Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons.

In the neocortex, the coexistence of temporally locked excitation and inhibition governs complex network activity underlying cognitive functions, and is believed to be altered in several brain diseases. Here we show that this equilibrium can be unlocked by increased activity of layer 5 pyramidal neu...

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Main Authors: Joana Lourenço, Simone Pacioni, Nelson Rebola, Geeske M van Woerden, Silvia Marinelli, David DiGregorio, Alberto Bacci
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-07-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC4086817?pdf=render
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spelling doaj-b3400b542c2648bbbbc88579bb81b56b2021-07-02T10:55:56ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852014-07-01127e100190310.1371/journal.pbio.1001903Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons.Joana LourençoSimone PacioniNelson RebolaGeeske M van WoerdenSilvia MarinelliDavid DiGregorioAlberto BacciIn the neocortex, the coexistence of temporally locked excitation and inhibition governs complex network activity underlying cognitive functions, and is believed to be altered in several brain diseases. Here we show that this equilibrium can be unlocked by increased activity of layer 5 pyramidal neurons of the mouse neocortex. Somatic depolarization or short bursts of action potentials of layer 5 pyramidal neurons induced a selective long-term potentiation of GABAergic synapses (LTPi) without affecting glutamatergic inputs. Remarkably, LTPi was selective for perisomatic inhibition from parvalbumin basket cells, leaving dendritic inhibition intact. It relied on retrograde signaling of nitric oxide, which persistently altered presynaptic GABA release and diffused to inhibitory synapses impinging on adjacent pyramidal neurons. LTPi reduced the time window of synaptic summation and increased the temporal precision of spike generation. Thus, increases in single cortical pyramidal neuron activity can induce an interneuron-selective GABAergic plasticity effectively altering the computation of temporally coded information.http://europepmc.org/articles/PMC4086817?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Joana Lourenço
Simone Pacioni
Nelson Rebola
Geeske M van Woerden
Silvia Marinelli
David DiGregorio
Alberto Bacci
spellingShingle Joana Lourenço
Simone Pacioni
Nelson Rebola
Geeske M van Woerden
Silvia Marinelli
David DiGregorio
Alberto Bacci
Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons.
PLoS Biology
author_facet Joana Lourenço
Simone Pacioni
Nelson Rebola
Geeske M van Woerden
Silvia Marinelli
David DiGregorio
Alberto Bacci
author_sort Joana Lourenço
title Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons.
title_short Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons.
title_full Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons.
title_fullStr Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons.
title_full_unstemmed Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons.
title_sort non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2014-07-01
description In the neocortex, the coexistence of temporally locked excitation and inhibition governs complex network activity underlying cognitive functions, and is believed to be altered in several brain diseases. Here we show that this equilibrium can be unlocked by increased activity of layer 5 pyramidal neurons of the mouse neocortex. Somatic depolarization or short bursts of action potentials of layer 5 pyramidal neurons induced a selective long-term potentiation of GABAergic synapses (LTPi) without affecting glutamatergic inputs. Remarkably, LTPi was selective for perisomatic inhibition from parvalbumin basket cells, leaving dendritic inhibition intact. It relied on retrograde signaling of nitric oxide, which persistently altered presynaptic GABA release and diffused to inhibitory synapses impinging on adjacent pyramidal neurons. LTPi reduced the time window of synaptic summation and increased the temporal precision of spike generation. Thus, increases in single cortical pyramidal neuron activity can induce an interneuron-selective GABAergic plasticity effectively altering the computation of temporally coded information.
url http://europepmc.org/articles/PMC4086817?pdf=render
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