Dopaminergic neurons write and update memories with cell-type-specific rules

By Yoshinori Aso, Gerald M. Rubin. 2016

261 citations recorded by the source corpus.

Associative learning is thought to involve parallel and distributed mechanisms of memory formation and storage. In Drosophila, the mushroom body (MB) is the major site of associative odor memory formation. Previously we described the anatomy of the adult MB and defined 20 types of dopaminergic neurons (DANs) that each innervate distinct MB compartments (Aso et al., 2014a, 2014b). Here we compare the properties of memories formed by optogenetic activation of individual DAN cell types. We found extensive differences in training requirements for memory formation, decay dynamics, storage capacity and flexibility to learn new associations. Even a single DAN cell type can either write or reduce an aversive memory, or write an appetitive memory, depending on when it is activated relative to odor delivery. Our results show that different learning rules are executed in seemingly parallel memory systems, providing multiple distinct circuit-based strategies to predict future events from past experiences. DOI: http://dx.doi.org/10.7554/eLife.16135.001

Subfields: Cellular and Molecular Neuroscience, Endocrine and Autonomic Systems, Plant Science, Neuroscience

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. Raphael Cohn
2. Ianessa Morantte
3. V. Ruta
4. Andrew C. Lin
5. Qian Li
6. Yoshinori Aso
7. Yi Zhong
8. Hoger Amin

In Endocrine and Autonomic Systems

1. Andrew C. Lin
2. Yi Zhong
3. Yoshinori Aso
4. S. Waddell
5. Pedro F. Jacob

In Plant Science

1. Glenn C. Turner
2. Yi Zhong

In Neuroscience

1. Liyuan Wang
2. Andrew C. Lin
3. Hoger Amin
4. Glenn C. Turner
5. Jun Zhu
6. Qian Li
7. Yi Zhong
8. Hang Su

Citations in the corpus

• A Comprehensive Survey of Continual Learning: Theory, Method and Application (2023, background): “, a memory center in fruit fly) coordinating multiple parallel compartments to process the sequentially-arrived experiences [23], [24], [78], [310], [421], corresponding to the use of modular networks in continual learning [15], [353], [430].”
• Incorporating neuro-inspired adaptability for continual learning in artificial intelligence (2023, background): “As for the five compartments of the γ MB system, the modulated forgetting rates have been shown to be important for coping with conflicting memories in succession [26, 38–41].”
• Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila (2022, background): “Therefore, the same basic mechanisms, odor- induced α2 receptor dynamics, seem to express two opposed plastic outcomes in the context of associative and non- associative memories and contribute to different learning rules across MB compartments (Hige et al., 2015; Aso and Rubin, 2016).”
• Dopamine activity in projection neurons regulates short‐lasting olfactory approach memory in Drosophila (2022, background): “In addition, recent studies have shown that different DA signalling is involved in relief memory and safety memory in flies (Aso & Rubin, 2016; Handler et al., 2019; Jacob & Waddell, 2020; Konig et al., 2018).”
• A connectome of a learning and memory center in the adult Drosophila brain (2017, methodology): “…aversive/appetitive food stimulus (Das et al., 2014), or by simultaneous optogenetic activation of a composite set of DANs covering both appetitive and aversive compart- ments (Aso and Rubin, 2016) results in a compound memory that is initially aversive and later transi- tions to appetitive.”
• A genetically-encoded fluorescent sensor enables rapid and specific detection of dopamine in flies, fish, and mice (2018, background): “It is reported that different types of DANs innervate different compartments of MBs, and these different dopaminergic pathways may play distinct roles in appetitive and aversive olfactory-dependent behaviors (Aso and Rubin, 2016; Cognigni et al., 2017).”
• Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning (2019, background): “A learned olfactory association can be weakened if an animal encounters the odor in the absence of the anticipated reinforcement or the reinforcement in the absence of the conditioned odor, violating the expected contingency between these cues (Aso and Rubin, 2016; Berry et al., 2012; Bouton, 2002; ”
• 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).”
• Neuronal mechanisms underlying innate and learned olfactory processing in Drosophila. (2019, background): “Many DANs respond 206 specifically to punishment (electric shock) or reward (sugar) [63], and blocking DANs 207 prevents memory formation [64-66], while artificial activation of DANs alone during odor 208 stimulus is sufficient to induce memory formation [67-73] (see Table 1).”