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

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.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data for all behavioral and imaging data have been provided in Excel spreadsheets with data for individual figure panels in separate tabs. Two spreadsheets are provided for main and supplementary figures

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.

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

  • 3,381
    views
  • 539
    downloads
  • 37
    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. Asuka Takeishi
  2. Jihye Yeon
  3. Nathan Harris
  4. Wenxing Yang
  5. Piali Sengupta
(2020)
Feeding state functionally reconfigures a sensory circuit to drive thermosensory behavioral plasticity
eLife 9:e61167.
https://doi.org/10.7554/eLife.61167

Share this article

https://doi.org/10.7554/eLife.61167

Further reading

    1. Neuroscience
    Nicolas Langer, Maurice Weber ... Ce Zhang
    Tools and Resources

    Memory deficits are a hallmark of many different neurological and psychiatric conditions. The Rey–Osterrieth complex figure (ROCF) is the state-of-the-art assessment tool for neuropsychologists across the globe to assess the degree of non-verbal visual memory deterioration. To obtain a score, a trained clinician inspects a patient’s ROCF drawing and quantifies deviations from the original figure. This manual procedure is time-consuming, slow and scores vary depending on the clinician’s experience, motivation, and tiredness. Here, we leverage novel deep learning architectures to automatize the rating of memory deficits. For this, we collected more than 20k hand-drawn ROCF drawings from patients with various neurological and psychiatric disorders as well as healthy participants. Unbiased ground truth ROCF scores were obtained from crowdsourced human intelligence. This dataset was used to train and evaluate a multihead convolutional neural network. The model performs highly unbiased as it yielded predictions very close to the ground truth and the error was similarly distributed around zero. The neural network outperforms both online raters and clinicians. The scoring system can reliably identify and accurately score individual figure elements in previously unseen ROCF drawings, which facilitates explainability of the AI-scoring system. To ensure generalizability and clinical utility, the model performance was successfully replicated in a large independent prospective validation study that was pre-registered prior to data collection. Our AI-powered scoring system provides healthcare institutions worldwide with a digital tool to assess objectively, reliably, and time-efficiently the performance in the ROCF test from hand-drawn images.

    1. Neuroscience
    Masahiro Takigawa, Marta Huelin Gorriz ... Daniel Bendor
    Research Article

    During rest and sleep, memory traces replay in the brain. The dialogue between brain regions during replay is thought to stabilize labile memory traces for long-term storage. However, because replay is an internally-driven, spontaneous phenomenon, it does not have a ground truth - an external reference that can validate whether a memory has truly been replayed. Instead, replay detection is based on the similarity between the sequential neural activity comprising the replay event and the corresponding template of neural activity generated during active locomotion. If the statistical likelihood of observing such a match by chance is sufficiently low, the candidate replay event is inferred to be replaying that specific memory. However, without the ability to evaluate whether replay detection methods are successfully detecting true events and correctly rejecting non-events, the evaluation and comparison of different replay methods is challenging. To circumvent this problem, we present a new framework for evaluating replay, tested using hippocampal neural recordings from rats exploring two novel linear tracks. Using this two-track paradigm, our framework selects replay events based on their temporal fidelity (sequence-based detection), and evaluates the detection performance using each event's track discriminability, where sequenceless decoding across both tracks is used to quantify whether the track replaying is also the most likely track being reactivated.