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Development and physiology of GABAergic feedback excitation in parvalbumin expressing interneurons of the mouse basolateral amygdala

We have previously shown that in the basolateral amygdala (BLA), action potentials in one type of parvalbumin (PV)‐expressing GABAergic interneuron can evoke a disynaptic feedback excitatory postsynaptic potential (fbEPSP) onto the same presynaptic interneuron. Here, using whole‐cell recordings from...

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Autores principales: Spampanato, Jay, Sullivan, Robert K. P., Perumal, Madhusoothanan B., Sah, Pankaj
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4760394/
https://www.ncbi.nlm.nih.gov/pubmed/26733246
http://dx.doi.org/10.14814/phy2.12664
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author Spampanato, Jay
Sullivan, Robert K. P.
Perumal, Madhusoothanan B.
Sah, Pankaj
author_facet Spampanato, Jay
Sullivan, Robert K. P.
Perumal, Madhusoothanan B.
Sah, Pankaj
author_sort Spampanato, Jay
collection PubMed
description We have previously shown that in the basolateral amygdala (BLA), action potentials in one type of parvalbumin (PV)‐expressing GABAergic interneuron can evoke a disynaptic feedback excitatory postsynaptic potential (fbEPSP) onto the same presynaptic interneuron. Here, using whole‐cell recordings from PV‐expressing interneurons in acute brain slices we expand on this finding to show that this response is first detectable at 2‐week postnatal, and is most prevalent in animals beyond 3 weeks of age (>P21). This circuit has a very high fidelity, and single action potential evoked fbEPSPs display few failures. Reconstruction of filled neurons, and electron microscopy show that interneurons that receive feedback excitation make symmetrical synapses on both the axon initial segments (AIS), as well as the soma and proximal dendrites of local pyramidal neurons, suggesting fbEPSP interneurons are morphologically distinct from the highly specialized chandelier neurons that selectively target the axon initial segment of pyramidal neurons. Single PV interneurons could trigger very large (~ 1 nA) feedback excitatory postsynaptic currents (fbEPSCs) suggesting that these neurons are heavily reciprocally connected to local glutamatergic principal cells. We conclude that in the BLA, a subpopulation of PV interneurons forms a distinct neural circuit in which a single action potential can recruit multiple pyramidal neurons to discharge near simultaneously and feed back onto the presynaptic interneuron.
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spelling pubmed-47603942016-02-22 Development and physiology of GABAergic feedback excitation in parvalbumin expressing interneurons of the mouse basolateral amygdala Spampanato, Jay Sullivan, Robert K. P. Perumal, Madhusoothanan B. Sah, Pankaj Physiol Rep Original Research We have previously shown that in the basolateral amygdala (BLA), action potentials in one type of parvalbumin (PV)‐expressing GABAergic interneuron can evoke a disynaptic feedback excitatory postsynaptic potential (fbEPSP) onto the same presynaptic interneuron. Here, using whole‐cell recordings from PV‐expressing interneurons in acute brain slices we expand on this finding to show that this response is first detectable at 2‐week postnatal, and is most prevalent in animals beyond 3 weeks of age (>P21). This circuit has a very high fidelity, and single action potential evoked fbEPSPs display few failures. Reconstruction of filled neurons, and electron microscopy show that interneurons that receive feedback excitation make symmetrical synapses on both the axon initial segments (AIS), as well as the soma and proximal dendrites of local pyramidal neurons, suggesting fbEPSP interneurons are morphologically distinct from the highly specialized chandelier neurons that selectively target the axon initial segment of pyramidal neurons. Single PV interneurons could trigger very large (~ 1 nA) feedback excitatory postsynaptic currents (fbEPSCs) suggesting that these neurons are heavily reciprocally connected to local glutamatergic principal cells. We conclude that in the BLA, a subpopulation of PV interneurons forms a distinct neural circuit in which a single action potential can recruit multiple pyramidal neurons to discharge near simultaneously and feed back onto the presynaptic interneuron. John Wiley and Sons Inc. 2016-01-05 /pmc/articles/PMC4760394/ /pubmed/26733246 http://dx.doi.org/10.14814/phy2.12664 Text en © 2016 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Spampanato, Jay
Sullivan, Robert K. P.
Perumal, Madhusoothanan B.
Sah, Pankaj
Development and physiology of GABAergic feedback excitation in parvalbumin expressing interneurons of the mouse basolateral amygdala
title Development and physiology of GABAergic feedback excitation in parvalbumin expressing interneurons of the mouse basolateral amygdala
title_full Development and physiology of GABAergic feedback excitation in parvalbumin expressing interneurons of the mouse basolateral amygdala
title_fullStr Development and physiology of GABAergic feedback excitation in parvalbumin expressing interneurons of the mouse basolateral amygdala
title_full_unstemmed Development and physiology of GABAergic feedback excitation in parvalbumin expressing interneurons of the mouse basolateral amygdala
title_short Development and physiology of GABAergic feedback excitation in parvalbumin expressing interneurons of the mouse basolateral amygdala
title_sort development and physiology of gabaergic feedback excitation in parvalbumin expressing interneurons of the mouse basolateral amygdala
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4760394/
https://www.ncbi.nlm.nih.gov/pubmed/26733246
http://dx.doi.org/10.14814/phy2.12664
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