Dopamine-based mechanism for transient forgetting

Sabandal, John Martin; Berry, Jacob A.; Davis, Ronald L.

doi:10.1038/s41586-020-03154-y

Cited by 44 publications

(36 citation statements)

References 33 publications

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“…A large number of studies reported a wide range of olfactory learning‒related changes in synaptic plasticity in the Drosophila MB (Akalal et al, 2010; Berry et al, 2018; Bilz et al, 2020; Boto et al, 2014; Boto et al, 2019; Bouzaiane et al, 2015; Cohn et al, 2015; Dylla et al, 2017; Felsenberg et al, 2017; Felsenberg et al, 2018; Gervasi et al, 2010; Handler et al, 2019; Hige et al, 2015; Louis et al, 2018; McCurdy et al, 2021; Owald et al, 2015; Perisse et al, 2016; Placais et al, 2013; Sabandal et al, 2021; Sejourne et al, 2011; Stahl et al, 2021; Wang et al, 2008; Yu et al, 2006; Yu et al, 2005; Zhang and Roman, 2013; Zhang et al, 2019b; Zhou et al, 2019). However, some studies differed with respect to the location (i.e., the specific MB compartment), direction (i.e., potentiation vs. depression) and whether the change occurs in presynaptic KCs or postsynaptic MBONs.…”

Section: Discussionmentioning

confidence: 99%

Local 5-HT signal bi-directionally regulates the coincidence time window of associative learning

Zeng

Zhangren

et al. 2022

Preprint

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Temporal coincidence between the conditioned stimulus (CS) and unconditioned stimulus (US) is essential for associative learning across species. Despite its ubiquitous presence, the mechanism that may regulate this time window duration remains unclear yet. Using olfactory associative learning in Drosophila as a model, we find that suppressing or promoting serotonin (5-HT) signal could respectively shorten or prolong the coincidence time window of odor-shock associative learning and synaptic plasticity in mushroom body (MB) Kenyon cells (KCs). Capitalizing on GPCR-activation based (GRAB) sensors for 5-HT and acetylcholine (ACh), we characterized the in vivo 5-HT dynamics in MB lobes during odor and shock stimulations and further dissected this microcircuit. Interestingly, local KC-released ACh activates nicotinic receptors on the dorsal paired medial (DPM) neuron, and in turn the DPM neuron releases 5-HT to inhibit the ACh signal via the 5-HT1a receptor. Finally, we demonstrated that the DPM-mediated serotonergic feedback circuit is sufficient and necessary to regulate the coincidence time window. This work provides a model for studying the temporal contingency of environmental events and their causal relationship

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Section: Discussionmentioning

confidence: 99%

Local 5-HT signal bi-directionally regulates the coincidence time window of associative learning

Zeng

Zhangren

et al. 2022

Preprint

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“…Endogenous signals relayed by upstream elements (i.e., recurrent loops or pacemaker neurons) may induce spontaneous DAN activity in the absence of identified environmental stimuli, providing homeostatic regulation of the memory circuit (Scaplen et al, 2021;Vaccaro et al, 2017). Alternatively, persistent PPL1 DAN activity may reflect spurious exogenous sensory input (i.e., unrelated to planned experiments), causing either proactive or retroactive interference (in a cognitive psychology context) that contributes to the erosion of memory (Postman and Underwood, 1973;Berry et al, 2015;Sabandal et al, 2021). As such, our observation…”

Section: Persistent Dan Activity In Ltm Formationmentioning

confidence: 99%

Neuropeptide F inhibits dopamine neuron interference of long-term memory consolidation in Drosophila

et al. 2021

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Long-term memory (LTM) formation requires consolidation processes to overcome interfering signals that erode memory formation. Olfactory memory in Drosophila involves convergent projection neuron (PN; odor) and dopaminergic neuron (DAN; reinforcement) input to the mushroom body (MB). How posttraining DAN activity in the posterior lateral protocerebrum (PPL1) continues to regulate memory consolidation remains unknown. Here we address this question using targeted transgenes in behavior and electrophysiology experiments to show that (1) persistent post-training activity of PPL1-a2a 0 2 and PPL1-a3 DANs interferes with aversive LTM formation; (2) neuropeptide F (NPF) signaling blocks this interference in PPL1-a2a 0 2 and PPL1-a3 DANs after spaced training to enable LTM formation; and (3) training-induced NPF release and neurotransmission from two upstream dorsal-anterior-lateral (DAL2) neurons are required to form LTM. Thus, NPF signals from DAL2 neurons to specific PPL1 DANs disinhibit the memory circuit, ensuring that periodic events are remembered as consolidated LTM.

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“…On the behavioral front, research over the past several decades has transformed the fruit fly into a key model organism for the study of associative learning and choice behavior [33][34][35] . A rich body of experiments has shown that flies can learn a variety of Pavlovian conditioning paradigms [36][37][38][39][40][41][42] and exhibit features common in vertebrate memory, such as forgetting, re-evaluation, and consolidation, amongst others [43][44][45][46][47][48][49][50] . However, most existing tasks rely on studying the place preference behavior of groups of flies.…”

Section: Introductionmentioning

confidence: 99%

Reward expectations direct learning and drive operant matching inDrosophila

Rajagopalan

Darshan

Fitzgerald

et al. 2022

Preprint

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Foraging animals must use decision-making strategies that dynamically account for uncertainty in the world. To cope with this uncertainty, animals have developed strikingly convergent strategies that use information about multiple past choices and reward to learn representations of the current state of the world. However, the underlying learning rules that drive the required learning have remained unclear. Here, working in the relatively simple nervous system of Drosophila, we combine behavioral measurements, mathematical modeling, and neural circuit perturbations to show that dynamic foraging depends on a learning rule incorporating reward expectation. Using a novel olfactory dynamic foraging task, we characterize the behavioral strategies used by individual flies when faced with unpredictable rewards and show, for the first time, that they perform operant matching. We build on past theoretical work and demonstrate that this strategy requires the existence of a covariance-based learning rule in the mushroom body - a hub for learning in the fly. In particular, the behavioral consequences of optogenetic perturbation experiments suggest that this learning rule incorporates reward expectation. Our results identify a key element of the algorithm underlying dynamic foraging in flies and suggest a comprehensive mechanism that could be fundamental to these behaviors across species.

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Dopamine-based mechanism for transient forgetting

Cited by 44 publications

References 33 publications

Local 5-HT signal bi-directionally regulates the coincidence time window of associative learning

Local 5-HT signal bi-directionally regulates the coincidence time window of associative learning

Neuropeptide F inhibits dopamine neuron interference of long-term memory consolidation in Drosophila

Reward expectations direct learning and drive operant matching inDrosophila

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