Whole-brain network topology, the ascending arousal system, and information processing dynamics

Li M, Han Y, Aburn MJ, Breakspear M, Poldrack RA, Shine JM, et al. (2019) Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain. PLoS Comput Biol 15(10): e1006957. https://doi.org/10.1371/journal.pcbi.1006957

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.

Author summary

Higher brain function relies on a dynamic balance between functional integration and segregation. Previous work has shown that this balance is mediated in part by alterations in neural gain, which are thought to relate to projections from ascending neuromodulatory nuclei, such as the locus coeruleus. Here, we extend this work by demonstrating that the modulation of neural gain parameters alters the information processing dynamics of the brain regions of a biophysical neural model. Specifically, we find that subcritical dynamics in the phase space of neural gain parameters are characterized by high Active Information Storage, whereas supercritical dynamics in this phase space are associated with an increase in inter-regional Transfer Entropy. Our results suggest that the modulation of neural gain via the ascending arousal system may fundamentally alter the information processing mode of the brain, which in turn has important implications for understanding the biophysical basis of cognition.

Note that the locus coeruleus is part of the reticular activating system (RAS), which suggests that these results are relevant to Warren McCulloch's concept of behavioral mode, which was about the role of the RAS in modulating activity of the whole brain.