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Predominantly linear summation of metabotropic postsynaptic potentials follows coactivation of neurogliaform interneurons

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Cite this article as: eLife 2021;10:e65634 doi: 10.7554/eLife.65634

Abstract

Summation of ionotropic receptor-mediated responses is critical in neuronal computation by shaping input-output characteristics of neurons. However, arithmetics of summation for metabotropic signals are not known. We characterized the combined ionotropic and metabotropic output of neocortical neurogliaform cells (NGFCs) using electrophysiological and anatomical methods in the rat cerebral cortex. These experiments revealed that GABA receptors are activated outside release sites and confirmed coactivation of putative NGFCs in superficial cortical layers in vivo. Triple recordings from presynaptic NGFCs converging to a postsynaptic neuron revealed sublinear summation of ionotropic GABAA responses and linear summation of metabotropic GABAB responses. Based on a model combining properties of volume transmission and distributions of all NGFC axon terminals, we predict that in 83% of cases one or two NGFCs can provide input to a point in the neuropil. We suggest that interactions of metabotropic GABAergic responses remain linear even if most superficial layer interneurons specialized to recruit GABAB receptors are simultaneously active.

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All data generated or analysed during this study are included in the manuscript and supporting files.

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Author details

  1. Attila Ozsvár

    MTA-SZTE Research Group for Cortical Microcircuits, University of Szeged, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  2. Gergely Komlósi

    MTA-SZTE Research Group for Cortical Microcircuits, University of Szeged, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  3. Gáspár Oláh

    MTA-SZTE Research Group for Cortical Microcircuits, University of Szeged, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  4. Judith Baka

    MTA-SZTE Research Group for Cortical Microcircuits, Department of Physiology, Anatomy and Neuroscience, University of Szeged, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  5. Gábor Molnár

    MTA-SZTE Research Group for Cortical Microcircuits, Department of Physiology, Anatomy and Neuroscience, University of Szeged, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  6. Gábor Tamás

    MTA-SZTE Research Group for Cortical Microcircuits, Department of Physiology, Anatomy and Neuroscience, University of Szeged, Szeged, Hungary
    For correspondence
    gtamas@bio.u-szeged.hu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7905-6001

Funding

European Research Council (INTERIMPACT)

  • Gábor Tamás

ELKH-SZTE Research Network (ELKH-SZTE Research Group for Cortical Microcircuits)

  • Gábor Tamás

Hungarian National Office for Research and Technology (GINOP 2.3.2-15-2016-00018)

  • Gábor Tamás

Hungarian National Office for Research and Technology (Élvonal KKP 133807)

  • Gábor Tamás

National Research, Development and Innovation Office (OTKA K128863)

  • Gábor Molnár
  • Gábor Tamás

New National Excellence Program of the Ministry for Innovation and Technology (ÚNKP-20-5 - SZTE-681)

  • Gábor Tamás

Hungarian Academy of Sciences (János Bolyai Research Scholarship)

  • Gábor Molnár

Ministry for Innovation and Technology (New National Excellence Program)

  • Gábor Molnár

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

Ethics

Animal experimentation: Experiments were conducted to the guidelines of University of Szeged Animal Care and Use Committee (ref. no. XX/897/2018).

Reviewing Editor

  1. Marco Capogna, University of Aarhus, Denmark

Publication history

  1. Received: December 10, 2020
  2. Preprint posted: December 11, 2020 (view preprint)
  3. Accepted: July 14, 2021
  4. Accepted Manuscript published: July 26, 2021 (version 1)
  5. Version of Record published: August 12, 2021 (version 2)

Copyright

© 2021, Ozsvár 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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