A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster

  1. Paula R Haynes
  2. Bethany L Christmann
  3. Leslie C Griffith  Is a corresponding author
  1. Brandeis University, United States

Abstract

Sleep promotes memory consolidation in humans and many other species, but the physiological and anatomical relationships between sleep and memory remain unclear. Here we show the dorsal paired medial (DPM) neurons, which are required for memory consolidation in Drosophila, are sleep-promoting inhibitory neurons. DPMs increase sleep via release of GABA onto wake-promoting mushroom body (MB) α'/β' neurons. Functional imaging demonstrates that DPM activation evokes robust increases in chloride in MB neurons, but is unable to cause detectable increases in calcium or cAMP. Downregulation of α'/β' GABAA and GABABR3 receptors results in sleep loss, suggesting these receptors are the sleep-relevant targets of DPM-mediated inhibition. Regulation of sleep by neurons necessary for consolidation suggests that these brain processes may be functionally interrelated via their shared anatomy. These findings have important implications for the mechanistic relationship between sleep and memory consolidation, arguing for a significant role of inhibitory neurotransmission in regulating these processes.These results argue for a significant role of inhibitory neurotransmission in memory consolidation and its regulation by sleep.

Article and author information

Author details

  1. Paula R Haynes

    Department of Biology, Volen Center for Complex Systems, National Center for Behavioral Genomics, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
  2. Bethany L Christmann

    Department of Biology, Volen Center for Complex Systems, National Center for Behavioral Genomics, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
  3. Leslie C Griffith

    Department of Biology, Volen Center for Complex Systems, National Center for Behavioral Genomics, Brandeis University, Waltham, United States
    For correspondence
    griffith@brandeis.edu
    Competing interests
    Leslie C Griffith, Reviewing editor, eLife.

Reviewing Editor

  1. Graeme W Davis, University of California, San Francisco, United States

Version history

  1. Received: July 3, 2014
  2. Accepted: January 7, 2015
  3. Accepted Manuscript published: January 7, 2015 (version 1)
  4. Version of Record published: January 26, 2015 (version 2)

Copyright

© 2015, Haynes et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 9,830
    views
  • 1,366
    downloads
  • 129
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Paula R Haynes
  2. Bethany L Christmann
  3. Leslie C Griffith
(2015)
A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster
eLife 4:e03868.
https://doi.org/10.7554/eLife.03868

Share this article

https://doi.org/10.7554/eLife.03868

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Kenneth Chiou, Noah Snyder-Mackler
    Insight

    Single-cell RNA sequencing reveals the extent to which marmosets carry genetically distinct cells from their siblings.

    1. Neuroscience
    Flavio J Schmidig, Simon Ruch, Katharina Henke
    Research Article

    We are unresponsive during slow-wave sleep but continue monitoring external events for survival. Our brain wakens us when danger is imminent. If events are non-threatening, our brain might store them for later consideration to improve decision-making. To test this hypothesis, we examined whether novel vocabulary consisting of simultaneously played pseudowords and translation words are encoded/stored during sleep, and which neural-electrical events facilitate encoding/storage. An algorithm for brain-state-dependent stimulation selectively targeted word pairs to slow-wave peaks or troughs. Retrieval tests were given 12 and 36 hr later. These tests required decisions regarding the semantic category of previously sleep-played pseudowords. The sleep-played vocabulary influenced awake decision-making 36 hr later, if targeted to troughs. The words’ linguistic processing raised neural complexity. The words’ semantic-associative encoding was supported by increased theta power during the ensuing peak. Fast-spindle power ramped up during a second peak likely aiding consolidation. Hence, new vocabulary played during slow-wave sleep was stored and influenced decision-making days later.