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

Abstract

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.

Consciousness is supported by near-critical slow cortical electrodynamics

“…And such critical behavior is known to have important computational benefits, because critical and near-critical systems tend to have a high capacity for encoding and transmitting information ( 6 – 9 ). For these reasons, it is widely believed that being poised at—or at least near ( 10 – 12 )—criticality of some form endows neural populations with a high capacity for encoding and communicating information ( 4 , 5 , 12 , 13 ), particularly during conscious states ( 1 , 2 ). Conversely, because signatures of cortical criticality have been observed to disappear or diminish during unconscious states ( 4 , 14 , 15 ), it may be that a transition of cortical activity away from some critical point is what underlies the disruption to cortical information processing during unconscious states ( 2 ).…”

The ascending arousal system shapes low-dimensional neural dynamics to mediate awareness of intrinsic cognitive states

“…1A) through the modulation of second-messenger cascades 4 , noradrenaline released by the LC would augment inter-regional coordination 30 . Importantly, this capacity could confer adaptive benefits across a spectrum, potentially facilitating the formation of flexible coalitions in precise cognitive contexts 46 , while also forcing a broader landscape flattening (i.e., a ‘reset’) in the context of large, unexpected changes 27,40 . Similarly, the idea that phasic cholinergic bursts deepens energy wells is consistent with the idea that the cholinergic system instantiates divisive normalization within the cerebral cortex 14 .…”

Extracting Dynamical Understanding From Neural-Mass Models of Mouse Cortex

“…We have focused on the behavior of the model in three specific dynamical regimes (a fixed point with gain, hysteresis, and limit cycle), but the results should be qualitatively applicable to those same dynamical regimes of other models. However, we note that other models with different dynamical features may display different behavior, such as the Wong–Wang model (Wong and Wang, 2006 ; Deco et al, 2013 , 2021 ; Murray et al, 2017 ; Demirtas et al, 2019 ; Wang et al, 2019 ), or models that incorporate cortico–thalamic interactions (Wilson and Cowan, 1973 ; Robinson et al, 2015 ; Lin et al, 2020 ; Müller et al, 2020 ). We also note that while our aim here was to understand the model dynamics directly, it is common practice to simulate a hemodynamic response, such as the Balloon–Windkessel model (Friston et al, 2000 ) or a more sophisticated hemodynamic response function (Aquino et al, 2014 ).…”