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Stimulation mapping and whole-brain modeling reveal gradients of excitability and recurrence in cortical networks

Author

Listed:
  • Davide Momi

    (Centre for Addiction and Mental Health (CAMH)
    Stanford University Medical Center
    Stanford University)

  • Zheng Wang

    (Centre for Addiction and Mental Health (CAMH))

  • Sara Parmigiani

    (Stanford University Medical Center
    Stanford University)

  • Ezequiel Mikulan

    (Università degli studi di Milano)

  • Sorenza P. Bastiaens

    (Centre for Addiction and Mental Health (CAMH)
    University of Toronto)

  • Mohammad P. Oveisi

    (Centre for Addiction and Mental Health (CAMH)
    University of Toronto)

  • Kevin Kadak

    (Centre for Addiction and Mental Health (CAMH)
    University of Toronto)

  • Gianluca Gaglioti

    (Università degli Studi di Milano)

  • Allison C. Waters

    (Icahn School of Medicine at Mount Sinai)

  • Sean Hill

    (Centre for Addiction and Mental Health (CAMH)
    University of Toronto
    University of Toronto)

  • Andrea Pigorini

    (Università degli Studi di Milano
    Fondazione IRCCS Cà Granda, Ospedale Maggiore Policlinico)

  • Corey J. Keller

    (Stanford University Medical Center
    Stanford University
    Veterans Affairs Palo Alto Healthcare System)

  • John D. Griffiths

    (Centre for Addiction and Mental Health (CAMH)
    University of Toronto
    University of Toronto
    University of Toronto)

Abstract

The human brain exhibits a modular and hierarchical structure, spanning low-order sensorimotor to high-order cognitive/affective systems. What is the mechanistic significance of this organization for brain dynamics and information processing properties? We investigated this question using rare simultaneous multimodal electrophysiology (stereotactic and scalp electroencephalography - EEG) recordings in 36 patients with drug-resistant focal epilepsy during presurgical intracerebral electrical stimulation (iES) (323 stimulation sessions). Our analyses revealed an anatomical gradient of excitability across the cortex, with stronger iES-evoked EEG responses in high-order compared to low-order regions. Mathematical modeling further showed that this variation in excitability levels results from a differential dependence on recurrent feedback from non-stimulated regions across the anatomical hierarchy, and could be extinguished by suppressing those connections in-silico. High-order brain regions/networks thus show an activity pattern characterized by more inter-network functional integration than low-order ones, which manifests as a spatial gradient of excitability that is emergent from, and causally dependent on, the underlying hierarchical network structure. These findings offer new insights into how hierarchical brain organization influences cognitive functions and could inform strategies for targeted neuromodulation therapies.

Suggested Citation

  • Davide Momi & Zheng Wang & Sara Parmigiani & Ezequiel Mikulan & Sorenza P. Bastiaens & Mohammad P. Oveisi & Kevin Kadak & Gianluca Gaglioti & Allison C. Waters & Sean Hill & Andrea Pigorini & Corey J., 2025. "Stimulation mapping and whole-brain modeling reveal gradients of excitability and recurrence in cortical networks," Nature Communications, Nature, vol. 16(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-58187-6
    DOI: 10.1038/s41467-025-58187-6
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    References listed on IDEAS

    as
    1. Caio Seguin & Adeel Razi & Andrew Zalesky, 2019. "Inferring neural signalling directionality from undirected structural connectomes," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Robert Leech & Reinder Vos De Wael & František Váša & Ting Xu & R. Austin Benn & Robert Scholz & Rodrigo M. Braga & Michael P. Milham & Jessica Royer & Boris C. Bernhardt & Emily J. H. Jones & Elizabe, 2023. "Variation in spatial dependencies across the cortical mantle discriminates the functional behaviour of primary and association cortex," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
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