Search

Learning to predict threat depends on amygdala plasticity and does not require auditory cortex (ACX) when threat predictors (conditioned stimuli, CS) are simple sine tones. However, ACX is required in rodents to learn from some naturally occurring CS. Yet, the precise function of ACX, and whether it differs for different CS types, is unknown. Here, we address how ACX encodes threat predictions during human fear conditioning using functional magnetic resonance imaging (fMRI) with multivariate pattern analysis. As in previous rodent work, CS+ and CS- were defined either by direction of frequency modulation (complex) or by frequency of pure tones (simple). In an instructed non-reinforcement context, different sets of simple and complex sounds were always presented without reinforcement (neutral sounds, NS). Threat encoding was measured by separation of fMRI response patterns induced by CS+/CS-, or similar NS1/NS2 pairs. We found that fMRI patterns in Heschl's gyrus encoded threat prediction over and above encoding the physical stimulus features also present in NS, i.e. CS+/CS- could be separated better than NS1/NS2. This was the case both for simple and complex CS. Furthermore, cross-prediction demonstrated that threat representations were similar for simple and complex CS, and thus unlikely to emerge from stimulus-specific top-down, or learning-induced, receptive field plasticity. Searchlight analysis across the entire ACX demonstrated further threat representations in a region including BA22 and BA42. However, in this region, patterns were distinct for simple and complex sounds, and could thus potentially arise from receptive field plasticity. Strikingly, across participants, individual size of Heschl's gyrus predicted strength of fear learning for complex sounds. Overall, our findings suggest that ACX represents threat predictions, and that Heschl's gyrus contains a threat representation that is invariant across physical stimulus categories. [ABSTRACT FROM AUTHOR]

Abstract: Specific neuronal subpopulations within specific brain areas are responsible for learning and memory. A fear memory engages a subset of lateral amygdala neurons, but whether multiple contextual fear memories engage the same or different subsets of lateral amygdala neurons remains unclear. Here, we demonstrate the representation of multiple contextual fear memories in the amygdala with cellular and temporal resolution using a large-scale imaging method. Mice were conditioned with a footshock in 2 separate chambers. They were then re-exposed to either the same conditioning chamber twice or 2 different conditioning chambers. The activities of individual neurons related to the re-exposures were determined by the subcellular distribution of Arc/Arg3.1 RNA. Reactivation of different memories activated partially (about 50%) overlapping neurons, whereas reactivation of the same memory activated more overlapping (about 65%) neurons. These findings indicate that lateral amygdala neurons related to different fear memories are partly common, and that a small but significant neuronal population (2.7% of total lateral amygdala neurons) encodes differences in individual fear memories. Moreover, memory retrieval increased the size of the neuronal subpopulation activated during subsequent retrieval. Taken together, our findings indicate that small plastic subsets of neurons encode fear memories from individual contexts. [Copyright &y& Elsevier]