A sleep state in Drosophila larvae required for neural stem cell proliferation
Abstract
Sleep during development is involved in refining brain circuitry, but a role for sleep in the earliest periods of nervous system elaboration, when neurons are first being born, has not been explored. Here we identify a sleep state in Drosophila larvae that coincides with a major wave of neurogenesis. Mechanisms controlling larval sleep are partially distinct from adult sleep: octopamine, the Drosophila analog of mammalian norepinephrine, is the major arousal neuromodulator in larvae, but dopamine is not required. Using real-time behavioral monitoring in a closed-loop sleep deprivation system, we find that sleep loss in larvae impairs cell division of neural progenitors. This work establishes a system uniquely suited for studying sleep during nascent periods, and demonstrates that sleep in early life regulates neural stem cell proliferation.
Article and author information
Author details
Funding
National Institutes of Health (K08NS090461)
- Matthew S Kayser
Burroughs Wellcome Fund
- Matthew S Kayser
Alfred P. Sloan Foundation
- Matthew S Kayser
March of Dimes Foundation
- Matthew S Kayser
National Institutes of Health (R01NS088432)
- David M Raizen
National Institutes of Health (R01NS084835)
- Christopher Fang-Yen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2018, Szuperak 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
-
- 6,304
- views
-
- 756
- downloads
-
- 39
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Neuroscience
The neural noise hypothesis of dyslexia posits an imbalance between excitatory and inhibitory (E/I) brain activity as an underlying mechanism of reading difficulties. This study provides the first direct test of this hypothesis using both electroencephalography (EEG) power spectrum measures in 120 Polish adolescents and young adults (60 with dyslexia, 60 controls) and glutamate (Glu) and gamma-aminobutyric acid (GABA) concentrations from magnetic resonance spectroscopy (MRS) at 7T MRI scanner in half of the sample. Our results, supported by Bayesian statistics, show no evidence of E/I balance differences between groups, challenging the hypothesis that cortical hyperexcitability underlies dyslexia. These findings suggest that alternative mechanisms must be explored and highlight the need for further research into the E/I balance and its role in neurodevelopmental disorders.
-
- Neuroscience
Recognizing and responding to threat cues is essential to survival. Freezing is a predominant threat behavior in rats. We have recently shown that a threat cue can organize diverse behaviors beyond freezing, including locomotion (Chu et al., 2024). However, that experimental design was complex, required many sessions, and had rats receive many foot shock presentations. Moreover, the findings were descriptive. Here, we gave female and male Long Evans rats cue light illumination paired or unpaired with foot shock (8 total) in a conditioned suppression setting, using a range of shock intensities (0.15, 0.25, 0.35, or 0.50 mA). We found that conditioned suppression was only observed at higher foot shock intensities (0.35 mA and 0.50 mA). We constructed comprehensive temporal ethograms by scoring 22,272 frames across 12 behavior categories in 200-ms intervals around cue light illumination. The 0.50 mA and 0.35 mA shock-paired visual cues suppressed reward seeking, rearing, and scaling, as well as light-directed rearing and light-directed scaling. The shock-paired visual cue further elicited locomotion and freezing. Linear discriminant analyses showed that ethogram data could accurately classify rats into paired and unpaired groups. Using complete ethogram data produced superior classification compared to behavior subsets, including an Immobility subset featuring freezing. The results demonstrate diverse threat behaviors – in a short and simple procedure – containing sufficient information to distinguish the visual fear conditioning status of individual rats.