Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain

PLoS Comput Biol. 2019 Oct 15;15(10):e1006957. doi: 10.1371/journal.pcbi.1006957. eCollection 2019 Oct.

Abstract

A key component of the flexibility and complexity of the brain is its ability to dynamically adapt its functional network structure between integrated and segregated brain states depending on the demands of different cognitive tasks. Integrated states are prevalent when performing tasks of high complexity, such as maintaining items in working memory, consistent with models of a global workspace architecture. Recent work has suggested that the balance between integration and segregation is under the control of ascending neuromodulatory systems, such as the noradrenergic system, via changes in neural gain (in terms of the amplification and non-linearity in stimulus-response transfer function of brain regions). In a previous large-scale nonlinear oscillator model of neuronal network dynamics, we showed that manipulating neural gain parameters led to a 'critical' transition in phase synchrony that was associated with a shift from segregated to integrated topology, thus confirming our original prediction. In this study, we advance these results by demonstrating that the gain-mediated phase transition is characterized by a shift in the underlying dynamics of neural information processing. Specifically, the dynamics of the subcritical (segregated) regime are dominated by information storage, whereas the supercritical (integrated) regime is associated with increased information transfer (measured via transfer entropy). Operating near to the critical regime with respect to modulating neural gain parameters would thus appear to provide computational advantages, offering flexibility in the information processing that can be performed with only subtle changes in gain control. Our results thus link studies of whole-brain network topology and the ascending arousal system with information processing dynamics, and suggest that the constraints imposed by the ascending arousal system constrain low-dimensional modes of information processing within the brain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain / physiology*
  • Brain Mapping / methods*
  • Cognition / physiology
  • Computer Simulation
  • Humans
  • Magnetic Resonance Imaging / methods
  • Memory, Short-Term / physiology
  • Mental Processes / physiology*
  • Models, Neurological
  • Nerve Net / physiology
  • Neural Pathways / physiology
  • Neurons / physiology
  • Nonlinear Dynamics

Grants and funding

MJA was supported through a Queensland Government Advance Queensland Innovation Partnership grant AQIP12316-17RD2 - https://advance.qld.gov.au/investors-universities-and-researchers/innovation-partnerships. JL was supported through the Australian Research Council DECRA grant DE160100630 - https://www.arc.gov.au/grants/discovery-program/discovery-early-career-researcher-award-decra. JMS was supported through a University of Sydney Robinson Fellowship and NHMRC Project Grant 1156536 - https://nhmrc.gov.au/funding/find-funding/project-grants. JMS and JL were supported through The University of Sydney Research Accelerator (SOAR) Fellowship program - https://sydney.edu.au/research/our-researchers/sydney-research-accelerator-fellows.html. High performance computing facilities provided by QIMR Berghofer Medical Research Institute and The University of Sydney (artemis) have contributed to the research results reported within this paper. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.