Reward signal in a recurrent circuit drives appetitive long-term memory formation

By Toshiharu Ichinose, Yoshinori Aso, Nobuhiro Yamagata, Ayako Abe, Gerald M. Rubin, Hiromu Tanimoto. 2015

130 citations recorded by the source corpus.

Dopamine signals reward in animal brains. A single presentation of a sugar reward to Drosophila activates distinct subsets of dopamine neurons that independently induce short- and long-term olfactory memories (STM and LTM, respectively). In this study, we show that a recurrent reward circuit underlies the formation and consolidation of LTM. This feedback circuit is composed of a single class of reward-signaling dopamine neurons (PAM-α1) projecting to a restricted region of the mushroom body (MB), and a specific MB output cell type, MBON-α1, whose dendrites arborize that same MB compartment. Both MBON-α1 and PAM-α1 neurons are required during the acquisition and consolidation of appetitive LTM. MBON-α1 additionally mediates the retrieval of LTM, which is dependent on the dopamine receptor signaling in the MB α/β neurons. Our results suggest that a reward signal transforms a nascent memory trace into a stable LTM using a feedback circuit at the cost of memory specificity. DOI: http://dx.doi.org/10.7554/eLife.10719.001

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

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. Yi Zhong
2. Qian Li
3. Yoshinori Aso
4. Gerald M. Rubin
5. Glenn C. Turner
6. Xuchen Zhang
7. Toshihide Hige
8. Lianzhang Wang

In Ecology, Evolution, Behavior and Systematics

1. Gerald M. Rubin
2. Yoshinori Aso
3. Qian Li
4. Yi Zhong
5. Glenn C. Turner
6. Toshihide Hige
7. V. Ruta
8. Raphael Cohn

In Immunology

1. Qian Li
2. Yi Zhong
3. Glenn C. Turner
4. Gerald M. Rubin
5. Toshihide Hige
6. Yoshinori Aso
7. Xuchen Zhang
8. Lianzhang Wang

Citations in the corpus

• Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “…(Yamagata et al., 2015; Huetteroth et al., 2015) and has an unusual circuit structure: its MBON (MBON-a1) appears to form synapses on the dendrites of the DAN that innervates the a1 compartment (PAM-a1) forming a recurrent circuit necessary for longterm memory formation (Ichinose et al., 2015).”
• Dopamine activity in projection neurons regulates short‐lasting olfactory approach memory in Drosophila (2022, background): “Recently, it has become evident that functional feedback loops in the MBs are important in olfactory memory formation (Horiuchi, 2019; Ichinose et al., 2015; Lin et al., 2014; Wu et al., 2017).”
• Cdc42-Dependent Forgetting Regulates Repetition Effect in Prolonging Memory Retention. (2016, background): “It will be of interest to study whether there is a distinct forgetting mechanism for LTM.”
• A connectome of a learning and memory center in the adult Drosophila brain (2017, background): “…observed between DPM and the two MBON-a1s (Table 5); while the role of these connections is unclear, we note that DPM has been shown to play a role in consolidation of long-term appetitive memory (Krashes and Waddell, 2008), a process that takes place in the a1 compartment (Ichinose et al., 2015).”