Short and Long-term memory in Drosophila require cAMP signaling in distinct neuron types

By Allison Blum, Wanhe Li, Michael Cressy, Josh Dubnau. 2009

189 citations recorded by the source corpus.

Summary Background A common feature of memory and its underlying synaptic plasticity is that each can be dissected into short-lived forms involving modification or trafficking of existing proteins and long-term forms that require new gene expression. An underlying assumption of this cellular view of memory consolidation is that these different mechanisms occur within a single neuron. At the neuro-anatomical level, however, different temporal stages of memory can engage distinct neural circuits, a notion that has not been conceptually integrated with the cellular view. Results We have investigated this issue in the context of aversive Pavlovian olfactory memory in Drosophila. Previous studies have demonstrated a central role for cAMP signaling in the mushroom body (MB). The Ca++ responsive adenylyl cyclase rutabaga is believed to be a coincidence detector in γ neurons, one of the three principle classes of MB Kenyon cells. We are able to separately restore short-term or long-term memory to a rutabaga mutant with expression of rutabaga in different subsets of MB neurons. Conclusions Our findings suggest a model in which the learning experience initiates two parallel associations: a short-lived trace in MB γ neurons, and a long-lived trace in α/β neurons.

Subfields: Cellular and Molecular Neuroscience, Immunology, Molecular Biology

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “DOI: 10.7554/eLife.16135.001”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “…our results indicate that circuits in the α lobe play key roles in long-term aversive and appetitive memory (Figure 10) (Pascual and Preat, 2001; Isabel et al., 2004; Yu et al., 2006; Blum et al., 2009; Sejourne et al., 2011; Cervantes-Sandoval et al., 2013; Pai et al., 2013; Placais et al., 2013).”
A connectome of a learning and memory center in the adult Drosophila brain (2017, methodology): “We have densely reconstructed the connectome of the a lobe of the adult Drosophila MB, a region essential for long-term associative memory (Pascual and Préat, 2001; Pai et al., 2013; Yu et al., 2006; Séjourné et al., 2011; Akalal et al., 2011; Blum et al., 2009; Trannoy et al., 2011).”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, unknown): “We further hypothesize that the genes identified so far represent only a fraction of the genes involved in LTM.”
Pain-relief learning in flies, rats, and man: basic research and applied perspectives (2014, background): “2011), with the AC-cAMP-PKA signaling cascade as one of the necessary processes involved in molecular coincidence detection (Zars et al. 2000; Thum et al. 2007; Blum et al. 2009; Tomchik and Davis 2009; for a similar conclusion for appetitive learning, see Gervasi et al. 2010; for discussions of pur”
System-like consolidation of olfactory memories in Drosophila (2013, background): “Second, the STM deficit of the rutabaga (rut, calciumdependent adenylyl cyclase) mutant in aversive memory can be partially rescued by expression of a rut wild-type transgene in MBNs, whereas the LTM deficit is partially rescued with expression in / MB cells (Zars et al., 2000; Akalal et al., 2006; ”
Shared mushroom body circuits underlie visual and olfactory memories in Drosophila (2014, background): “In olfactory conditioning, the γ lobe was shown to contribute mainly to short-term memory (Zars et al., 2000; Isabel et al., 2004; Blum et al., 2009; Trannoy et al., 2011; Qin et al., 2012).”
Event Timing in Associative Learning: From Biochemical Reaction Dynamics to Behavioural Observations (2012, background): “, loss of function mutations [30,32,33], RNAiknockdown [62].”
Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability (2012, background): “These results indicate shock reinforcement recruits a specific set of the dopamine pathways to the MBs and induces multiple memory traces in Kenyon cells through different receptors [18,30,32].”
The Biology of Forgetting – A Perspective (2017, background): “The current evidence suggests that STM relies primarily on the g MBn, while LTM relies on the a/b MBn (Zars et al., 2000; Isabel et al., 2004; Akalal et al., 2006; Blum et al., 2009; Huang et al., 2012, 2013; Xie et al., 2013).”
Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila (2013, unknown): “…g in short-term memory, for a0b0 after training for memory consolidation, and for ab in later memory retrieval, with the ab requirement becoming more pro- nounced as time passes (Zars et al., 2000; Yu et al., 2006; Krashes et al., 2007; Blum et al., 2009; Trannoy et al., 2011; Qin et al., 2012).”
Are mushroom bodies cerebellum-like structures? (2011, background): “…consolidation and recall (Zars et al., 2000; Dubnau et al., 2001; Pascual and Préat, 2001; Yu et al., 2006; Krashes et al., 2007; Wang et al., 2008; Blum et al., 2009), and identify loci of plasticity both pre- and postsynaptic to Kenyon cells (Mauelshagen, 1993; Menzel and Manz, 2005; Yu et al.,…”
Forgetting is regulated through Rac activity in Drosophila. (2010, unknown): “Moreover, as genetic background controls, elav-Gal4/+; Gal80ts/+; UASDrac1(N17)/+ flies without heat shock induction showed normal learning and memory performance (Figure S1I).”
The Long-Term Memory Trace Formed in the Drosophilaα/β Mushroom Body Neurons is abolished in Long-Term Memory Mutants (2011, unknown): “, 1998) and behavioral experiments that target expression of rescuing transgenes in specific subsets of these neurons (Zars et al., 2000; McGuire et al., 2003; Blum et al., 2009).”