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Multisensory flicker modulates widespread brain networks and reduces interictal epileptiform discharges

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  • Lou T. Blanpain

    (Emory University School of Medicine
    Emory University
    Georgia Institute of Technology & Emory University)

  • Eric R. Cole

    (Emory University School of Medicine
    Georgia Institute of Technology & Emory University)

  • Emily Chen

    (Emory University School of Medicine)

  • James K. Park

    (Emory University School of Medicine)

  • Michael Y. Walelign

    (Georgia Institute of Technology)

  • Robert E. Gross

    (Emory University School of Medicine
    New Brunswick and New Jersey Medical School)

  • Brian T. Cabaniss

    (Emory University School of Medicine)

  • Jon T. Willie

    (Washington University)

  • Annabelle C. Singer

    (Emory University
    Georgia Institute of Technology & Emory University)

Abstract

Modulating brain oscillations has strong therapeutic potential. Interventions that both non-invasively modulate deep brain structures and are practical for chronic daily home use are desirable for a variety of therapeutic applications. Repetitive audio-visual stimulation, or sensory flicker, is an accessible approach that modulates hippocampus in mice, but its effects in humans are poorly defined. We therefore quantified the neurophysiological effects of flicker with high spatiotemporal resolution in patients with focal epilepsy who underwent intracranial seizure monitoring. In this interventional trial (NCT04188834) with a cross-over design, subjects underwent different frequencies of flicker stimulation in the same recording session with the effect of sensory flicker exposure on local field potential (LFP) power and interictal epileptiform discharges (IEDs) as primary and secondary outcomes, respectively. Flicker focally modulated local field potentials in expected canonical sensory cortices but also in the medial temporal lobe and prefrontal cortex, likely via resonance of stimulated long-range circuits. Moreover, flicker decreased interictal epileptiform discharges, a pathological biomarker of epilepsy and degenerative diseases, most strongly in regions where potentials were flicker-modulated, especially the visual cortex and medial temporal lobe. This trial met the scientific goal and is now closed. Our findings reveal how multi-sensory stimulation may modulate cortical structures to mitigate pathological activity in humans.

Suggested Citation

  • Lou T. Blanpain & Eric R. Cole & Emily Chen & James K. Park & Michael Y. Walelign & Robert E. Gross & Brian T. Cabaniss & Jon T. Willie & Annabelle C. Singer, 2024. "Multisensory flicker modulates widespread brain networks and reduces interictal epileptiform discharges," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47263-y
    DOI: 10.1038/s41467-024-47263-y
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    References listed on IDEAS

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    1. Guillaume Etter & Suzanne Veldt & Jisoo Choi & Sylvain Williams, 2023. "Optogenetic frequency scrambling of hippocampal theta oscillations dissociates working memory retrieval from hippocampal spatiotemporal codes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Sander van Bree & Ediz Sohoglu & Matthew H Davis & Benedikt Zoefel, 2021. "Sustained neural rhythms reveal endogenous oscillations supporting speech perception," PLOS Biology, Public Library of Science, vol. 19(2), pages 1-33, February.
    3. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    4. Minagi Ozawa & Patrick Davis & Jianguang Ni & Jamie Maguire & Thomas Papouin & Leon Reijmers, 2020. "Experience-dependent resonance in amygdalo-cortical circuits supports fear memory retrieval following extinction," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    5. Hunter F. Iaccarino & Annabelle C. Singer & Anthony J. Martorell & Andrii Rudenko & Fan Gao & Tyler Z. Gillingham & Hansruedi Mathys & Jinsoo Seo & Oleg Kritskiy & Fatema Abdurrob & Chinnakkaruppan Ad, 2016. "Gamma frequency entrainment attenuates amyloid load and modifies microglia," Nature, Nature, vol. 540(7632), pages 230-235, December.
    6. Jessica A. Cardin & Marie Carlén & Konstantinos Meletis & Ulf Knoblich & Feng Zhang & Karl Deisseroth & Li-Huei Tsai & Christopher I. Moore, 2009. "Driving fast-spiking cells induces gamma rhythm and controls sensory responses," Nature, Nature, vol. 459(7247), pages 663-667, June.
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