Dataset Information

Selective suppression and recall of long-term memories in Drosophila.

ABSTRACT: Adaptive decision-making depends on the formation of novel memories. In Drosophila, the mushroom body (MB) is the site of associative olfactory long-term memory (LTM) storage. However, due to the sparse and stochastic representation of olfactory information in Kenyon cells (KCs), genetic access to individual LTMs remains elusive. Here, we develop a cAMP response element (CRE)-activity-dependent memory engram label (CAMEL) tool that genetically tags KCs responding to the conditioned stimulus (CS). CAMEL activity depends on protein-synthesis-dependent aversive LTM conditioning and reflects the time course of CRE binding protein 2 (CREB2) activity during natural memory formation. We demonstrate that inhibition of LTM-induced CAMEL neurons reduces memory expression and that artificial optogenetic reactivation is sufficient to evoke aversive behavior phenocopying memory recall. Together, our data are consistent with CAMEL neurons marking a subset of engram KCs encoding individual memories. This study provides new insights into memory circuitry organization and an entry point towards cellular and molecular understanding of LTM storage.

SUBMITTER: Siegenthaler D

PROVIDER: S-EPMC6711512 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Selective suppression and recall of long-term memories in Drosophila.

Siegenthaler Dominique D Escribano Benjamin B Bräuler Vanessa V Pielage Jan J

PLoS biology 20190827 8

Adaptive decision-making depends on the formation of novel memories. In Drosophila, the mushroom body (MB) is the site of associative olfactory long-term memory (LTM) storage. However, due to the sparse and stochastic representation of olfactory information in Kenyon cells (KCs), genetic access to individual LTMs remains elusive. Here, we develop a cAMP response element (CRE)-activity-dependent memory engram label (CAMEL) tool that genetically tags KCs responding to the conditioned stimulus (CS) ...[more]

PMID: 31454345

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Project description:Ensembles of principal neurons in the basolateral amygdala (BLA) generate the initial engrams for fear memories, while projections from the BLA to the medial prefrontal cortex (mPFC) are essential for the encoding, transfer and storage of remote fear memories. We tested the effects of chronic pain on remote fear memories in mice. Male mice underwent classic fear conditioning by pairing a single tone (conditional stimulus, CS) with a single electric foot shock (unconditional stimulus, US). Sciatic nerve constriction was used to induce neuropathic pain at various time points before or after the fear conditioning. The mice with sciatic nerve cuffs implanted 48 h after the fear conditioning showed an increased freezing response to CS when compared to mice without cuffs or when compared to mice in which the nerve cuffing was performed 48 h before the fear conditioning. The enhancing effect of pain on consolidated fear memory was further tested and mice in which the nerve cuffing was performed 14 days after the fear conditioning also showed an increased fear response when tested 56 days later. We used immunostaining to detect morphological changes in the BLA that could suggest a mechanism for the observed increase in fear response. We found an increased number of calbindin/parvalbumin positive neurons in the BLA and increased perisomatic density of GAD65 on projection neurons that connect BLA to mPFC in mice with nerve cuffs. Despite the strong increase of c-Fos expression in BLA and mPFC that was induced by fear recall, neither the BLA to mPFC nor the mPFC to BLA projection neurons were activated in mice with nerve cuffs. Furthermore, non-injured mice had an increased fear response when BLA to mPFC projections were inhibited by a chemogenetic method. In conclusion, this study provides evidence that persistent pain has a significant impact on consolidated fear memories. Very likely the underlying mechanism for this phenomenon is increased inhibitory input onto the BLA to mPFC projection neurons, possibly from neurons with induced parvalbumin expression. Conceivably, the increased fear response to consolidated fear memory is a harbinger for the later development of anxiety and depression symptoms associated with chronic pain.

Dataset Information

Selective suppression and recall of long-term memories in Drosophila.

Publications

Selective suppression and recall of long-term memories in Drosophila.

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