Diffuse neural coupling mediates complex network dynamics through the formation of quasi-critical brain states

• Published in: Nature communications Vol. 11; no. 1; p. 6337
• Main Authors: Müller, Eli J., Munn, Brandon R., Shine, James M.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 10.12.2020; Nature Publishing Group; Nature Portfolio
• Subjects: 631/378/116/2392; 631/378/116/2393; Anatomy; Arousal; Brain; Brain - physiology; Brain architecture; Coupling; Data processing; Dynamics; Humanities and Social Sciences; Humans; Information processing; Magnetic Resonance Imaging; Medical imaging; Models, Neurological; multidisciplinary; Nervous system; Neural networks; Neuroimaging; Neurosciences; Rest - physiology; Science; Science (multidisciplinary); Signatures; Task Performance and Analysis; Thalamus; Time Factors; Uniqueness
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-19716-7

The biological mechanisms that allow the brain to balance flexibility and integration remain poorly understood. A potential solution may lie in a unique aspect of neurobiology, which is that numerous brain systems contain diffuse synaptic connectivity. Here, we demonstrate that increasing diffuse cortical coupling within a validated biophysical corticothalamic model traverses the system through a quasi-critical regime in which spatial heterogeneities in input noise support transient critical dynamics in distributed subregions. The presence of quasi-critical states coincides with known signatures of complex, adaptive brain network dynamics. Finally, we demonstrate the presence of similar dynamic signatures in empirical whole-brain human neuroimaging data. Together, our results establish that modulating the balance between local and diffuse synaptic coupling in a thalamocortical model subtends the emergence of quasi-critical brain states that act to flexibly transition the brain between unique modes of information processing. A principle of neuroanatomy, namely diffuse connectivity, is modeled using a large-scale network of corticothalamic neural masses. We demonstrate that increases in diffuse coupling transition the system through a quasi-critical regime, which coincides with known signatures of complex adaptive brain dynamics, and model fits to human imaging data orient task states to higher levels of diffusivity, consistent with the influence of arousal systems.