γ neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila

By H. Qin, Michael Cressy, Wanhe Li, Jonathan S. Coravos, Stephanie A. Izzi, Josh Dubnau. 2012

185 citations recorded by the source corpus.

SUMMARY Mushroom body (MB) dependent olfactory learning in Drosophila provides a powerful model to investigate memory mechanisms. MBs integrate olfactory conditioned stimuli (CS) inputs with neuromodulatory reinforcement (unconditioned stimuli, US) [1, 2], which for aversive learning is thought to rely on dopaminergic (DA) signaling [3–6] to DopR, a D1-like dopamine receptor expressed in MB [7, 8]. A wealth of evidence suggests the conclusion that parallel and independent signaling occurs downstream of DopR within two MB neuron cell types, with each supporting half of memory performance. For instance, expression of the rutabaga adenylyl cyclase (rut) in γ neurons is sufficient to restore normal learning to rut mutants [9] whereas expression of Neurofibromatosis I (NFI) in α/β neurons is sufficient to rescue NF1 mutants [10, 11]. DopR mutations are the only case where memory performance is fully eliminated [7], consistent with the hypothesis that DopR receives the US inputs for both γ and α/β lobe traces. We demonstrate, however, that DopR expression in γ neurons is sufficient to fully support short (STM) and long-term memory (LTM). We argue that DA-mediated CS-US association is formed in γ neurons followed by communication between γ and α/β neurons to drive consolidation.

Subfields: Cellular and Molecular Neuroscience, Genetics, Insect Science

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “…Dopamine signaling to KCs has been implicated in both learning and forgetting (Schwaerzel et al., 2003; Schroll et al., 2006, Kim et al., 2007; Tomchik and Davis, 2009; Gervasi et al., 2010; Qin et al., 2012; Placais et al., 2012; Berry et al., 2012; Boto et al., 2014; Shuai et al., 2015).”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “Indeed, while DopR1 in KCs is essential to the formation of learned olfactory associations (Kim et al., 2007; Qin et al., 2012), we find this receptor plays only a subtle role in the context-dependent patterning of Ca 2+ along their axons.”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “…formation (Livingstone et al., 1984; Zars et al., 2000; Schwaerzel et al., 2003; Kim et al., 2007; McGuire et al., 2003; Gervasi et al., 2010; Qin et al., 2012) and rutabaga was shown to be required for the establishment of the differences in MBON odor tuning between individuals (Hige et…”
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; ”
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].”
Active Protection: Learning-Activated Raf/MAPK Activity Protects Labile Memory from Rac1-Independent Forgetting. (2018, unknown): “First, g neurons are believed to be a primary location for the acquisition and expression of early memory (Boto et al., 2014; Guven-Ozkan and Davis, 2014; Hige et al., 2015; Qin et al., 2012; Zhang and Roman, 2013).”
Two independent mushroom body output circuits retrieve the six discrete components of Drosophila aversive memory. (2015, background): “STM is thought to be encoded in g KCs (Blum et al., 2009; Qin et al., 2012) and LTM in a/b KCs (Blum et al.”
The Drosophila Mushroom Body: From Architecture to Algorithm in a Learning Circuit. (2020, background): “The dopamine receptor as well as many signaling pathway components involved in learning have the KCs as their site of action (Davis 2005, Kim et al. 2007, Margulies et al. 2005, Qin et al. 2012).”
Dissecting neural pathways for forgetting in Drosophila olfactory aversive memory (2015, background): “Rac-mediated forgetting has been localized to a large population of KCs (6), including the γ-subset, which is also critical for initial memory formation (21, 27).”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, unknown): “While we confirmed that KCs express DopR, DopR2, OAMB, and 5-HT1A and 1B receptors (Han et al., 1998; Han et al., 1996; Qin et al., 2012; Silva et al., 2014; Yuan et al., 2006), we discovered that these receptors are also expressed in MBONs, but at lower levels than in the KCs (see also Figure S5).”
A connectome of a learning and memory center in the adult Drosophila brain (2017, background): “Cell-type-specific rescue of dopamine receptor mutants suggests that dopamine acts presynaptically in the KCs of KC>MBON synapses (Kim et al., 2007; Qin et al., 2012a; Liu et al., 2012; Ichinose et al., 2015).”
Modelling learning and memory in Drosophila to understand Intellectual Disabilities. (2020, unknown): “This process is believed to form the neural basis of olfactory associative learning (Heisenberg, 2003; Schwaerzel et al., 2003; Kim et al., 2007; Burke et al., 2012; Liu et al., 2012; Qin et al., 2012; Cohn et al., 2015; Hige et al., 2015; Owald and Waddell, 2015; Rohwedder et al., 2016; Kaun and Ro”
Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning (2019, background): “While naive odor tracking in DopR1 and DopR2 mutant animals was indistinguishable from wild-type animals (Figures S8E–S8S), DopR1 mutants failed to vigorously track ACV after forward conditioning with PAM activation (Figures 7A, S8A, and S8C), in line with behavioral evidence that DopR1 is required ”
Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila (2013, background): “…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).”
Dopamine activity in projection neurons regulates short‐lasting olfactory approach memory in Drosophila (2022, background): “Activity of D1Rs in the MBs is required for olfactory aversive learning (Kim et al., 2007; Qin et al., 2012).”