Kainate-type of glutamate receptors regulate development of glutamatergic synaptic circuitry in the rodent amygdala

Abstract

Perturbed information processing in the amygdala has been implicated in developmentally originating neuropsychiatric disorders. However, little is known on the mechanisms that guide formation and refinement of intrinsic connections between amygdaloid nuclei. We demonstrate that in rodents the glutamatergic connection from basolateral to central amygdala (BLA-CeA) develops rapidly during the first ten postnatal days, before external inputs underlying amygdala dependent behaviors emerge. During this restricted period of synaptic development, kainate-type of ionotropic glutamate receptors (KARs) are highly expressed in the BLA and tonically activated to regulate glutamate release via a G-protein dependent mechanism. Genetic manipulation of this endogenous KAR activity locally in the newborn LA perturbed development of glutamatergic input to CeA, identifying KARs as a physiological mechanism regulating formation of the glutamatergic circuitry in the amygdala.

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All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all Figures.

Article and author information

Author details

  1. Maria Ryazantseva

    Research Programme in Molecular and Integrative Biosciences and Neuroscience Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  2. Jonas Englund

    Research Programme in Molecular and Integrative Biosciences and Neuroscience Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexandra Shintyapina

    Research Programme in Molecular and Integrative Biosciences and Neuroscience Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  4. Johanna Huupponen

    Research Programme in Molecular and Integrative Biosciences and Neuroscience Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  5. Vasilii Shteinikov

    Research Programme in Molecular and Integrative Biosciences and Neuroscience Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  6. Asla Pitkänen

    A I Virtanen Institute, Department of Neurobiology, University of Eastern Finland, Kuopio, Finland
    Competing interests
    The authors declare that no competing interests exist.
  7. Juha Partanen

    Department of Biosciences, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  8. Sari E Lauri

    Research Programme in Molecular and Integrative Biosciences and Neuroscience Center, University of Helsinki, Helsinki, Finland
    For correspondence
    sari.lauri@helsinki.fi
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5895-1357

Funding

Academy of Finland (SA 297211)

  • Sari E Lauri

Aatos Erkko Foundation

  • Sari E Lauri

Sigrid Juselius Foundation

  • Sari E Lauri

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

Ethics

Animal experimentation: All experiments were done in accordance with the guidelines given by the ethics committee for animal research at the University of Helsinki (license numbers ESAVI/6853/04.10.07/2017 and ESAVI/29384/2019).

Copyright

© 2020, Ryazantseva 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. Maria Ryazantseva
  2. Jonas Englund
  3. Alexandra Shintyapina
  4. Johanna Huupponen
  5. Vasilii Shteinikov
  6. Asla Pitkänen
  7. Juha Partanen
  8. Sari E Lauri
(2020)
Kainate-type of glutamate receptors regulate development of glutamatergic synaptic circuitry in the rodent amygdala
eLife 9:e52798.
https://doi.org/10.7554/eLife.52798

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https://doi.org/10.7554/eLife.52798