UP-DOWN cortical dynamics reflect state transitions in a bistable network
Abstract
In the idling brain, neuronal circuits transition between periods of sustained firing (UP state) and quiescence (DOWN state), a pattern the mechanisms of which remain unclear. Here we analyzed spontaneous cortical population activity from anesthetized rats and found that UP and DOWN durations were highly variable and that population rates showed no significant decay during UP periods. We built a network rate model with excitatory (E) and inhibitory (I) populations exhibiting a novel bistable regime between a quiescent and an inhibition-stabilized state of arbitrarily low rate. Fluctuations triggered state transitions, while adaptation in E cells paradoxically caused a marginal decay of E-rate but a marked decay of I-rate in UP periods, a prediction that we validated experimentally. A spiking network implementation further predicted that DOWN-to-UP transitions must be caused by synchronous high-amplitude events. Our findings provide evidence of bistable cortical network that exhibits non-rhythmic state transitions when the brain rests.
Article and author information
Author details
Funding
AGAUR of the Generalitat de Catalunya (SGR14-1265)
- Albert Compte
Spanish Ministry of Economy and Competitiveness together with the European Regional Development Fund (BFU2009-09537,BFU2012-34838)
- Albert Compte
Spanish Ministry of Economy and Competitiveness together with the European Regional Development Fund (RYC-2011-08755)
- Alex Roxin
EU Biotrack contract (PCOFUND-GA-2008-229673)
- Alex Roxin
Hungarian Brain Research Program Grant (KTIA_NAP_13-2-2014-0016)
- Peter Barthó
Spanish Ministry of Economy and Competitiveness together with the European Regional Development Fund (SAF2010-15730,SAF2013-46717-R,RYC-2009-04829)
- Jaime de la Rocha
EU Marie Curie grants (PIRG07-GA-2010-268382)
- Jaime de la Rocha
Spanish Ministry of Economy and Competitiveness (SAF2015-70324R)
- Jaime de la Rocha
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Mark CW van Rossum, University of Edinburgh, United Kingdom
Ethics
Animal experimentation: This study involved analysis of previously published and new data. Previously published data (Bartho et al, J Neurophys. 2004, 92(1)) was obtained under a protocol approved by the Rutgers University Animal Care and Use Committee. One new data set was acquired in accordance with a protocol approved by the Animal Welfare Committee at University of Lethbridge (protocol # 0907). All surgeries were performed under anesthesia, and every effort was made to minimize suffering.
Version history
- Received: October 16, 2016
- Accepted: July 21, 2017
- Accepted Manuscript published: August 4, 2017 (version 1)
- Version of Record published: September 4, 2017 (version 2)
Copyright
© 2017, Jercog et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 6,116
- views
-
- 903
- downloads
-
- 87
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.
-
- Neuroscience
Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.