Early-life experience reorganizes neuromodulatory regulation of stage-specific behavioral responses and individuality dimensions during development

  1. Reemy Ali Nasser
  2. Yuval Harel
  3. Shay Stern  Is a corresponding author
  1. Technion - Israel Institute of Technology, Israel

Abstract

Early-life experiences may promote stereotyped behavioral alterations that are dynamic across development time, but also behavioral responses that are variable among individuals, even when initially exposed to the same stimulus. Here, by utilizing longitudinal monitoring of C. elegans individuals throughout development we show that behavioral effects of early-life starvation are exposed during early and late developmental stages and buffered during intermediate stages of development. We further found that both dopamine and serotonin shape the discontinuous behavioral responses by opposite and temporally segregated functions across development time. While dopamine buffers behavioral responses during intermediate developmental stages, serotonin promotes behavioral sensitivity to stress during early and late stages. Interestingly, unsupervised analysis of individual biases across development uncovered multiple individuality dimensions that coexist within stressed and unstressed populations and further identified experience-dependent effects on variation within specific individuality dimensions. These results provide insight into the complex temporal regulation of behavioral plasticity across developmental timescales, structuring shared and unique individual responses to early-life experiences.

Data availability

Behavioral datasets have been deposited in Mendeleyhttps://data.mendeley.com/datasets/kxrcmtyfr6/draft?a=4f4e420b-5d9b-42e6-890a-16e6332ffe0ahttps://data.mendeley.com/datasets/fgsyppvpnc/draft?a=bc4739f1-7311-4019-99e0-ec3bfb51e8f6Code of individuality analysis was deposited inhttps://github.com/yha/ElegansIndividuality

Article and author information

Author details

  1. Reemy Ali Nasser

    Faculty of Biology, Technion - Israel Institute of Technology, Haifa, Israel
    Competing interests
    The authors declare that no competing interests exist.
  2. Yuval Harel

    Faculty of Biology, Technion - Israel Institute of Technology, Haifa, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Shay Stern

    Faculty of Biology, Technion - Israel Institute of Technology, Technion, Israel
    For correspondence
    sstern@technion.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9576-7938

Funding

HORIZON EUROPE European Research Council (ERC-2019-STG)

  • Shay Stern

Israel Science Foundation (3035/20)

  • Shay Stern

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

Reviewing Editor

  1. Douglas Portman, University of Rochester, United States

Version history

  1. Received: October 19, 2022
  2. Preprint posted: October 25, 2022 (view preprint)
  3. Accepted: May 16, 2023
  4. Accepted Manuscript published: May 17, 2023 (version 1)
  5. Version of Record published: June 1, 2023 (version 2)

Copyright

© 2023, Ali Nasser 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.

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  1. Reemy Ali Nasser
  2. Yuval Harel
  3. Shay Stern
(2023)
Early-life experience reorganizes neuromodulatory regulation of stage-specific behavioral responses and individuality dimensions during development
eLife 12:e84312.
https://doi.org/10.7554/eLife.84312

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https://doi.org/10.7554/eLife.84312

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