Learning fears by observing others: the neural systems of social fear transmission

Abstract

Classical fear conditioning has been used as a model paradigm to explain fear learning across species. In this paradigm, the amygdala is known to play a critical role. However, classical fear conditioning requires first-hand experience with an aversive event, which may not be how most fears are acquired in humans. It remains to be determined whether the conditioning model can be extended to indirect forms of learning more common in humans. Here we show that fear acquired indirectly through social observation, with no personal experience of the aversive event, engages similar neural mechanisms as fear conditioning. The amygdala was recruited both when subjects observed someone else being submitted to an aversive event, knowing that the same treatment awaited themselves, and when subjects were subsequently placed in an analogous situation. These findings confirm the central role of the amygdala in the acquisition and expression of observational fear learning, and validate the extension of cross-species models of fear conditioning to learning in a human sociocultural context. Our findings also provides new insights into the relationship between learning from, and empathizing with, fearful others. This study suggests that indirectly attained fears may be as powerful as fears originating from direct experiences.

Negative Emotional Responses Elicited by the Anticipation of Pain in Others: Psychophysiological Evidence

“…The mean level of average and worst pain reported by the observed participants was The present findings corroborate previous findings on vicarious fear conditioning in humans 15,16,17,42,60,72,78 and suggest that seeing others in pain has a profound influence on observers 40 . Specifically, findings indicate that other's pain can serve as a sign of threat, resulting into fearful responses towards previously neutral stimuli.…”

“…The heightened corrugator EMG response and fear-potentiated startle suggest the activation of a self-oriented, aversive system 26,28,39,47,48 . Supporting this idea, the amygdala, a key structure implied in fear responses, plays a critical role in the evocation of the fearpotentiated startle reflex 21,39,46,60,61 . Furthermore, research on personal pain experience has consistently shown that participants display a fear-potentiated startle when experiencing or 18 anticipating pain 25,38,41,47 , particularly when pain is perceived as highly threatening 7 Observers' distress towards pain signals in others likely serve a protective function of preparing observers for dealing with impending threat 40 .…”

“…Furthermore, it provides us with information about when others will likely experience pain and suffer. It is no surprise that studies on vicarious conditioning reveal that signals of pain in others elicit fear and anxiety in observers 40,42,60,78 . Several issues however deserve further scrutiny.…”

Observation of Distressed Conspecific as a Model of Emotional Trauma Generates Silent Synapses in the Prefrontal-Amygdala Pathway and Enhances Fear Learning, but Ketamine Abolishes those Effects

“…In particular, exposure to the person(s) in pain and distress is recognized as a cause of psychological distress, which can produce fear learning (Olsson et al, 2007) and elicit traits of PTSD (Eriksson et al, 2001;Figley, 1995;Munroe, 1999). Such exposure, in contrast to physical pain, recruits the brain circuits for social cognition through multimodal sensory processing.…”

Distinct neural signatures of threat learning in adolescents and adults

“…Electrical shocks, the most widely used UCS in adults, may not be appropriate for adolescents, yet less noxious UCSs typically provoke minimal fear in adolescents (23). To overcome these barriers, we developed a unique task that capitalizes on the intrinsic aversiveness of witnessing fear in others (24). Thus, the task uses a fearful facial expression paired with a scream as the UCS (23).…”