Neural signals of vicarious extinction learning

Abstract

Social transmission of both threat and safety is ubiquitous, but little is known about the neural circuitry underlying vicarious safety learning. This is surprising given that these processes are critical to flexibly adapt to a changeable environment. To address how the expression of previously learned fears can be modified by the transmission of social information, two conditioned stimuli (CS + s) were paired with shock and the third was not. During extinction, we held constant the amount of direct, non-reinforced, exposure to the CSs (i.e. direct extinction), and critically varied whether another individual-acting as a demonstrator-experienced safety (CS + vic safety) or aversive reinforcement (CS + vic reinf). During extinction, ventromedial prefrontal cortex (vmPFC) responses to the CS + vic reinf increased but decreased to the CS + vic safety This pattern of vmPFC activity was reversed during a subsequent fear reinstatement test, suggesting a temporal shift in the involvement of the vmPFC. Moreover, only the CS + vic reinf association recovered. Our data suggest that vicarious extinction prevents the return of conditioned fear responses, and that this efficacy is reflected by diminished vmPFC involvement during extinction learning. The present findings may have important implications for understanding how social information influences the persistence of fear memories in individuals suffering from emotional disorders.

Keywords: amygdala; extinction; social learning; vicarious learning; vmPFC.

Fig. 1.

Experimental design. The experiment was divided into different stages. Within each stage, all CSs were presented eight times each in a pseudorandomized order. During acquisition, two angry faces (CS + s) were repeatedly paired with a mild electric shock (US) given to the participants’ wrist (six reinforced presentations/CS). The third angry face (CS−) was never paired with the shock. During extinction, participants watched a video depicting an individual (the demonstrator) acting calmly when exposed to non-reinforced presentations of the CS− and to one of the previously reinforced CS + s (CS + _{vic safety}), but received shocks on the presentations of the other CS+ (CS + _{vic reinf}; six reinforced presentations). The demonstrator reacted to the shocks by twitching the arm and blinking. Critically, the participants did not receive any shocks during this stage. Finally, participants were then re-exposed to all three CSs after receiving three reminder shocks during the reinstatement test.

Fig. 2.

(a) Mean SCR as a function of experimental stage and conditioned stimulus (CS). (b) Trial-by-trial data for extinction (E1-E) and reinstatement (R1–R8). Note that in order to capture the immediate response to a new context (i.e. the orienting response), the first CS presentation during the reinstatement test was always a CS−. Error bars indicate SEM. *Statistically significant differences (P < 0.05).

Fig. 3.

(a) Activity in the vmPFC ROI increased linearly to CS + _{vic reinf} during extinction learning whereas responses in this region decreased to the CS + _{vic safety.} (b) Functional connectivity during extinction using the vmPFC ROI as seed revealed coupling with a region located in the lateral amygdala and anterior hippocampus that was stronger during the CS + _{vic rein} vs the CS + _{vic safety}. T-values are superimposed on a normalized average structural image. fMRI display threshold: P < 0.005, uncorrected for illustrative purposes. Error bars represent SEM.

Fig. 4.

(a) Mean estimated evoked responses (arbitrary units) within the amygdala during reinstatement testing scaled to the response at onset of each CS. Shaded areas represent SEM. (b) Correlation between amygdala activity during Reinstatement test in the contrast CS + _{vic reinf}>CS + _{vic safety} and the reinstated SCRs for CS + _{vic reinf}>CS + _{vic safety.} T-values are superimposed on a normalized average structural image. fMRI display threshold: P < 0.005, uncorrected for illustrative purposes.

Fig. 5.

(a) Change in vmPFC activity from extinction to reinstatement testing displayed for all CSs separately (b). Mean estimated evoked responses (arbitrary units) within the vmPFC during Reinstatement test scaled to the response at onset of each CS. Shaded areas represent SEM. T-values are superimposed on a normalized average structural image. fMRI display threshold: P < 0.005, uncorrected for illustrative purposes.