Functional characterization of the basal amygdala – dorsal BNST pathway during contextual fear conditioning

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Both the basal amygdala (BA) and the bed nucleus of the stria terminalis (BNST) can participate in contextual fear, but it is unclear if contextual fear engrams involve a direct interaction between these two brain regions. To determine if dorsal BNST (dBNST)-projecting neurons in the BA participate in contextual fear engrams, we combined the TetTag mouse with a retrograde tracer to label dBNST-projecting cells in the BA. We identified a population of neurons located in the anterior subdivision of the BA that was activated during fear conditioning and reactivated during retrieval, but that did not project to the dBNST. In contrast, dBNST-projecting neurons located in the posterior BA were activated during contextual fear conditioning, but were not reactivated during retrieval. Similarly, we found neurons in the oval BNST subdivision (ovBNST) that were activated during contextual fear conditioning without being reactivated during retrieval. However, the anterodorsal BNST subdivision (adBNST) was not activated during either contextual fear conditioning or retrieval, underscoring the divergent functionality of these two dBNST subdivisions. Finally, we found that the ovBNST receives a monosynaptic projection from neurons located in the BA. Our results indicate that anterior BA neurons that do not project to the dBNST participate in contextual fear engrams. In contrast, dBNST-projecting neurons in the BA do not appear to participate in contextual fear engrams, but might instead contain a BA -> ovBNST pathway that is active during the initial encoding of contextual fear memories.

SIGNIFICANCE STATEMENT Both the basal amygdala (BA) and the dorsal bed nucleus of the stria terminalis (dBNST) can participate in contextual fear, but it is unclear if this reflects a direct interaction between these two brain regions. BA neurons that do not project to the dBNST were found to be active during both the encoding and retrieval of a contextual fear memory, indicating their participation in a contextual fear engram. In contrast, BA neurons that do project to the dBNST were found to be active during the encoding, but not the retrieval of a contextual fear memory. These findings suggest a direct interaction between the BA and dBNST during the initial encoding, but not the subsequent storage of contextual fear memories.

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