Predominantly linear summation of metabotropic postsynaptic potentials follows coactivation of neurogliaform interneurons
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.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files.
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Data from: Predominantly linear summation of metabotropic postsynaptic potentials follows coactivation of neurogliaform interneuronsDryad Digital Repository, doi:10.5061/dryad.qv9s4mwf4.
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Predominantly linear summation of metabotropic postsynaptic potentials follows coactivation of neurogliaform interneuronshttps://creativecommons.org/publicdomain/zero/1.0/.
Article and author information
Author details
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.
Reviewing Editor
- Marco Capogna, University of Aarhus, Denmark
Ethics
Animal experimentation: Experiments were conducted to the guidelines of University of Szeged Animal Care and Use Committee (ref. no. XX/897/2018).
Version history
- Received: December 10, 2020
- Preprint posted: December 11, 2020 (view preprint)
- Accepted: July 14, 2021
- Accepted Manuscript published: July 26, 2021 (version 1)
- 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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