By: Eli Muller
The biological mechanisms that allow the brain to balance flexibility and integration remain poorly understood. A potential solution to this mystery may lie in a unique aspect of neurobiology, which is that numerous brain systems contain diffuse synaptic connectivity. In this manuscript, 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 sub-regions. We then demonstrate that 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 key feature of the human brain is its ability to adapt to a diverse range of tasks and environmental stimuli. In order to facilitate this level of flexibility, the brain has been shown to strike a balance between network-level segregation and integration [1]. How it is able to shift between these operational modes, and what physical mechanisms underpin the presence of these states, remains an open question.
A potential solution to this mystery may lie in a unique aspect of neurobiology, which is that numerous brain systems contain both targeted and diffuse synaptic connections.
A network of biophysically-plausible corticothalamic neural masses is formed that produces realistic eyes-closed power spectrum with characteristic alpha-band activity.
Two levels of network connectivity are introduced: local nearest neighbor, and diffuse one-to-all coupling. Neural mass models incorporate realistic anatomy of neural populations, nonlinear neural responses, interpopulation connections; and dendritic, synaptic, cell-body, and axonal dynamics.

Spatial heterogeneities extend a critical point into a region of state space called a Griffiths phase, where quasi-critical states can be realized by multiple parameter combinations. Much like how water can undergo evaporation at temperatures below boiling due to above average kinetic energy in subsets of the system, the brain might exploit a similar physical niche by using diffuse subcortical input to the cortex (analogous to temperature) as a mechanism to support quasi-critical states within sub-regions of the system.

Quasi-critical states are defined by a distribution of integrated and segregated regions, and these maximize the diversity of stimulus response time-scales in addition to increased memory duration.

Within the quasi-critical zone, the network is both integrated and low dimensional, and has highly variable functional connectivity. 𝜅 shows coincidence across figures.
Summary:
- Spatial heterogeneities extend the critical point into a quasi-critical region of state space which can be realized by multiple parameter combinations.
- Diffuse coupling facilitates quasi-critical states, where sub-regions are locally critical.
- These quasi-critical states support a broadened dynamic repertoire, reduced dimensionality, and mix of integration and segregation.