IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38576-5.html
   My bibliography  Save this article

Semantic novelty modulates neural responses to visual change across the human brain

Author

Listed:
  • Maximilian Nentwich

    (The City College of New York)

  • Marcin Leszczynski

    (Columbia University College of Physicians and Surgeons
    Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute
    Jagiellonian University)

  • Brian E. Russ

    (Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute
    Icahn School of Medicine
    New York University at Langone)

  • Lukas Hirsch

    (The City College of New York)

  • Noah Markowitz

    (Northwell Health)

  • Kaustubh Sapru

    (The City College of New York)

  • Charles E. Schroeder

    (Columbia University College of Physicians and Surgeons
    Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute)

  • Ashesh D. Mehta

    (Northwell Health
    Zucker School of Medicine at Hofstra/Northwell)

  • Stephan Bickel

    (Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute
    Northwell Health
    Zucker School of Medicine at Hofstra/Northwell)

  • Lucas C. Parra

    (The City College of New York)

Abstract

Our continuous visual experience in daily life is dominated by change. Previous research has focused on visual change due to stimulus motion, eye movements or unfolding events, but not their combined impact across the brain, or their interactions with semantic novelty. We investigate the neural responses to these sources of novelty during film viewing. We analyzed intracranial recordings in humans across 6328 electrodes from 23 individuals. Responses associated with saccades and film cuts were dominant across the entire brain. Film cuts at semantic event boundaries were particularly effective in the temporal and medial temporal lobe. Saccades to visual targets with high visual novelty were also associated with strong neural responses. Specific locations in higher-order association areas showed selectivity to either high or low-novelty saccades. We conclude that neural activity associated with film cuts and eye movements is widespread across the brain and is modulated by semantic novelty.

Suggested Citation

  • Maximilian Nentwich & Marcin Leszczynski & Brian E. Russ & Lukas Hirsch & Noah Markowitz & Kaustubh Sapru & Charles E. Schroeder & Ashesh D. Mehta & Stephan Bickel & Lucas C. Parra, 2023. "Semantic novelty modulates neural responses to visual change across the human brain," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38576-5
    DOI: 10.1038/s41467-023-38576-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38576-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38576-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Matthew F. Glasser & Timothy S. Coalson & Emma C. Robinson & Carl D. Hacker & John Harwell & Essa Yacoub & Kamil Ugurbil & Jesper Andersson & Christian F. Beckmann & Mark Jenkinson & Stephen M. Smith , 2016. "A multi-modal parcellation of human cerebral cortex," Nature, Nature, vol. 536(7615), pages 171-178, August.
    2. Yi Pu & Xiang-Zhen Kong & Charan Ranganath & Lucia Melloni, 2022. "Event boundaries shape temporal organization of memory by resetting temporal context," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Tobias Staudigl & Elisabeth Hartl & Soheyl Noachtar & Christian F Doeller & Ole Jensen, 2017. "Saccades are phase-locked to alpha oscillations in the occipital and medial temporal lobe during successful memory encoding," PLOS Biology, Public Library of Science, vol. 15(12), pages 1-15, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Haewon Nam & Chongwon Pae & Jinseok Eo & Maeng-Keun Oh & Hae-Jeong Park, 2021. "Inter-species cortical registration between macaques and humans using a functional network property under a spherical demons framework," PLOS ONE, Public Library of Science, vol. 16(10), pages 1-22, October.
    2. Arno Klein & Satrajit S Ghosh & Forrest S Bao & Joachim Giard & Yrjö Häme & Eliezer Stavsky & Noah Lee & Brian Rossa & Martin Reuter & Elias Chaibub Neto & Anisha Keshavan, 2017. "Mindboggling morphometry of human brains," PLOS Computational Biology, Public Library of Science, vol. 13(2), pages 1-40, February.
    3. Ann Hillier & Ryan P Kelly & Terrie Klinger, 2016. "Narrative Style Influences Citation Frequency in Climate Change Science," PLOS ONE, Public Library of Science, vol. 11(12), pages 1-12, December.
    4. Manish Saggar & James M. Shine & Raphaël Liégeois & Nico U. F. Dosenbach & Damien Fair, 2022. "Precision dynamical mapping using topological data analysis reveals a hub-like transition state at rest," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    5. Casey Paquola & Reinder Vos De Wael & Konrad Wagstyl & Richard A I Bethlehem & Seok-Jun Hong & Jakob Seidlitz & Edward T Bullmore & Alan C Evans & Bratislav Misic & Daniel S Margulies & Jonathan Small, 2019. "Microstructural and functional gradients are increasingly dissociated in transmodal cortices," PLOS Biology, Public Library of Science, vol. 17(5), pages 1-28, May.
    6. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Gustavo Deco & Diego Vidaurre & Morten L. Kringelbach, 2021. "Revisiting the global workspace orchestrating the hierarchical organization of the human brain," Nature Human Behaviour, Nature, vol. 5(4), pages 497-511, April.
    8. Sofie L. Valk & Ting Xu & Casey Paquola & Bo-yong Park & Richard A. I. Bethlehem & Reinder Vos de Wael & Jessica Royer & Shahrzad Kharabian Masouleh & Şeyma Bayrak & Peter Kochunov & B. T. Thomas Yeo , 2022. "Genetic and phylogenetic uncoupling of structure and function in human transmodal cortex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    9. Natalie Weed & Trygve Bakken & Nile Graddis & Nathan Gouwens & Daniel Millman & Michael Hawrylycz & Jack Waters, 2019. "Identification of genetic markers for cortical areas using a Random Forest classification routine and the Allen Mouse Brain Atlas," PLOS ONE, Public Library of Science, vol. 14(9), pages 1-13, September.
    10. Zachariah M. Reagh & Charan Ranganath, 2023. "Flexible reuse of cortico-hippocampal representations during encoding and recall of naturalistic events," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    11. Daniel S. Kluger & Carina Forster & Omid Abbasi & Nikos Chalas & Arno Villringer & Joachim Gross, 2023. "Modulatory dynamics of periodic and aperiodic activity in respiration-brain coupling," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    12. Ernst Schwartz & Karl-Heinz Nenning & Katja Heuer & Nathan Jeffery & Ornella C. Bertrand & Roberto Toro & Gregor Kasprian & Daniela Prayer & Georg Langs, 2023. "Evolution of cortical geometry and its link to function, behaviour and ecology," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    13. Mohamed Abdelhack & Peter Zhukovsky & Milos Milic & Shreyas Harita & Michael Wainberg & Shreejoy J. Tripathy & John D. Griffiths & Sean L. Hill & Daniel Felsky, 2023. "Opposing brain signatures of sleep in task-based and resting-state conditions," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    14. Santarnecchi, Emiliano & Emmendorfer, Alexandra & Pascual-Leone, Alvaro, 2017. "Dissecting the parieto-frontal correlates of fluid intelligence: A comprehensive ALE meta-analysis study," Intelligence, Elsevier, vol. 63(C), pages 9-28.
    15. Panagiotis Fotiadis & Matthew Cieslak & Xiaosong He & Lorenzo Caciagli & Mathieu Ouellet & Theodore D. Satterthwaite & Russell T. Shinohara & Dani S. Bassett, 2023. "Myelination and excitation-inhibition balance synergistically shape structure-function coupling across the human cortex," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    16. Andrew D. Grotzinger & Travis T. Mallard & Zhaowen Liu & Jakob Seidlitz & Tian Ge & Jordan W. Smoller, 2023. "Multivariate genomic architecture of cortical thickness and surface area at multiple levels of analysis," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    17. Lucas G. S. França & Judit Ciarrusta & Oliver Gale-Grant & Sunniva Fenn-Moltu & Sean Fitzgibbon & Andrew Chew & Shona Falconer & Ralica Dimitrova & Lucilio Cordero-Grande & Anthony N. Price & Emer Hug, 2024. "Neonatal brain dynamic functional connectivity in term and preterm infants and its association with early childhood neurodevelopment," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    18. Paulina Kieliba & Sasidhar Madugula & Nicola Filippini & Eugene P Duff & Tamar R Makin, 2019. "Large-scale intrinsic connectivity is consistent across varying task demands," PLOS ONE, Public Library of Science, vol. 14(4), pages 1-21, April.
    19. Xiaoguang Tian & Yuyan Chen & Piotr Majka & Diego Szczupak & Yonatan Sanz Perl & Cecil Chern-Chyi Yen & Chuanjun Tong & Furui Feng & Haiteng Jiang & Daniel Glen & Gustavo Deco & Marcello G. P. Rosa & , 2022. "An integrated resource for functional and structural connectivity of the marmoset brain," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    20. David M Alexander & Tonio Ball & Andreas Schulze-Bonhage & Cees van Leeuwen, 2019. "Large-scale cortical travelling waves predict localized future cortical signals," PLOS Computational Biology, Public Library of Science, vol. 15(11), pages 1-34, November.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38576-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.