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Binding of cortical functional modules by synchronous high-frequency oscillations

Nature Human Behaviour (2024)Cite this article

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Abstract

Whether high-frequency phase-locked oscillations facilitate integration (‘binding’) of information across widespread cortical areas is controversial. Here we show with intracranial electroencephalography that cortico-cortical co-ripples (~100-ms-long ~90 Hz oscillations) increase during reading and semantic decisions, at the times and co-locations when and where binding should occur. Fusiform wordform areas co-ripple with virtually all language areas, maximally from 200 to 400 ms post-word-onset. Semantically specified target words evoke strong co-rippling between wordform, semantic, executive and response areas from 400 to 800 ms, with increased co-rippling between semantic, executive and response areas prior to correct responses. Co-ripples were phase-locked at zero lag over long distances (>12 cm), especially when many areas were co-rippling. General co-activation, indexed by non-oscillatory high gamma, was mainly confined to early latencies in fusiform and earlier visual areas, preceding co-ripples. These findings suggest that widespread synchronous co-ripples may assist the integration of multiple cortical areas for sustained periods during cognition.

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Fig. 1: Cortical ripple and co-ripple characteristics during a reading task.
Fig. 2: Co-ripple and co-HGB initial responses to words.
Fig. 3: Cortical co-ripples selective for words and semantic decisions.
Fig. 4: Response accuracy.
Fig. 5: Comparison of controls to co-ripple target responses.
Fig. 6: Widespread left-hemisphere phase-locking.

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Data availability

The data underlying the present study including electrode localization, ripple detections, phase data and other ripple characteristics are publicly available via Zenodo at https://doi.org/10.1101/2023.05.20.541597 (ref. 73) for density analyses and https://doi.org/10.5281/zenodo.12520199 (ref. 74) for phase analyses. Imaging and raw intracranial recordings are available upon reasonable request to the corresponding author.

Code availability

The MATLAB code underlying the present study is available via Zenodo at https://doi.org/10.1101/2023.05.20.541597 (ref. 73) for co-ripple density analyses and at https://doi.org/10.5281/zenodo.12520199 (ref. 74) for phase-related analyses. Code implementing previously published methods for ripple detection is available on GitHub (https://github.com/iverzh/ripple-detection).

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Acknowledgements

We thank C. Dickey, B. Rosen, L. Breston, E. Mukamel and S. Kajfez for their support. This project was funded by National Institutes of Health grant no. MH117155 (E.H.), National Institutes of Health grant no. T32MH020002 (J.C.G.) and Office of Naval Research grant no. N00014-16-1-2829 (E.H.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Author notes

  1. These authors contributed equally: Thomas Thesen, Eric Halgren.

Authors and Affiliations

  1. Neurosciences Graduate Program, University of California, San Diego, La Jolla, CA, USA

    Jacob C. Garrett & Ilya A. Verzhbinsky

  2. Medical Scientist Training Program, University of California, San Diego, La Jolla, CA, USA

    Ilya A. Verzhbinsky

  3. Center for Multimodal Imaging and Genetics, University of California, San Diego, La Jolla, CA, USA

    Erik Kaestner

  4. Department of Neurology, Medical College of Wisconsin, Milwaukee, WI, USA

    Chad Carlson

  5. Department of Neurosurgery, New York University Langone School of Medicine, New York, NY, USA

    Werner K. Doyle

  6. Department of Neurology, New York University Langone School of Medicine, New York, NY, USA

    Orrin Devinsky

  7. Department of Medical Education, Geisel School of Medicine, Dartmouth College, Hanover, NH, USA

    Thomas Thesen

  8. Departments of Radiology and Neurosciences, University of California, San Diego, La Jolla, CA, USA

    Eric Halgren

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Contributions

Conceptualization: E.H. Data curation: J.C.G., E.K., I.A.V. and T.T. Formal analysis: J.C.G., I.A.V. and E.H. Funding acquisition: E.H., T.T. and O.D. Investigation: T.T., C.C., W.K.D., O.D. and E.H. Methodology: J.C.G. and E.H. Project administration: E.H., T.T. and O.D. Resources: O.D., W.K.D. and C.C. Software: J.C.G. and I.A.V. Supervision: E.H. and T.T. Visualization: J.C.G. Writing—original draft: E.H. and J.C.G. Writing—review and editing: E.H. and J.C.G.

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Correspondence to Eric Halgren.

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Garrett, J.C., Verzhbinsky, I.A., Kaestner, E. et al. Binding of cortical functional modules by synchronous high-frequency oscillations. Nat Hum Behav (2024). https://doi.org/10.1038/s41562-024-01952-2

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