1. Neuroscience
Download icon

Feeding state functionally reconfigures a sensory circuit to drive thermosensory behavioral plasticity

  1. Asuka Takeishi
  2. Jihye Yeon
  3. Nathan Harris
  4. Wenxing Yang
  5. Piali Sengupta  Is a corresponding author
  1. RIKEN, Japan
  2. Brandeis University, United States
  3. West China School of Basic Medical Sciences and Forensic Medicine, China
Short Report
  • Cited 1
  • Views 1,489
  • Annotations
Cite this article as: eLife 2020;9:e61167 doi: 10.7554/eLife.61167

Abstract

Internal state alters sensory behaviors to optimize survival strategies. The neuronal mechanisms underlying hunger-dependent behavioral plasticity are not fully characterized. Here we show that feeding state alters C. elegans thermotaxis behavior by engaging a modulatory circuit whose activity gates the output of the core thermotaxis network. Feeding state does not alter the activity of the core thermotaxis circuit comprised of AFD thermosensory and AIY interneurons. Instead, prolonged food deprivation potentiates temperature responses in the AWC sensory neurons, which inhibit the postsynaptic AIA interneurons to override and disrupt AFD-driven thermotaxis behavior. Acute inhibition and activation of AWC and AIA, respectively, restores negative thermotaxis in starved animals. We find that state-dependent modulation of AWC-AIA temperature responses requires INS-1 insulin-like peptide signaling from the gut and DAF-16 FOXO function in AWC. Our results describe a mechanism by which functional reconfiguration of a sensory network via gut-brain signaling drives state-dependent behavioral flexibility.

Article and author information

Author details

  1. Asuka Takeishi

    Center for Brain Science, RIKEN, Wako, Japan
    Competing interests
    No competing interests declared.
  2. Jihye Yeon

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
  3. Nathan Harris

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
  4. Wenxing Yang

    Physiology, West China School of Basic Medical Sciences and Forensic Medicine, Chengdu, China
    Competing interests
    No competing interests declared.
  5. Piali Sengupta

    Department of Biology, Brandeis University, Waltham, United States
    For correspondence
    sengupta@brandeis.edu
    Competing interests
    Piali Sengupta, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7468-0035

Funding

National Institute of General Medical Sciences (R35 GM122463)

  • Piali Sengupta

National Institute of Neurological Disorders and Stroke (T32 NS007292)

  • Nathan Harris

National Institute of Neurological Disorders and Stroke (F32 NS112453)

  • Nathan Harris

RIKEN (H28-1058)

  • Asuka Takeishi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Publication history

  1. Received: July 16, 2020
  2. Accepted: October 18, 2020
  3. Accepted Manuscript published: October 19, 2020 (version 1)
  4. Version of Record published: November 5, 2020 (version 2)

Copyright

© 2020, Takeishi 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

  • 1,489
    Page views
  • 260
    Downloads
  • 1
    Citations

Article citation count generated by polling the highest count across the following sources: PubMed Central, Crossref, Scopus.

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)

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

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

Further reading

    1. Neuroscience
    Laura E Maglio et al.
    Research Article Updated

    Insulin-like growth factor-1 (IGF-1) plays a key role in synaptic plasticity, spatial learning, and anxiety-like behavioral processes. While IGF-1 regulates neuronal firing and synaptic transmission in many areas of the central nervous system, its signaling and consequences on excitability, synaptic plasticity, and animal behavior dependent on the prefrontal cortex remain unexplored. Here, we show that IGF-1 induces a long-lasting depression of the medium and slow post-spike afterhyperpolarization (mAHP and sAHP), increasing the excitability of layer 5 pyramidal neurons of the rat infralimbic cortex. Besides, IGF-1 mediates a presynaptic long-term depression of both inhibitory and excitatory synaptic transmission in these neurons. The net effect of this IGF-1-mediated synaptic plasticity is a long-term potentiation of the postsynaptic potentials. Moreover, we demonstrate that IGF-1 favors the fear extinction memory. These results show novel functional consequences of IGF-1 signaling, revealing IGF-1 as a key element in the control of the fear extinction memory.

    1. Computational and Systems Biology
    2. Neuroscience
    Brian Q Geuther et al.
    Research Article Updated

    Automated detection of complex animal behaviors remains a challenging problem in neuroscience, particularly for behaviors that consist of disparate sequential motions. Grooming is a prototypical stereotyped behavior that is often used as an endophenotype in psychiatric genetics. Here, we used mouse grooming behavior as an example and developed a general purpose neural network architecture capable of dynamic action detection at human observer-level performance and operating across dozens of mouse strains with high visual diversity. We provide insights into the amount of human annotated training data that are needed to achieve such performance. We surveyed grooming behavior in the open field in 2457 mice across 62 strains, determined its heritable components, conducted GWAS to outline its genetic architecture, and performed PheWAS to link human psychiatric traits through shared underlying genetics. Our general machine learning solution that automatically classifies complex behaviors in large datasets will facilitate systematic studies of behavioral mechanisms.