Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning

By Annie Handler, Thomas G. W. Graham, Raphael Cohn, Ianessa Morantte, Andrew F. Siliciano, Jianzhi Zeng, Yulong Li, V. Ruta. 2019

199 citations recorded by the source corpus.

Animals rely on the relative timing of events in their environment to form and update predictive associations, but the molecular and circuit mechanisms for this temporal sensitivity remain incompletely understood. Here we show that olfactory associations in Drosophila can be written and reversed on a trial-by-trial basis depending on the temporal relationship between an odor cue and dopaminergic reinforcement. Through the synchronous recording of neural activity and behavior, we show that reversals in learned odor attraction correlate with bidirectional neural plasticity in the mushroom body, the associative olfactory center of the fly. Two dopamine receptors, DopR1 and DopR2, contribute to this temporal sensitivity by coupling to distinct second-messengers and directing either synaptic depression or potentiation. Our results reveal how dopamine receptor signaling pathways can detect the order of events to instruct opposing forms of synaptic and behavioral plasticity, allowing animals to flexibly update their associations in a dynamic environment.

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Genetics

How researchers see this paper

The researchers whose trusted networks rank it highest, strongest advocate first. Every researcher gets a different order.

In Cellular and Molecular Neuroscience

1. Liyuan Wang
2. Qian Li
3. Yi Zhong
4. Jun Zhu
5. Xingxing Zhang
6. Hang Su
7. Mingtian Zhang
8. Lisa Scheunemann

In Ecology, Evolution, Behavior and Systematics

1. Qian Li
2. Yi Zhong
3. D. Owald

In Genetics

1. Liyuan Wang
2. Jun Zhu
3. Yi Zhong
4. Hang Su
5. Qian Li
6. Lisa Scheunemann
7. Xingxing Zhang
8. D. Owald

Citations in the corpus

• Incorporating neuro-inspired adaptability for continual learning in artificial intelligence (2023, positive): “In this case, the forgetting rates serve to diversify these learners, similar to the neurological strategy of decaying old memories differentially in each compartment 24,36–39 .”
• Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila (2022, background): “…that both pre- and postsynaptic mechanisms of memory storage exist in vertebrates, invertebrate memory- related synaptic plasticity has been largely localized to the presynaptic compartment (Bilz et  al., 2020; Boto et  al., 2014; Handler et  al., 2019; Ehmann et  al., 2018; Tully et  al., 1994).”
• Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila (2019, unknown): “If shock, or artificial DAN activation is presented <45 seconds before odor presentation flies form an appetitive ‘relief memory’ for that odor (Tanimoto et al., 2004; Aso and Rubin, 2016; Handler et al., 2019).”