Sleep facilitates memory by blocking dopamine neuron mediated forgetting

By Jacob A. Berry, Isaac Cervantes-Sandoval, M. Chakraborty, Ronald L. Davis. 2015

216 citations recorded by the source corpus.

SUMMARY Early studies from psychology suggest that sleep facilitates memory retention by stopping ongoing retroactive interference caused by mental activity or external sensory stimuli. Neuroscience research with animal models, on the other hand, suggests that sleep facilitates retention by enhancing memory consolidation. Recently in Drosophila, the ongoing activity of specific dopamine neurons was shown to regulate the forgetting of olfactory memories. Here we show this ongoing dopaminergic activity is modulated with behavioral state, increasing robustly with locomotor activity and decreasing with rest. Increasing sleep-drive, with either the sleep-promoting agent Gaboxadol or by genetic stimulation of the neural circuit for sleep, decreases ongoing dopaminergic activity, while enhancing memory retention. Conversely, increasing arousal stimulates ongoing dopaminergic activity and accelerates dopaminergic based forgetting. Therefore, forgetting is regulated by the behavioral state modulation of dopaminergic-based plasticity. Our findings integrate psychological and neuroscience research on sleep and forgetting.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Endocrine and Autonomic Systems

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Citations in the corpus

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).”
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).”
A connectome of a learning and memory center in the adult Drosophila brain (2017, unknown): “DOI: 10.7554/eLife.26975 31 of 43 dependent changes in DAN activity have indeed been observed with calcium imaging (Cohn et al., 2015; Musso et al., 2015; Berry et al., 2015; Perisse et al., 2016; Krashes et al., 2009).”
Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning (2019, background): “Similar patterns of DAN activity are also elicited by a fly’s locomotion (Berry et al., 2015; Cohn et al., 2015), raising the possibility that, in the context of an odor plume, an animal’s behavior may serve as a reinforcement stimulus that itself drives bidirectional synaptic plasticity to regulate”
The Persistence and Transience of Memory. (2017, background): “…work has provided evidence that this pathway is modulated by dopamine (via dopamine receptor activation and the scaffolding protein Scribble), and thus provides a link between different behavioral states (e.g., sleep) and transience (Berry et al., 2012, 2015; Cervantes-Sandoval et al., 2016).”
A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection (2020, methodology): “First, PFN phase shifts should enable coordinate transformations, such as converting the allocentric head direction representation into an allocentric body direction representation (Figure 69D) (Andersen and Cui, 2009; Andersen et al., 1993; Batista, 2002; Bicanski and Burgess, 2020).”
The Drosophila Mushroom Body: From Architecture to Algorithm in a Learning Circuit. (2020, background): “Another important factor is of course DAN activity, which is often very different across compartments (see, for example, Berry et al. 2012, Mao & Davis 2009, Yamagata et al. 2016).”
The Biology of Forgetting – A Perspective (2017, background): “Internal States and External Factors that Stimulate or Inhibit Forgetting Cells Some and perhaps all of the neural circuits that promote forgetting are regulated by external factors and internal states, including activity, stress, and sleep (Shuai et al., 2011b; Berry et al., 2015).”
Propagation of homeostatic sleep signals by segregated synaptic microcircuits of the Drosophila mushroom body (2015, unknown): “Previous studies using broadly expressed traditional GAL4 drivers have implicated the MB in the control of sleep [3, 4, 6, 8–12], but due to lack of appropriate cell-specific drivers, were unable to resolve specific sleep-regulating MB cell types, although very recent studies have specifically impli”