An inhibitory gate for state transition in cortex

Large scale transitions between active (up) and silent (down) states during quiet wakefulness or NREM sleep regulate fundamental cortical functions and are known to involve both excitatory and inhibitory cells. However, if and how inhibition regulates these activity transitions is unclear. Using flu...

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Main Authors: Stefano Zucca, Giulia D’Urso, Valentina Pasquale, Dania Vecchia, Giuseppe Pica, Serena Bovetti, Claudio Moretti, Stefano Varani, Manuel Molano-Mazón, Michela Chiappalone, Stefano Panzeri, Tommaso Fellin
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/26177
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author Stefano Zucca
Giulia D’Urso
Valentina Pasquale
Dania Vecchia
Giuseppe Pica
Serena Bovetti
Claudio Moretti
Stefano Varani
Manuel Molano-Mazón
Michela Chiappalone
Stefano Panzeri
Tommaso Fellin
spellingShingle Stefano Zucca
Giulia D’Urso
Valentina Pasquale
Dania Vecchia
Giuseppe Pica
Serena Bovetti
Claudio Moretti
Stefano Varani
Manuel Molano-Mazón
Michela Chiappalone
Stefano Panzeri
Tommaso Fellin
An inhibitory gate for state transition in cortex
eLife
Neocortex
parvalbumin positive interneuron
somatostatin positive interneuron
up and down states
author_facet Stefano Zucca
Giulia D’Urso
Valentina Pasquale
Dania Vecchia
Giuseppe Pica
Serena Bovetti
Claudio Moretti
Stefano Varani
Manuel Molano-Mazón
Michela Chiappalone
Stefano Panzeri
Tommaso Fellin
author_sort Stefano Zucca
title An inhibitory gate for state transition in cortex
title_short An inhibitory gate for state transition in cortex
title_full An inhibitory gate for state transition in cortex
title_fullStr An inhibitory gate for state transition in cortex
title_full_unstemmed An inhibitory gate for state transition in cortex
title_sort inhibitory gate for state transition in cortex
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2017-05-01
description Large scale transitions between active (up) and silent (down) states during quiet wakefulness or NREM sleep regulate fundamental cortical functions and are known to involve both excitatory and inhibitory cells. However, if and how inhibition regulates these activity transitions is unclear. Using fluorescence-targeted electrophysiological recording and cell-specific optogenetic manipulation in both anesthetized and non-anesthetized mice, we found that two major classes of interneurons, the parvalbumin and the somatostatin positive cells, tightly control both up-to-down and down-to-up state transitions. Inhibitory regulation of state transition was observed under both natural and optogenetically-evoked conditions. Moreover, perturbative optogenetic experiments revealed that the inhibitory control of state transition was interneuron-type specific. Finally, local manipulation of small ensembles of interneurons affected cortical populations millimetres away from the modulated region. Together, these results demonstrate that inhibition potently gates transitions between cortical activity states, and reveal the cellular mechanisms by which local inhibitory microcircuits regulate state transitions at the mesoscale.
topic Neocortex
parvalbumin positive interneuron
somatostatin positive interneuron
up and down states
url https://elifesciences.org/articles/26177
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spelling doaj-c206d9bde67749daa7e688274ac6cec52021-05-05T13:28:48ZengeLife Sciences Publications LtdeLife2050-084X2017-05-01610.7554/eLife.26177An inhibitory gate for state transition in cortexStefano Zucca0Giulia D’Urso1Valentina Pasquale2https://orcid.org/0000-0002-4499-9536Dania Vecchia3Giuseppe Pica4Serena Bovetti5Claudio Moretti6Stefano Varani7Manuel Molano-Mazón8Michela Chiappalone9Stefano Panzeri10https://orcid.org/0000-0003-1700-8909Tommaso Fellin11https://orcid.org/0000-0003-2718-7533Optical Approaches to Brain Function Laboratory, Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; Neural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, ItalyOptical Approaches to Brain Function Laboratory, Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; Neural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, ItalyDepartment of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, ItalyOptical Approaches to Brain Function Laboratory, Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; Neural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, ItalyNeural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, Italy; Neural Computation Laboratory, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, ItalyOptical Approaches to Brain Function Laboratory, Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; Neural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, ItalyOptical Approaches to Brain Function Laboratory, Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; Neural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, ItalyOptical Approaches to Brain Function Laboratory, Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; Neural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, ItalyNeural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, Italy; Neural Computation Laboratory, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, ItalyDepartment of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, ItalyOptical Approaches to Brain Function Laboratory, Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; Neural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, Italy; Neural Computation Laboratory, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, ItalyOptical Approaches to Brain Function Laboratory, Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; Neural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, ItalyLarge scale transitions between active (up) and silent (down) states during quiet wakefulness or NREM sleep regulate fundamental cortical functions and are known to involve both excitatory and inhibitory cells. However, if and how inhibition regulates these activity transitions is unclear. Using fluorescence-targeted electrophysiological recording and cell-specific optogenetic manipulation in both anesthetized and non-anesthetized mice, we found that two major classes of interneurons, the parvalbumin and the somatostatin positive cells, tightly control both up-to-down and down-to-up state transitions. Inhibitory regulation of state transition was observed under both natural and optogenetically-evoked conditions. Moreover, perturbative optogenetic experiments revealed that the inhibitory control of state transition was interneuron-type specific. Finally, local manipulation of small ensembles of interneurons affected cortical populations millimetres away from the modulated region. Together, these results demonstrate that inhibition potently gates transitions between cortical activity states, and reveal the cellular mechanisms by which local inhibitory microcircuits regulate state transitions at the mesoscale.https://elifesciences.org/articles/26177Neocortexparvalbumin positive interneuronsomatostatin positive interneuronup and down states