D1 Dopamine Receptor dDA1 Is Required in the Mushroom Body Neurons for Aversive and Appetitive Learning in Drosophila

By Young-cho Kim, Hyun-Gwan Lee, K. Han. 2007

381 citations recorded by the source corpus.

Drosophila has robust behavioral plasticity to avoid or prefer the odor that predicts punishment or food reward, respectively. Both types of plasticity are mediated by the mushroom body (MB) neurons in the brain, in which various signaling molecules play crucial roles. However, important yet unresolved molecules are the receptors that initiate aversive or appetitive learning cascades in the MB. We have shown previously that D1 dopamine receptor dDA1 is highly enriched in the MB neuropil. Here, we demonstrate that dDA1 is a key receptor that mediates both aversive and appetitive learning in pavlovian olfactory conditioning. We identified two mutants, dumb1 and dumb2, with abnormal dDA1 expression. When trained with the same conditioned stimuli, both dumb alleles showed negligible learning in electric shock-mediated conditioning while they exhibited moderately impaired learning in sugar-mediated conditioning. These phenotypes were not attributable to anomalous sensory modalities of dumb mutants because their olfactory acuity, shock reactivity, and sugar preference were comparable to those of control lines. Remarkably, the dumb mutant's impaired performance in both paradigms was fully rescued by reinstating dDA1 expression in the same subset of MB neurons, indicating the critical roles of the MB dDA1 in aversive as well as appetitive learning. Previous studies using dopamine receptor antagonists implicate the involvement of D1/D5 receptors in various pavlovian conditioning tasks in mammals; however, these have not been supported by the studies of D1- or D5-deficient animals. The findings described here unambiguously clarify the critical roles of D1 dopamine receptor in aversive and appetitive pavlovian conditioning.

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Insect Science

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “…in one compartment 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…”
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): “…the rutabaga gene, are required specifically in the KCs for memory 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…”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, background): “In addition, D1-like dopamine receptors in the KCs are necessary to form olfactory memories (Kim et al., 2007).”
Dopamine Is Required for Learning and Forgetting in Drosophila (2012, positive): “However, because dDA1mutants do not form aversive olfactory memories due to the dDA1 role in acquisition (Kim et al., 2007), we chose to look at the potential role for DAMB in forgetting.”
WRITING MEMORIES WITH LIGHT-ADDRESSABLE REINFORCEMENT CIRCUITRY (2009, background): “We do know that dopamine is an essential mediator of aversive reinforcement in adult flies (Schwaerzel et al., 2003; Kim et al., 2007) and that its broad release can substitute for aversive salt conditioning in larvae (Schroll et al.”
Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability (2012, background): “ory, some of which are mapped in the MB [17,21,24,26,27,28,29].”
cAMP signalling in mushroom bodies modulates temperature preference behaviour in Drosophila (2008, background): “Moreover, DopR in MB is required in learning and memory [32].”
Shared mushroom body circuits underlie visual and olfactory memories in Drosophila (2014, positive): “DOI: 10.7554/eLife.02395 9 of 22 Research article we made use of the PiggyBac insertion mutant (dumb2) that contains UAS in the first intron of the DopR gene allowing GAL4-dependent expression of the gene (Kim et al., 2007).”
Modelling learning and memory in Drosophila to understand Intellectual Disabilities. (2020, positive): “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”
Layered reward signaling through octopamine and dopamine in Drosophila (2012, positive): “Flies with the dumb 1 mutation have impaired appetitive memory that can be restored by expressing DopR in the MB 16 .”
Event Timing in Associative Learning: From Biochemical Reaction Dynamics to Behavioural Observations (2012, background): “Blocking the neuronal output from two different, incomplete sets of dopaminergic neurons leaves relief learning intact [16]; however, given the caveats of the genetic techniques used in the respective study, the complementary approach of interfering with dopamine receptor function using genetic [27,”
Dopamine Neurons Mediate Learning and Forgetting through Bidirectional Modulation of a Memory Trace (2018, neutral): “However, differential DA receptor signaling is also involved, with the dDA1 receptor driving learning (Kim et al., 2007; Qin et al., 2012) and the DAMB receptor driving forgetting (Berry et al.”
A Drosophila model for alcohol reward (2011, result): “Our data, however, in combination with other evidence showing the dopamine receptor dDA1 mediates formation of memories associated with sucrose reward in Drosophila”
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).”
Reward signal in a recurrent circuit drives appetitive long-term memory formation (2015, positive): “DOI: 10.7554/eLife.10719 4 of 18 DopR1-mediated appetitive LTM trace is formed in α/β KCs Several lines of evidence suggest that D1-like dopamine receptor (DopR1) is required in KCs for appetitive memory (Kim et al., 2007; Liu et al., 2012; Boto et al., 2014).”
Specific dopaminergic neurons for the formation of labile aversive memory (2010, neutral): “To cancel the effect of the order of reinforcement [1, 49], the first odor was pairedwith reinforcement in half of the experiments and the second odor was paired with reinforcement in the other half.”
Dopaminergic neurons encode a distributed, asymmetric representation of temperature in Drosophila (2013, background): “However, several studies have also uncovered roles of dopaminergic circuits in appetitive forms of learning in flies (Kim et al., 2007; Krashes et al., 2009; Liu et al., 2012).”
Eight Different Types of Dopaminergic Neurons Innervate the Drosophila Mushroom Body Neuropil: Anatomical and Physiological Heterogeneity (2009, neutral): “Past models had envisioned DA inputs as providing uniform innervation of the mushroom bodies to convey US information (Han et al., 1996; Kim et al., 2007).”