The modulation of neural gain facilitates a transition between functional segregation and integration in the brain

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Abstract

Cognitive function relies on a dynamic, context-sensitive balance between functional integration and segregation in the brain. Previous work has proposed that this balance is mediated by global fluctuations in neural gain by projections from ascending neuromodulatory nuclei. To test this hypothesis in silico, we studied the effects of neural gain on network dynamics in a model of large-scale neuronal dynamics. We found that increases in neural gain directed the network through an abrupt dynamical transition, leading to an integrated network topology that was maximal in frontoparietal ‘rich club’ regions. This gain-mediated transition was also associated with increased topological complexity, as well as increased variability in time-resolved topological structure, further highlighting the potential computational benefits of the gain-mediated network transition. These results support the hypothesis that neural gain modulation has the computational capacity to mediate the balance between integration and segregation in the brain.

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Impulses and Physiological States in Theoretical Models of Nerve Membrane

Richard Fitzhugh (1961)

Van der Pol's equation for a relaxation oscillator is generalized by the addition of terms to produce a pair of non-linear differential equations with either a stable singular point or a limit cycle. The resulting "BVP model" has two variables of state, representing excitability and refractoriness, and qualitatively resembles Bonhoeffer's theoretical model for the iron wire model of nerve. This BVP model serves as a simple representative of a class of excitable-oscillatory systems including the Hodgkin-Huxley (HH) model of the squid giant axon. The BVP phase plane can be divided into regions corresponding to the physiological states of nerve fiber (resting, active, refractory, enhanced, depressed, etc.) to form a "physiological state diagram," with the help of which many physiological phenomena can be summarized. A properly chosen projection from the 4-dimensional HH phase space onto a plane produces a similar diagram which shows the underlying relationship between the two models. Impulse trains occur in the BVP and HH models for a range of constant applied currents which make the singular point representing the resting state unstable.

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Structural and functional brain networks: from connections to cognition.

Hae-Jeong Park, Karl Friston (2013)

How rich functionality emerges from the invariant structural architecture of the brain remains a major mystery in neuroscience. Recent applications of network theory and theoretical neuroscience to large-scale brain networks have started to dissolve this mystery. Network analyses suggest that hierarchical modular brain networks are particularly suited to facilitate local (segregated) neuronal operations and the global integration of segregated functions. Although functional networks are constrained by structural connections, context-sensitive integration during cognition tasks necessarily entails a divergence between structural and functional networks. This degenerate (many-to-one) function-structure mapping is crucial for understanding the nature of brain networks. The emergence of dynamic functional networks from static structural connections calls for a formal (computational) approach to neuronal information processing that may resolve this dialectic between structure and function.

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The θ-γ neural code.

John Lisman, Ole Jensen (2013)

Theta and gamma frequency oscillations occur in the same brain regions and interact with each other, a process called cross-frequency coupling. Here, we review evidence for the following hypothesis: that the dual oscillations form a code for representing multiple items in an ordered way. This form of coding has been most clearly demonstrated in the hippocampus, where different spatial information is represented in different gamma subcycles of a theta cycle. Other experiments have tested the functional importance of oscillations and their coupling. These involve correlation of oscillatory properties with memory states, correlation with memory performance, and effects of disrupting oscillations on memory. Recent work suggests that this coding scheme coordinates communication between brain regions and is involved in sensory as well as memory processes. Copyright © 2013 Elsevier Inc. All rights reserved.

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Author and article information

Contributors

James M Shine:

ORCID: http://orcid.org/0000-0003-1762-5499

Russell A Poldrack:

ORCID: http://orcid.org/0000-0001-6755-0259

Gustavo Deco: Role: Reviewing Editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 29 January 2018

Publication date Collection: 2018

Volume: 7

Electronic Location Identifier: e31130

Affiliations

[1 ]deptDepartment of Psychology Stanford University StanfordUnited States

[2 ]deptCentral Clinical School The University of Sydney SydneyAustralia

[3 ]QIMR Berghofer Medical Research Institute BrisbaneAustralia

[4 ]Metro North Mental Health Service BrisbaneAustralia

[5]Universitat Pompeu Fabra Spain

[6]Universitat Pompeu Fabra Spain

Author information

James M Shine http://orcid.org/0000-0003-1762-5499

Russell A Poldrack http://orcid.org/0000-0001-6755-0259

Article

Publisher ID: 31130

DOI: 10.7554/eLife.31130

PMC ID: 5818252

PubMed ID: 29376825

SO-VID: 3e3aba32-c18d-4a69-b68e-8d94209a1dd4

License:

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.

History

Date received : 09 August 2017

Date accepted : 26 January 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;

Award ID: GNT1072403

Award Recipient : James M Shine

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Author impact statement The flexible network architecture of the brain is sensitive to the modulation of neural gain, which may be mediated by ascending arousal nuclei, such as the noradrenergic locus coeruleus.

ScienceOpen disciplines: Life sciences

Keywords: integration,neural gain,noradrenaline,biophysical model,excitability,bold,none

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: integration, neural gain, noradrenaline, biophysical model, excitability, bold, none

The modulation of neural gain facilitates a transition between functional segregation and integration in the brain

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BIO Integration

Most cited references 46

Impulses and Physiological States in Theoretical Models of Nerve Membrane

Structural and functional brain networks: from connections to cognition.

The θ-γ neural code.

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