Dopamine Is Required for Learning and Forgetting in Drosophila

By Jacob A. Berry, Isaac Cervantes-Sandoval, Eric Nicholas, Ronald L. Davis. 2012

271 citations recorded by the source corpus.

SUMMARY Psychological studies in humans and behavioral studies of model organisms suggest that forgetting is a common and biologically regulated process, but the molecular, cellular, and circuit mechanisms underlying forgetting are poorly understood. Here we show that the bidirectional modulation of a small subset of dopamine neurons (DANs) after olfactory learning regulates the rate of forgetting of both punishing (aversive) and rewarding (appetitive) memories. Two of these DANs, MP1 and MV1, exhibit synchronized ongoing activity in the mushroom body neuropil in alive and awake flies before and after learning, as revealed by functional cellular imaging. Furthermore, while the mushroom-body-expressed dDA1 dopamine receptor is essential for the acquisition of memory, we show that the dopamine receptor DAMB, also highly expressed in mushroom body neurons, is required for forgetting. We propose a dual role for dopamine: memory acquisition through dDA1 signaling and forgetting through DAMB signaling in the mushroom body neurons.

Subfields: Cell Biology, Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Neuroscience

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Citations in the corpus

Incorporating neuro-inspired adaptability for continual learning in artificial intelligence (2023, positive): “…for a single continual learner (SCL), we turn to investigate the organizing principles of the γMB system where new memory forms and active forgetting happens 19–22, 25 , 36, 38, In such a γMB-like architecture, the relationship between learners is critical to the performance of continual learning.”
Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “…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 et al., 2015).”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “Conversely, DopR2 strongly influences the topography of presynaptic Ca 2+ along KC axons, in accord with evidence that tonic release of dopamine during ongoing behavior acts through this receptor to interfere with the maintenance of specific learned olfactory associations (Berry et al., 2012, 2015).”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “It is also noteworthy that the effect of dopamine can be dependent on the activity status of Kenyon cells; activation of PPL1-γ1pedc together with odor presentation induces memory, while its activation without an odor has been reported to erase memory (Berry et al., 2012; Placais et al., 2012).”
System-like consolidation of olfactory memories in Drosophila (2013, background): “With time, consolidation reinforces the / memory trace, whereas STM/ITM traces in the / and MBNs decay, perhaps partly through dopamine-dependent forgetting mechanisms (Berry et al., 2012).”
Active Protection: Learning-Activated Raf/MAPK Activity Protects Labile Memory from Rac1-Independent Forgetting. (2018, unknown): “The recently proposed concept of active forgetting (Berry et al., 2012; Inoue et al., 2013; Liu et al., 2016b; Shuai et al., 2010; Zhang et al., 2016) describes an intrinsic mechanism that at least partially explains the inevitability: learning itself activates active forgetting to accelerate the…”
A genetically-encoded fluorescent sensor enables rapid and specific detection of dopamine in flies, fish, and mice (2018, unknown): “These results provide direct evidence of compartmentalized DA dynamics during sensory processing in the MB as postulated by indirect presynaptic Ca imaging of DAN (Berry et al., 2012; Cohn et al., 2015).”
Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning (2019, background): “In Drosophila, DopR1 and DopR2 have been proposed to play opposing roles in olfactory memory regulation at the behavioral level, with DopR1 essential to memory formation and DopR2 necessary for memory erosion (Berry et al., 2012; Kim et al., 2007; Qin et al., 2012).”
Cdc42-Dependent Forgetting Regulates Repetition Effect in Prolonging Memory Retention. (2016, methodology): “Studies have increasingly focused on the biological 818 Cell Reports 16, 817–825, July 19, 2016 basis of active forgetting using different animal models (Akers et al., 2014; Berry et al., 2012, 2015; Hadziselimovic et al., 2014; Inoue et al., 2013; Shuai et al., 2010, 2015).”
Pain-relief learning in flies, rats, and man: basic research and applied perspectives (2014, background): “behavior (e.g., Krashes et al. 2009; Berry et al. 2012; Placais et al. 2012; Perisse et al. 2013; see also Burke et al. 2012); for these aspects too, the roles of dopamine and octopamine apparently”