, 8 (2017).
Amodio, D. M. & Frith, C. D. Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 7, 268–277 (2006).
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).
Stanley, D. A. & Adolphs, R. Toward a neural basis for social behavior. Neuron 80, 816–826 (2013).
Zaki, J. Empathy: a motivated account. Psychol. Bull. 140, 1608–1647 (2014).
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).
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).
Yusufishaq, S. & Rosenkranz, J. A. Post-weaning social isolation impairs observational fear conditioning. Behav. Brain Res. 242, 142–149 (2013).
Inagaki, H. et al. Identification of a pheromone that increases anxiety in rats. Proc. Natl Acad. Sci. USA 111, 18751–18756 (2014).
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).
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.
Dezecache, G., Jacob, P. & Grèzes, J. Emotional contagion: its scope and limits. Trends Cogn. Sci. 19, 297–299 (2015).
Keum, S. & Shin, H.-S. Rodent models for studying empathy. Neurobiol. Learn. Mem. 135, 22–26 (2016).
Knapska, E., Mikosz, M., Werka, T. & Maren, S. Social modulation of learning in rats. Learn. Mem. 17, 35–42 (2010).
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).
de Waal, F. B. M. & Preston, S. D. Mammalian empathy: behavioural manifestations and neural basis. Nat. Rev. Neurosci. 18, 489–509 (2017).
Masserman, J. H., Wechkin, S. & Terris, W. ‘Altruistic’ behavior in rhesus monkeys. Am. J. Psychiatry 121, 584–585 (1964).
Brass, M. & Heyes, C. Imitation: is cognitive neuroscience solving the correspondence problem? Trends Cogn. Sci. 9, 489–495 (2005).
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).
Golkar, A. & Olsson, A. The interplay of social group biases in social threat learning. Sci. Rep. 7, 7685 (2017).
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).
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).
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.
Suzuki, S. et al. Learning to simulate others’ decisions. Neuron 74, 1125–1137 (2012).
Kilner, J. M., Friston, K. J. & Frith, C. D. Predictive coding: an account of the mirror neuron system. Cogn. Process. 8, 159–166 (2007).
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).
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).
Carlin, J. D. & Calder, A. J. The neural basis of eye gaze processing. Curr. Opin. Neurobiol. 23, 450–455 (2013).
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).
Hill, C. A. et al. A causal account of the brain network computations underlying strategic social behavior. Nat. Neurosci. 20, 1142–1149 (2017).
Falk, E. B. et al. The neural correlates of persuasion: a common network across cultures and media. J. Cogn. Neurosci. 22, 2447–2459 (2010).
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).
Saxe, R. & Houlihan, S. D. Formalizing emotion concepts within a Bayesian model of theory of mind. Curr. Opin. Psychol. 17, 15–21 (2017).
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.
Atsak, P. et al. Experience modulates vicarious freezing in rats: a model for empathy. PLoS ONE 6, e21855 (2011).
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).
Chen, Q., Panksepp, J. B. & Lahvis, G. P. Empathy is moderated by genetic background in mice. PLoS ONE 4, e4387 (2009).
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).
Mineka, S., Davidson, M., Cook, M. & Keir, R. Observational conditioning of snake fear in rhesus monkeys. J. Abnorm. Psychol. 93, 355–372 (1984).
Reynolds, G., Field, A. P. & Askew, C. Learning to fear a second-order stimulus following vicarious learning. Cogn. Emot. 31, 572–579 (2017).
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).
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.
Olsson, A. & Phelps, E. A. Learned fear of “unseen” faces after Pavlovian, observational, and instructed fear. Psychol. Sci. 15, 822–828 (2004).
Carrillo, M. et al. Emotional mirror neurons in the rat’s anterior cingulate cortex. Curr. Biol. 29, 1301–1312.e6 (2019).
Bissière, S. et al. The rostral anterior cingulate cortex modulates the efficiency of amygdala-dependent fear learning. Biol. Psychiatry 63, 821–831 (2008).
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.
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).
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).
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).
Terburg, D. et al. The basolateral amygdala is essential for rapid escape: a human and rodent study. Cell 175, 723–735.e16 (2018).
Wang, S. et al. The human amygdala parametrically encodes the intensity of specific facial emotions and their categorical ambiguity. Nat. Commun. 8, 14821 (2017).
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).
Olsson, A. et al. Vicarious fear learning depends on empathic appraisals and trait empathy. Psychol. Sci. 27, 25–33 (2016).
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).
Golkar, A., Selbing, I., Flygare, O., Öhman, A. & Olsson, A. Other people as means to a safe end. Psychol. Sci. 24, 2182–2190 (2013).
Chang, S. W. C., Winecoff, A. A. & Platt, M. L. Vicarious reinforcement in rhesus macaques (Macaca mulatta). Front. Neurosci. 5, 27 (2011).
Kendal, R. et al. Chimpanzees copy dominant and knowledgeable individuals: implications for cultural diversity. Evol. Hum. Behav. 36, 65–72 (2015).
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).
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).
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).
Berger, S. M. Conditioning through vicarious instigation. Psychol. Rev. 69, 450–466 (1962).
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.
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).
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).
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).
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).
Atlas, L. Y. & Phelps, E. A. Prepared stimuli enhance aversive learning without weakening the impact of verbal instructions. Learn. Mem. 25, 100–104 (2018).
Costa, V. D., Bradley, M. M. & Lang, P. J. From threat to safety: instructed reversal of defensive reactions. Psychophysiology 52, 325–332 (2015).
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).
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).
Posadas-Andrews, A. & Roper, T. J. Social transmission of food-preferences in adult rats. Anim. Behav. 31, 265–271 (1983).
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).
Munger, S. D. et al. An olfactory subsystem that detects carbon disulfide and mediates food-related social learning. Curr. Biol. 20, 1438–1444 (2010).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Mobbs, D. et al. A key role for similarity in vicarious reward. Science 324, 900 (2009).
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).
Singer, T. et al. Empathic neural responses are modulated by the perceived fairness of others. Nature 439, 466–469 (2006).
Lindström, B., Selbing, I. & Olsson, A. Co-evolution of social learning and evolutionary preparedness in dangerous environments. PLoS ONE 11, e0160245 (2016).
Bunch, G. B. & Zentall, T. R. Imitation of a passive avoidance response in the rat. Bull. Psychon. Soc. 15, 73–75 (1980).
Del Russo, J. E. Observational learning of discriminative avoidance in hooded rats. Anim. Learn. Behav. 3, 76–80 (1975).
Masuda, A. & Aou, S. Social transmission of avoidance behavior under situational change in learned and unlearned rats. PLoS ONE 4, e6794 (2009).
Masuda, A. & Aou, S. Lesions of the medial prefrontal cortex enhance social modulation of avoidance. Behav. Brain Res. 217, 309–314 (2011).
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).
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).
Huang, I.-N., Koski, C. A. & DeQuardo, J. R. Observational learning of a bar-press by rats. J. Gen. Psychol. 108, 103–111 (1983).
Zentall, T. R. & Levine, J. M. Observational learning and social facilitation in the rat. Science 178, 1220–1221 (1972).
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).
Groesbeck, R. W. & Duerfeldt, P. H. Some relevant variables in observational learning of the rat. Psychon. Sci. 22, 41–43 (1971).
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).
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).
Hill, M. R., Boorman, E. D. & Fried, I. Observational learning computations in neurons of the human anterior cingulate cortex. Nat. Commun. 7, 12722 (2016).
Apps, M. A. J. & Sallet, J. Social learning in the medial prefrontal cortex. Trends Cogn. Sci. 21, 151–152 (2017).
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.
Apps, M. A. J. & Ramnani, N. The anterior cingulate gyrus signals the net value of others’ rewards. J. Neurosci. 34, 6190–6200 (2014).
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.
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).
Hesslow, G. The current status of the simulation theory of cognition. Brain Res. 1428, 71–79 (2012).
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).
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).
Dorrance, B. R. & Zentall, T. R. Imitation of conditional discriminations in pigeons (Columba livia). J. Comp. Psychol. 116, 277–285 (2002).
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).
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).
Biele, G., Rieskamp, J., Krugel, L. K. & Heekeren, H. R. The neural basis of following advice. PLoS Biol. 9, e1001089 (2011).
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).
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).
Fazio, R. H., Eiser, J. R. & Shook, N. J. Attitude formation through exploration: valence asymmetries. J. Pers. Soc. Psychol. 87, 293–311 (2004).
Staudinger, M. R. & Büchel, C. How initial confirmatory experience potentiates the detrimental influence of bad advice. NeuroImage 76, 125–133 (2013).
Bikhchandani, S., Hirshleifer, D. & Welch, I. Learning from the behavior of others: conformity, fads, and informational cascades. J. Econ. Perspect. 12, 151–170 (1998).
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).
Selbing, I. & Olsson, A. Beliefs about others’ abilities alter learning from observation. Sci. Rep. 7, 16173 (2017).
Vostroknutov, A., Polonio, L. & Coricelli, G. The role of intelligence in social learning. Sci. Rep. 8, 6896 (2018).
Collette, S., Pauli, W. M., Bossaerts, P. & O’Doherty, J. Neural computations underlying inverse reinforcement learning in the human brain. eLife 6, e29718 (2017).
Ng, A. Y. & Russell, S. in Proceedings of the Seventeenth International Conference on Machine Learning (ed. Langley, P.) 663–670 (Morgan Kaufmann, 2000).
Heyes, C. Who knows? Metacognitive social learning strategies. Trends Cogn. Sci. 20, 204–213 (2016).
Jara-Ettinger, J. Theory of mind as inverse reinforcement learning. Curr. Opin. Behav. Sci. 29, 105–110 (2019).
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).
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).
Rendell, L. et al. Cognitive culture: theoretical and empirical insights into social learning strategies. Trends Cogn. Sci. 15, 68–76 (2011).
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).
Pike, T. W. & Laland, K. N. Conformist learning in nine-spined sticklebacks’ foraging decisions. Biol. Lett. 6, 466–468 (2010).
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.
van Leeuwen, E. J. C. & Haun, D. B. M. Conformity in nonhuman primates: fad or fact? Evol. Hum. Behav. 34, 1–7 (2013).
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).
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).
Klucharev, V., Hytönen, K., Rijpkema, M., Smidts, A. & Fernández, G. Reinforcement learning signal predicts social conformity. Neuron 61, 140–151 (2009).
Nook, E. C. & Zaki, J. Social norms shift behavioral and neural responses to foods. J. Cogn. Neurosci. 27, 1412–1426 (2015).
Suzuki, S., Adachi, R., Dunne, S., Bossaerts, P. & O’Doherty, J. P. Neural mechanisms underlying human consensus decision-making. Neuron 86, 591–602 (2015).
Parkinson, C. & Wheatley, T. The repurposed social brain. Trends Cogn. Sci. 19, 133–141 (2015).
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.
Heyes, C. Enquire within: cultural evolution and cognitive science. Philos. Trans. R. Soc. B Biol. Sci. 373, 20170051 (2018).
Heyes, C. & Pearce, J. M. Not-so-social learning strategies. Proc. R. Soc. B Biol. Sci. 282, 20141709 (2015).
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.
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).
Chang, D.-J. & Debiec, J. Neural correlates of the mother-to-infant social transmission of fear. J. Neurosci. Res. 94, 526–534 (2016).
Sanders, J., Mayford, M. & Jeste, D. Empathic fear responses in mice are triggered by recognition of a shared experience. PLoS ONE 8, e74609 (2013).
Öhman, A. & Mineka, S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol. Rev. 108, 483–522 (2001).
Cohen, J. D. et al. Computational approaches to fMRI analysis. Nat. Neurosci. 20, 304–313 (2017).
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).
Diaconescu, A. O. et al. Hierarchical prediction errors in midbrain and septum during social learning. Soc. Cogn. Affect. Neurosci. 12, 618–634 (2017).
Mineka, S. & Cook, M. Mechanisms involved in the observational conditioning of fear. J. Exp. Psychol. Gen. 122, 23–38 (1993).
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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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
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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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DOI: https://doi.org/10.1038/s41583-020-0276-4
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