Pattern Analyses Reveal Separate Experience-Based Fear Memories in the Human Right Amygdala

Abstract

Learning fear via the experience of contingencies between a conditioned stimulus (CS) and an aversive unconditioned stimulus (US) is often assumed to be fundamentally different from learning fear via instructions. An open question is whether fear-related brain areas respond differently to experienced CS-US contingencies than to merely instructed CS-US contingencies. Here, we contrasted two experimental conditions where subjects were instructed to expect the same CS-US contingencies while only one condition was characterized by prior experience with the CS-US contingency. Using multivoxel pattern analysis of fMRI data, we found CS-related neural activation patterns in the right amygdala (but not in other fear-related regions) that dissociated between whether a CS-US contingency had been instructed and experienced versus merely instructed. A second experiment further corroborated this finding by showing a categoryindependent neural response to instructed and experienced, but not merely instructed, CS presentations in the human right amygdala. Together, these findings are in line with previous studies showing that verbal fear instructions have a strong impact on both brain and behavior. However, even in the face of fear instructions, the human right amygdala still shows a separable neural pattern response to experience-based fear contingencies.

A review on the effects of verbal instructions in human fear conditioning: Empirical findings, theoretical considerations, and future directions

“…A second caveat, specifically concerning the second hypothesis, is that many similarities between fear learning through instructions and through CS-US pairings are based on comparisons between different experiments, rather than within the same experiment. Only a few studies have directly compared the different learning pathways (Braem et al, 2017;Lovibond, 2003;Mertens, Kuhn, et al, 2016;Mertens & De Houwer, 2016a, Olsson & Phelps, 2004Raes et al, 2014).…”

“…This, of course, entails a high risk of drawing incorrect conclusions about differences and similarities between the two learning pathways because of uncontrolled differences between studies. More recent studies have provided useful procedures to allow for such a comparison (Atlas et al, 2016;Braem et al, 2017;Mertens, Kuhn, et al, 2016;Raes et al, 2014).…”

Pain-related fear – Dissociable neural sources of different fear constructs

“…anterior cingulate, insula, medial prefrontal and orbitofrontal cortices (Tovote et al, 2015;Braem et al, 2017;Meier et al, 2014). The respective brain regions were parcellated according to the Automated Anatomical Labeling (AAL, see Table 3 for the different labels) ( (Shattuck and Leahy, 2002).…”

Initial neural representation of individual rules after first-time instruction

“…Our primary aim to track the initial representational dynamics of newly instructed task rules naturally required an 'aggregation-free' MVPA approach based on single-trial estimates associated with the trial-by-trial coding of individual S-R rule identities. This contrasts with earlier MVPA studies which relied in one way or the other on aggregation schemes either across time [40][41][42][43][44][45] or across individual rule identities 32,34,35,46,47 . Aggregation across individual rule identities improves signal-to-noise ratio regarding representations of task features on a more abstract level, but this generalization comes at the cost of losing specificity regarding individual rule identities.…”