RESEARCH ARTICLE
An inhibitory gate for state transition in cortex Stefano Zucca1,2†, Giulia D’Urso1,2†, Valentina Pasquale3, Dania Vecchia1,2, Giuseppe Pica2,4, Serena Bovetti1,2, Claudio Moretti1,2, Stefano Varani1,2, Manuel Molano-Mazo´n2,4, Michela Chiappalone3, Stefano Panzeri1,2,4, Tommaso Fellin1,2* 1
Optical Approaches to Brain Function Laboratory, Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; 2Neural Coding Laboratory, Istituto Italiano di Tecnologia, Genova and Rovereto, Italy; 3 Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova, Italy; 4Neural Computation Laboratory, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, Italy
Abstract Large scale transitions between active (up) and silent (down) states during quiet
*For correspondence: tommaso.
[email protected] †
These authors contributed equally to this work
Competing interests: The authors declare that no competing interests exist.
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. DOI: 10.7554/eLife.26177.001
Funding: See page 27 Received: 21 February 2017 Accepted: 15 May 2017 Published: 16 May 2017 Reviewing editor: John Huguenard, Stanford University School of Medicine, United States Copyright Zucca et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Introduction The mammalian brain generates internal activities independent of environmental stimuli (Destexhe, 2011). For example, during quiet wakefulness or NREM sleep the cortex and other brain regions (e.g., the thalamus) display rhythmic electrical signals characterized by large-amplitude and low frequency (
