Learning steers the ontogeny of an efficient hunting sequence in zebrafish larvae

  1. Konstantinos Lagogiannis  Is a corresponding author
  2. Giovanni Diana
  3. Martin P Meyer  Is a corresponding author
  1. King's College London, United Kingdom

Abstract

Goal-directed behaviours may be poorly coordinated in young animals but, with age and experience, behaviour progressively adapts to efficiently exploit the animal's ecological niche. How experience impinges on the developing neural circuits of behaviour is an open question. We have conducted a detailed study of the effects of experience on the ontogeny of hunting behaviour in larval zebrafish. We report that larvae with prior experience of live prey consume considerably more prey than naive larvae. This is mainly due to increased capture success and a modest increase in hunt rate. We demonstrate that the initial turn to prey and the final capture manoeuvre of the hunting sequence were jointly modified by experience and that modification of these components predicted capture success. Our findings establish an ethologically relevant paradigm in zebrafish for studying how the brain is shaped by experience to drive the ontogeny of efficient behaviour.

Data availability

All data analyzed during this study are included in the supporting github repository.

Article and author information

Author details

  1. Konstantinos Lagogiannis

    Developmental Neurobiology, King's College London, London, United Kingdom
    For correspondence
    costaslag@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9349-801X
  2. Giovanni Diana

    Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7497-5271
  3. Martin P Meyer

    Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom
    For correspondence
    martin.meyer@kcl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8337-630X

Funding

Wellcome (204788/Z/16/Z)

  • Konstantinos Lagogiannis
  • Giovanni Diana
  • Martin P Meyer

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

Ethics

Animal experimentation: This work was approved by the local Animal Care and Use Committee (King's College London) and was performed in accordance with the Animals (Scientific Procedures) Act, 1986, under license from the United Kingdom Home Office Licence number P9090AEFD. All primary data included in the manuscript came from the use of zebrafish larvae. All procedures were non-invasive and classified as mild according to the Animals Act 1986 and as defined by the United Kingdom Home Office, in order to minimize animal suffering. At the end of regulated procedures, animals were culled using a schedule 1 method (terminal dose of MS222).

Copyright

© 2020, Lagogiannis 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

  • 1,711
    views
  • 189
    downloads
  • 12
    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. Konstantinos Lagogiannis
  2. Giovanni Diana
  3. Martin P Meyer
(2020)
Learning steers the ontogeny of an efficient hunting sequence in zebrafish larvae
eLife 9:e55119.
https://doi.org/10.7554/eLife.55119

Share this article

https://doi.org/10.7554/eLife.55119

Further reading

    1. Developmental Biology
    2. Neuroscience
    Agnik Dasgupta, Caleb C Reagor ... AJ Hudspeth
    Research Article

    In a developing nervous system, axonal arbors often undergo complex rearrangements before neural circuits attain their final innervation topology. In the lateral line sensory system of the zebrafish, developing sensory axons reorganize their terminal arborization patterns to establish precise neural microcircuits around the mechanosensory hair cells. However, a quantitative understanding of the changes in the sensory arbor morphology and the regulators behind the microcircuit assembly remain enigmatic. Here, we report that Semaphorin7A (Sema7A) acts as an important mediator of these processes. Utilizing a semi-automated three-dimensional neurite tracing methodology and computational techniques, we have identified and quantitatively analyzed distinct topological features that shape the network in wild-type and Sema7A loss-of-function mutants. In contrast to those of wild-type animals, the sensory axons in Sema7A mutants display aberrant arborizations with disorganized network topology and diminished contacts to hair cells. Moreover, ectopic expression of a secreted form of Sema7A by non-hair cells induces chemotropic guidance of sensory axons. Our findings propose that Sema7A likely functions both as a juxtracrine and as a secreted cue to pattern neural circuitry during sensory organ development.

    1. Chromosomes and Gene Expression
    2. Developmental Biology
    Roger Huerlimann, Natacha Roux ... Timothy Ravasi
    Research Article

    Most teleost fishes exhibit a biphasic life history with a larval oceanic phase that is transformed into morphologically and physiologically different demersal, benthic, or pelagic juveniles. This process of transformation is characterized by a myriad of hormone-induced changes, during the often abrupt transition between larval and juvenile phases called metamorphosis. Thyroid hormones (TH) are known to be instrumental in triggering and coordinating this transformation but other hormonal systems such as corticoids, might be also involved as it is the case in amphibians. In order to investigate the potential involvement of these two hormonal pathways in marine fish post-embryonic development, we used the Malabar grouper (Epinephelus malabaricus) as a model system. We assembled a chromosome-scale genome sequence and conducted a transcriptomic analysis of nine larval developmental stages. We studied the expression patterns of genes involved in TH and corticoid pathways, as well as four biological processes known to be regulated by TH in other teleost species: ossification, pigmentation, visual perception, and metabolism. Surprisingly, we observed an activation of many of the same pathways involved in metamorphosis also at an early stage of the larval development, suggesting an additional implication of these pathways in the formation of early larval features. Overall, our data brings new evidence to the controversial interplay between corticoids and thyroid hormones during metamorphosis as well as, surprisingly, during the early larval development. Further experiments will be needed to investigate the precise role of both pathways during these two distinct periods and whether an early activation of both corticoid and TH pathways occurs in other teleost species.