Cortical ignition dynamics is tightly linked to the core organisation of the human connectome

Abstract

The capability of cortical regions to flexibly sustain an "ignited" state of activity has been discussed in relation to conscious perception or hierarchical information processing. Here, we investigate how the intrinsic propensity of different regions to get ignited is determined by the specific topological organisation of the structural connectome. More specifically, we simulated the resting-state dynamics of mean-field whole-brain models and assessed how dynamic multistability and ignition differ between a reference model embedding a realistic human connectome, and alternative models based on a variety of randomised connectome ensembles.We found that the strength of global excitation needed to first trigger ignition in a subset of regions is substantially smaller for the model embedding the empirical human connectome.Furthermore, when increasing the strength of excitation, the propagation of ignition outside of this initial core -which is able to self-sustain its high activity-is way more gradual than for any of the randomised connectomes, allowing for graded control of the number of ignited regions. We explain both these assets in terms of the exceptional weighed core-shell organisation of the empirical connectome, speculating that this topology of human structural connectivity may be attuned to support an enhanced ignition dynamic. Author summaryThe activity of the cortex in mammals constantly fluctuates in relation to cognitive tasks, but also during rest. The ability of brain regions to display ignition, a fast transition from low to high activity is central for the emergence of conscious perception and decision making. Here, using a biophysically inspired model of cortical activity, we show how the structural organization of human cortex supports and constrains the rise of this ignited dynamics in spontaneous cortical activity. We found that the weighted core-shell organization of the human connectome allows for a uniquely graded ignition. This graded ignition implies a smooth control of the ignition in cortical areas tuned by the global excitability. The smooth control cannot be replicated by surrogate connectomes, even though they conserve key local or global network properties. Indeed, the first trigger of ignition in the human cortex has the lowest global excitability and corresponds with the strongest interconnected areas, the ignition core.Finally, we suggest developmental and evolutionary constraints of the mesoscale organization that support this enhanced ignition dynamics in cortical activity.

Relations between large-scale brain connectivity and effects of regional stimulation depend on collective dynamical state

“…This may allow one to test which effects generalize across different network topologies and which are specific to brain network organization. For example, the recent study in [135] examines how human cortical networks may be structured to support ignition dynamics relative to other canonical network models, finding that the well-connected structural core present in actual brain networks plays a critical role. In extending this type of analysis, one could perhaps also consider whether the brain is especially well-organized for oscillatory control via localized perturbations, and how the brain's controllability depends on its current state.…”

A scale-invariant perturbative approach to study information communication in dynamic brain networks

“…The significance of the core-periphery axis has been pointed out by studies on various fronts, such as perturbation transfer [Gollo et al, 2017, Mišić et al, 2015], ignition dynamics [Castro et al, 2020], global communication [van den Heuvel et al, 2012, Harriger et al, 2012], task learning [Bassett et al, 2013], multi-layer frameworks [Battiston et al, 2018], and timescales of associated dynamics [Gollo et al, 2015]. Furthermore, neuropathological conditions have been widely associated with changes to the structural core [Crossley et al, 2014, Van Den Heuvel et al, 2013, Stam, 2014, Fornito et al, 2015], as opposed to the periphery.…”

“…The significance of the core-periphery axis has been pointed out by studies on various fronts, such as perturbation transfer [Gollo et al, 2017, Mišić et al, 2015, ignition dynamics [Castro et al, 2020],…”

Integrated World Modeling Theory (IWMT) Implemented: Towards Reverse Engineering Consciousness with the Free Energy Principle and Active Inference

“…With respect to consciousness, SOHM-formation involving deep pyramidal neurons is suggested to correspond to both "ignition" events as described by GNWT [54], as well as implementation of semi-stochastic sampling from the latent space of VAEs (cf. the "reparameterization trick") [55], including via latent (work)spaces shared by multiple VAEs.…”