Cited by 76Neurobiology and Insect Physiology ResearchSleep and Wakefulness ResearchMemory and Neural Mechanisms

Availability of food determines the need for sleep in memory consolidation

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Chouhan, Nitin S., Griffith, Leslie C., Haynes, Paula, Sehgal, Amita·2021·Nature

Abstract

Sleep remains a major mystery of biology, with little understood about its basic function. One of the most commonly proposed functions of sleep is the consolidation of memory1–3. However, as conditions such as starvation require the organism to be awake and active4, the ability to switch to a memory consolidation mechanism that is not contingent on sleep may confer an evolutionary advantage. Here we identify an adaptive circuit-based mechanism that enables Drosophila to form sleep-dependent and sleep-independent memory. Flies fed after appetitive conditioning needed increased sleep for memory consolidation, but flies starved after training did not require sleep to form memories. Memory in fed flies is mediated by the anterior–posterior α′/β′ neurons of the mushroom body, while memory under starvation is mediated by medial α′/β′ neurons. Sleep-dependent and sleep-independent memory rely on distinct dopaminergic neurons and corresponding mushroom body output neurons. However, sleep and memory are coupled such that mushroom body neurons required for sleep-dependent memory also promote sleep. Flies lacking Neuropeptide F display sleep-dependent memory even when starved, suggesting that circuit selection is determined by hunger. This plasticity in memory circuits enables flies to retain essential information in changing environments. Hunger status in a fly is shown to drive either sleep-dependent or sleep-independent memory formation through different mushroom body circuits.

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Crossref · 10.1038/s41586-020-2997-y

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  • Recent experiments have failed to reveal superior retrieval for post-encoding sleep compared with wake, and a few suggest enhanced forgetting by sleep.

    “recently, there has been a growing number of experiments failing to reveal superior retrieval of memory for post-encoding sleep compared with wake conditions, and a few studies even suggesting enhanced forgetting of memory by sleep.6,7”

    From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [7]

    The paper’s results report no effect of post-training sleep deprivation on long-term memory in starved flies, supporting a condition-specific lack of sleep benefit. They also report impaired memory after sleep deprivation in fed flies. The cited paper does not report a growing number of such experiments or suggest that sleep enhances forgetting; the only forgetting-related passage found is a reference title. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Unlike sleep consolidation, wake consolidation strongly depends on internal organismic states such as hunger.

    “Beyond pointing to distinct mechanisms mediating wake and sleep-dependent consolidation processes, the findings show that unlike sleep consolidation, wake consolidation strongly depends on internal organismic states such as hunger.”

    From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [7]

    The Abstract reports that hunger-related NPF signaling helps select the sleep-independent memory pathway in starved flies, supporting the point about wake consolidation. But the Abstract and Discussion describe a feeding/hunger-dependent switch between both pathways; they do not support the contrast that sleep-dependent consolidation is unlike wake consolidation in this respect. The study concerns appetitive memory in Drosophila. (LLM, conf=0.86)

    Experimental — accuracy not yet measured
  • Sleep was required for forming a long-term food-odor conditioning memory only in fed animals, and these animals displayed increased sleep after conditioning.

    “Sleep was required for forming a long-term food-odor conditioning memory only in the fed animals, and these animals indeed also displayed increased sleep after conditioning.”

    From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [7]

  • Sleep and wake-associated consolidation has been dissociated in Drosophila.

    “Against the backdrop that the mammalian hippocampus shows some homologies with the insect mushroom bodies in structure and function, 283 it is interesting that sleep and wake-associated consolidation has been also dissociated in Drosophila.”

    From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [7]

  • Sleep-independent memory formation in starved flies depended on the hunger signal neuropeptide F.

    “Sleep-independent memory formation in starved flies depended on the hunger signal neuropeptide F.”

    From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [7]

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Authors
Chouhan, N. S., Griffith, L. C., Haynes, P., & Sehgal, A.
Affiliations
  • Howard Hughes Medical Institute (US)
  • Brandeis University (US)
Corresponding author
Sehgal, Amita
Venue
Nature
Published
2020-12-02
Volume
589
Issue
7843
Pages
582-585
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W3108457971
Cited by
76
References
32
Citations by year
2026: 7 · 2025: 11 · 2024: 13 · 2023: 18 · 2022: 16 · 2021: 9 · 2020: 2
FWCI
5.16
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
Funders
  • National Institute of Mental Health (T32MH019929, T32MH014654, R01MH067284)
  • National Institute of Diabetes and Digestive and Kidney Diseases (R01DK120757)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
sleep-dependent memory consolidation, starvation, hunger, Drosophila, mushroom body, dopaminergic neurons, neuropeptide F, sleep regulation, appetitive conditioning
MeSH terms
Memory Consolidation, Animals, Appetitive Behavior, Drosophila melanogaster, Feeding Behavior, Female, Food, Hunger, Male, Neuronal Plasticity, Neurons, Neuropeptides, Sleep, Starvation, Wakefulness, Mushroom Bodies, Dopaminergic Neurons

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