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

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  • Samy Castro
  • Wael El-Deredy
  • Demian Battaglia
  • Patricio Orio

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 weighted core-shell organisation of the empirical connectome, speculating that this topology of human structural connectivity may be attuned to support enhanced ignition dynamics.Author summary: The 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, ignition in the human cortex is first triggered on the strongest and most densely interconnected cortical areas–the “ignition core”–, emerging at the lowest global excitability value compared to surrogate connectomes. Finally, we suggest developmental and evolutionary constraints of the mesoscale organization that support this enhanced ignition dynamics in cortical activity.

Suggested Citation

  • Samy Castro & Wael El-Deredy & Demian Battaglia & Patricio Orio, 2020. "Cortical ignition dynamics is tightly linked to the core organisation of the human connectome," PLOS Computational Biology, Public Library of Science, vol. 16(7), pages 1-23, July.
  • Handle: RePEc:plo:pcbi00:1007686
    DOI: 10.1371/journal.pcbi.1007686
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    References listed on IDEAS

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    1. Logan Harriger & Martijn P van den Heuvel & Olaf Sporns, 2012. "Rich Club Organization of Macaque Cerebral Cortex and Its Role in Network Communication," PLOS ONE, Public Library of Science, vol. 7(9), pages 1-13, September.
    2. Paul T E Cusack, 2020. "The Human Brain," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 31(3), pages 24261-24266, October.
    3. Richard F. Betzel & John D. Medaglia & Danielle S. Bassett, 2018. "Diversity of meso-scale architecture in human and non-human connectomes," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    4. Christoph Kirst & Marc Timme & Demian Battaglia, 2016. "Dynamic information routing in complex networks," Nature Communications, Nature, vol. 7(1), pages 1-9, April.
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