Homeostasis in C. elegans sleep is characterized by two behaviorally and genetically distinct mechanisms

  1. Stanislav Nagy
  2. Nora Tramm
  3. Jarred Sanders
  4. Shachar Iwanir
  5. Ian A Shirley
  6. Erel Levine
  7. David Biron  Is a corresponding author
  1. University of Chicago, United States
  2. Harvard University, United States

Abstract

Biological homeostasis invokes modulatory responses aimed at stabilizing internal conditions. Using tunable photo- and mechano-stimulation, we identified two distinct categories of homeostatic responses during the sleep-like state of C. elegans (lethargus). In the presence of weak or no stimuli, extended motion caused a subsequent extension of quiescence. The neuropeptide Y receptor homolog, NPR-1, and an inhibitory neuropeptide known to activate it, FLP-18, were required for this process. In the presence of strong stimuli, the correlations between motion and quiescence were disrupted for several minutes but homeostasis manifested as an overall elevation of the time spent in quiescence. This response to strong stimuli required the function of the DAF-16/FOXO transcription factor in neurons, but not that of NPR-1. Conversely, response to weak stimuli did not require the function of DAF-16/FOXO. These findings suggest that routine homeostatic stabilization of sleep may be distinct from homeostatic compensation following a strong disturbance.

Article and author information

Author details

  1. Stanislav Nagy

    Institute for Biophysical Dynamics, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Nora Tramm

    Department of Physics, James Franck Institute, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jarred Sanders

    Committee on Genetics, Genomics, and Systems Biology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Shachar Iwanir

    Department of Physics, James Franck Institute, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ian A Shirley

    Department of Physics, James Franck Institute, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Erel Levine

    Department of Physics, Harvard University, cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. David Biron

    Institute for Biophysical Dynamics, University of Chicago, Chicago, United States
    For correspondence
    david.biron@gmail.com
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2014, Nagy 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

  • 3,783
    views
  • 407
    downloads
  • 57
    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. Stanislav Nagy
  2. Nora Tramm
  3. Jarred Sanders
  4. Shachar Iwanir
  5. Ian A Shirley
  6. Erel Levine
  7. David Biron
(2014)
Homeostasis in C. elegans sleep is characterized by two behaviorally and genetically distinct mechanisms
eLife 3:e04380.
https://doi.org/10.7554/eLife.04380

Share this article

https://doi.org/10.7554/eLife.04380

Further reading

    1. Neuroscience
    David C Williams, Amanda Chu ... Michael A McDannald
    Research Advance

    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.

    1. Neuroscience
    Agnieszka Glica, Katarzyna Wasilewska ... Katarzyna Jednoróg
    Research Article

    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.