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Membrane Potential-Dependent Modulation of Recurrent Inhibition in Rat Neocortex
Dynamic balance of excitation and inhibition is crucial for network stability and cortical processing, but it is unclear how this balance is achieved at different membrane potentials (V (m)) of cortical neurons, as found during persistent activity or slow V (m) oscillation. Here we report that a V (...
Autores principales: | , , , , |
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Formato: | Texto |
Lenguaje: | English |
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Public Library of Science
2011
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3062529/ https://www.ncbi.nlm.nih.gov/pubmed/21445327 http://dx.doi.org/10.1371/journal.pbio.1001032 |
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author | Zhu, Jie Jiang, Man Yang, Mingpo Hou, Han Shu, Yousheng |
author_facet | Zhu, Jie Jiang, Man Yang, Mingpo Hou, Han Shu, Yousheng |
author_sort | Zhu, Jie |
collection | PubMed |
description | Dynamic balance of excitation and inhibition is crucial for network stability and cortical processing, but it is unclear how this balance is achieved at different membrane potentials (V (m)) of cortical neurons, as found during persistent activity or slow V (m) oscillation. Here we report that a V (m)-dependent modulation of recurrent inhibition between pyramidal cells (PCs) contributes to the excitation-inhibition balance. Whole-cell recording from paired layer-5 PCs in rat somatosensory cortical slices revealed that both the slow and the fast disynaptic IPSPs, presumably mediated by low-threshold spiking and fast spiking interneurons, respectively, were modulated by changes in presynaptic V (m). Somatic depolarization (>5 mV) of the presynaptic PC substantially increased the amplitude and shortened the onset latency of the slow disynaptic IPSPs in neighboring PCs, leading to a narrowed time window for EPSP integration. A similar increase in the amplitude of the fast disynaptic IPSPs in response to presynaptic depolarization was also observed. Further paired recording from PCs and interneurons revealed that PC depolarization increases EPSP amplitude and thus elevates interneuronal firing and inhibition of neighboring PCs, a reflection of the analog mode of excitatory synaptic transmission between PCs and interneurons. Together, these results revealed an immediate V (m)-dependent modulation of cortical inhibition, a key strategy through which the cortex dynamically maintains the balance of excitation and inhibition at different states of cortical activity. |
format | Text |
id | pubmed-3062529 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2011 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-30625292011-03-28 Membrane Potential-Dependent Modulation of Recurrent Inhibition in Rat Neocortex Zhu, Jie Jiang, Man Yang, Mingpo Hou, Han Shu, Yousheng PLoS Biol Research Article Dynamic balance of excitation and inhibition is crucial for network stability and cortical processing, but it is unclear how this balance is achieved at different membrane potentials (V (m)) of cortical neurons, as found during persistent activity or slow V (m) oscillation. Here we report that a V (m)-dependent modulation of recurrent inhibition between pyramidal cells (PCs) contributes to the excitation-inhibition balance. Whole-cell recording from paired layer-5 PCs in rat somatosensory cortical slices revealed that both the slow and the fast disynaptic IPSPs, presumably mediated by low-threshold spiking and fast spiking interneurons, respectively, were modulated by changes in presynaptic V (m). Somatic depolarization (>5 mV) of the presynaptic PC substantially increased the amplitude and shortened the onset latency of the slow disynaptic IPSPs in neighboring PCs, leading to a narrowed time window for EPSP integration. A similar increase in the amplitude of the fast disynaptic IPSPs in response to presynaptic depolarization was also observed. Further paired recording from PCs and interneurons revealed that PC depolarization increases EPSP amplitude and thus elevates interneuronal firing and inhibition of neighboring PCs, a reflection of the analog mode of excitatory synaptic transmission between PCs and interneurons. Together, these results revealed an immediate V (m)-dependent modulation of cortical inhibition, a key strategy through which the cortex dynamically maintains the balance of excitation and inhibition at different states of cortical activity. Public Library of Science 2011-03-22 /pmc/articles/PMC3062529/ /pubmed/21445327 http://dx.doi.org/10.1371/journal.pbio.1001032 Text en Zhu et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Zhu, Jie Jiang, Man Yang, Mingpo Hou, Han Shu, Yousheng Membrane Potential-Dependent Modulation of Recurrent Inhibition in Rat Neocortex |
title | Membrane Potential-Dependent Modulation of Recurrent Inhibition in Rat Neocortex |
title_full | Membrane Potential-Dependent Modulation of Recurrent Inhibition in Rat Neocortex |
title_fullStr | Membrane Potential-Dependent Modulation of Recurrent Inhibition in Rat Neocortex |
title_full_unstemmed | Membrane Potential-Dependent Modulation of Recurrent Inhibition in Rat Neocortex |
title_short | Membrane Potential-Dependent Modulation of Recurrent Inhibition in Rat Neocortex |
title_sort | membrane potential-dependent modulation of recurrent inhibition in rat neocortex |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3062529/ https://www.ncbi.nlm.nih.gov/pubmed/21445327 http://dx.doi.org/10.1371/journal.pbio.1001032 |
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