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.

Fig. 1

(A) A snap-shot from the movie presented to subjects during the observation stage, depicting the learning model facing a computer screen that displayed the CS+ and CS−. To each of the three shocks paired with a CS+, the model displayed signs of distress (e.g. lowering the eyebrows, raising the cheeks and twisting the right hand indicating the administration of the shock). (B) Mean skin conductance response (SCR) during the test stage to the CS+ (blue bar) and the CS− (yellow bar) and during the observation stage to the model's response to the shock (red bar) and CS− (yellow bar). Error bars show standard error.

Fig. 2

Amygdala activation at P < 0.005, uncorrected, during (A) the test stage for the contrast between CS+ vs CS− (x, y, z = −20, −2, −9 and 19, −2, −7 for the left and right amygdala, respectively) and (B) the observation stage for the contrast between CS+ and US combined vs the CS− (x, y, z = −28, −5, −12 and 23, −2, −10 for the left and right amygdala, respectively). (C) Shows the regions commonly activated in (a) and (b) (P < 0.05, uncorrected; x, y, z = −20, −9, −13 and 19, −6, −10 for the left and right amygdala, respectively). Region of interest (ROI) time courses for amygdala activation (percent signal change) in the (D) left and (E) right amygdala to the CS+ (blue line) and CS− (green line) during the test stage, and the (F) left and (G) right amygdala to the CS+ (blue line), US (red line) and CS− (green line) during the observation stage. ROIs were extracted from the CS+ vs CS− contrast during the test stage, with a P-threshold of P < 0.005, uncorrected. Error bars show standard error.