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E M OT I O N A N D D I S O R D E R S O F E M OT I O N

REVIEW

Social learning of fear

Andreas Olsson1 & Elizabeth A Phelps2,3

Research across species highlights the critical role of the amygdala in fear conditioning. However, fear conditioning, involving direct aversive experience, is only one means by which fears can be acquired. Exploiting aversive experiences of other individuals through social fear learning is less risky. Behavioral research provides important insights into the workings of social fear learning, and the neural mechanisms are beginning to be understood. We review research suggesting that an amygdala-centered model of fear conditioning can help to explain social learning of fear through observation and instruction. We also describe how observational and instructed fear is distinguished by involvement of additional neural systems implicated in social-emotional behavior, language and explicit memory, and propose a modified conditioning model to account for social fear learning. A better understanding of social fear learning promotes integration of biological principles of learning with cultural evolution.

Learning about potentially harmful stimuli and events is critical in shaping adaptive behavior in a rapidly changing environment. It allows animals to establish and update associations between external events and motivational states such as fear. Fear can be expressed, transmitted and acquired in various ways. For example, you might fear a particular neighborhood because you were assaulted there, because you saw someone being assaulted there, or because someone told you an intimidating anecdote about a similar crime there. Thus, fears can be acquired through direct experiences or indirectly through social transmission (Fig. 1ac). In all cases, your fear of the locality might express itself similarly, such as by avoidance of the locality and increased autonomic arousal when approaching it. These responses might serve you well. However, if the experienced assault was a one- time event, the observed event a scene in a movie, or the anecdote a distortion of reality, your responses might disrupt normal functioning, especially if the neighborhood was your home.

Whereas the neural circuitry of fear learning through classical conditioning is understood in considerable detail, researchers have just begun to study the neural mechanisms underlying social fear learning. Although similar neural processes may support direct and indirect fear learning, a distributed network of regions is involved in social perception and evaluation. Our aim is to survey cross-species work on social fear learning in light of our current understanding of the social brain and to outline a model describing how social interaction can guide affective processes underlying acquisition and expression of fear learning.

We begin by summarizing the neural substrates of direct fear learning through classical (pavlovian) fear conditioning with an emphasis on the role of the amygdala. Next, we selectively review behavioral findings of observational fear learning in nonhuman animals, followed by research on social fear learning in humans.

1 2 Department of Psychology, Columbia University, New York, New York, USA. Department of Psychology and 3Center for Neural Science, New York University, New York, New York, USA. Correspondence should be addressed to A.O. (aolsson@psych.columbia.edu).

Published online 28 August 2007; doi:10.1038/nn1968

Taken together, this work implies that the basic associative learning processes that are responsible for acquisition and expression of learned fear are similar across species and across different learning procedures, such as social observation and verbal instruction. However, social, affective and cognitive processes are likely to contribute to fear learning in a social context. Based on this literature, we propose a neural model for how social-affective processes contribute to acquisition and expres- sion of fears acquired through social means (Fig. 2ac).

Fear conditioning Most of our knowledge about basic neurobiological mechanisms of fear learning stems from classical conditioning. In a typical fear conditioning protocol, a neutral conditioned stimulus (CS) is paired with a naturally aversive stimulus (unconditioned stimulus, US), leading to a conditioned fear response to the CS. The extensive use of fear conditioning protocols since Pavlov1 has established this procedure as a model of fear learning2. Consistency in the physiological expression of conditioned fear elicited by the basic protocol indicates that mechanisms of emotional learning are analogous across species.

Research on the neurobiology of fear conditioning has focused on the amygdala in the medial temporal lobe, a key structure in the brain’s fear circuitry (Fig. 2a). Although the amygdala processes a wide range of emotionally relevant information, much of its anatomical and functional role in fear conditioning is homologous and analogous across species. The amygdala is a conglomerate of subnuclei, some of which have specific roles in fear conditioning. In rodents, sensory information arrives in the lateral nucleus from the thalamus and sensory cortices3,4. The lateral nucleus also receives nocioceptive information and is where synaptic plasticity builds an association between representations of the CS and US5–7. The lateral nucleus further projects to the central nucleus and basal nucleus, which mediates the output to other regions that regulate expression of fear and anxiety8. For example, projections to the hypothalamus9 are important for mediation of autonomic responses, which in humans can be indexed through the skin conductance response10. Other areas of projection, such as the ventral tegmental area11 and the central gray12 are important in regulation of behavioral expressions of fear.

NATURE NEUROSCIENCE VOLUME 10

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NUMBER 9

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SEPTEMBER 2007

1095

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