IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36616-8.html
   My bibliography  Save this article

Optogenetic stimulation of anterior insular cortex neurons in male rats reveals causal mechanisms underlying suppression of the default mode network by the salience network

Author

Listed:
  • Vinod Menon

    (Stanford University School of Medicine
    Stanford University School of Medicine
    Stanford University School of Medicine)

  • Domenic Cerri

    (University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill)

  • Byeongwook Lee

    (Stanford University School of Medicine)

  • Rui Yuan

    (Stanford University School of Medicine)

  • Sung-Ho Lee

    (University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill)

  • Yen-Yu Ian Shih

    (University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill)

Abstract

The salience network (SN) and default mode network (DMN) play a crucial role in cognitive function. The SN, anchored in the anterior insular cortex (AI), has been hypothesized to modulate DMN activity during stimulus-driven cognition. However, the causal neural mechanisms underlying changes in DMN activity and its functional connectivity with the SN are poorly understood. Here we combine feedforward optogenetic stimulation with fMRI and computational modeling to dissect the causal role of AI neurons in dynamic functional interactions between SN and DMN nodes in the male rat brain. Optogenetic stimulation of Chronos-expressing AI neurons suppressed DMN activity, and decreased AI-DMN and intra-DMN functional connectivity. Our findings demonstrate that feedforward optogenetic stimulation of AI neurons induces dynamic suppression and decoupling of the DMN and elucidates previously unknown features of rodent brain network organization. Our study advances foundational knowledge of causal mechanisms underlying dynamic cross-network interactions and brain network switching.

Suggested Citation

  • Vinod Menon & Domenic Cerri & Byeongwook Lee & Rui Yuan & Sung-Ho Lee & Yen-Yu Ian Shih, 2023. "Optogenetic stimulation of anterior insular cortex neurons in male rats reveals causal mechanisms underlying suppression of the default mode network by the salience network," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36616-8
    DOI: 10.1038/s41467-023-36616-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36616-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-36616-8?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. Marco Pagani & Noemi Barsotti & Alice Bertero & Stavros Trakoshis & Laura Ulysse & Andrea Locarno & Ieva Miseviciute & Alessia De Felice & Carola Canella & Kaustubh Supekar & Alberto Galbusera & Vinod, 2021. "mTOR-related synaptic pathology causes autism spectrum disorder-associated functional hyperconnectivity," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Jin Hyung Lee & Remy Durand & Viviana Gradinaru & Feng Zhang & Inbal Goshen & Dae-Shik Kim & Lief E. Fenno & Charu Ramakrishnan & Karl Deisseroth, 2010. "Global and local fMRI signals driven by neurons defined optogenetically by type and wiring," Nature, Nature, vol. 465(7299), pages 788-792, June.
    3. Jalil Taghia & Weidong Cai & Srikanth Ryali & John Kochalka & Jonathan Nicholas & Tianwen Chen & Vinod Menon, 2018. "Uncovering hidden brain state dynamics that regulate performance and decision-making during cognition," Nature Communications, Nature, vol. 9(1), pages 1-19, December.
    4. Priyamvada Rajasethupathy & Sethuraman Sankaran & James H. Marshel & Christina K. Kim & Emily Ferenczi & Soo Yeun Lee & Andre Berndt & Charu Ramakrishnan & Anna Jaffe & Maisie Lo & Conor Liston & Karl, 2015. "Projections from neocortex mediate top-down control of memory retrieval," Nature, Nature, vol. 526(7575), pages 653-659, October.
    5. Weidong Cai & Srikanth Ryali & Ramkrishna Pasumarthy & Viswanath Talasila & Vinod Menon, 2021. "Dynamic causal brain circuits during working memory and their functional controllability," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    6. Yi Chen & Patricia Pais-Roldan & Xuming Chen & Michael H. Frosz & Xin Yu, 2019. "MRI-guided robotic arm drives optogenetic fMRI with concurrent Ca2+ recording," Nature Communications, Nature, vol. 10(1), pages 1-11, 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. Nicolas Cazin & Martin Llofriu Alonso & Pablo Scleidorovich Chiodi & Tatiana Pelc & Bruce Harland & Alfredo Weitzenfeld & Jean-Marc Fellous & Peter Ford Dominey, 2019. "Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-32, July.
    2. Maanasa Jayachandran & Tatiana D. Viena & Andy Garcia & Abdiel Vasallo Veliz & Sofia Leyva & Valentina Roldan & Robert P. Vertes & Timothy A. Allen, 2023. "Nucleus reuniens transiently synchronizes memory networks at beta frequencies," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Arita Silapetere & Songhwan Hwang & Yusaku Hontani & Rodrigo G. Fernandez Lahore & Jens Balke & Francisco Velazquez Escobar & Martijn Tros & Patrick E. Konold & Rainer Matis & Roberta Croce & Peter J., 2022. "QuasAr Odyssey: the origin of fluorescence and its voltage sensitivity in microbial rhodopsins," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    4. Robert N. Fetcho & Baila S. Hall & David J. Estrin & Alexander P. Walsh & Peter J. Schuette & Jesse Kaminsky & Ashna Singh & Jacob Roshgodal & Charlotte C. Bavley & Viraj Nadkarni & Susan Antigua & Th, 2023. "Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Thibault Cholvin & Marlene Bartos, 2022. "Hemisphere-specific spatial representation by hippocampal granule cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Jens Leth Hougaard & Juan D. Moreno-Ternero & Lars Peter Østerdal, 2022. "Optimal Management of Evolving Hierarchies," Management Science, INFORMS, vol. 68(8), pages 6024-6038, August.
    7. Federico Rocchi & Carola Canella & Shahryar Noei & Daniel Gutierrez-Barragan & Ludovico Coletta & Alberto Galbusera & Alexia Stuefer & Stefano Vassanelli & Massimo Pasqualetti & Giuliano Iurilli & Ste, 2022. "Increased fMRI connectivity upon chemogenetic inhibition of the mouse prefrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    8. Brent Kevin Young & Jayden Nicole Brennan & Ping Wang & Ning Tian, 2018. "Virtual reality method to analyze visual recognition in mice," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-14, May.
    9. Heather C. Ratigan & Seetha Krishnan & Shai Smith & Mark E. J. Sheffield, 2023. "A thalamic-hippocampal CA1 signal for contextual fear memory suppression, extinction, and discrimination," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Yulia Dembitskaya & Andrew K. J. Boyce & Agata Idziak & Atefeh Pourkhalili Langeroudi & Misa Arizono & Jordan Girard & Guillaume Bourdellès & Mathieu Ducros & Marie Sato-Fitoussi & Amaia Ochoa de Amez, 2023. "Shadow imaging for panoptical visualization of brain tissue in vivo," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    11. Adam Institoris & Milène Vandal & Govind Peringod & Christy Catalano & Cam Ha Tran & Xinzhu Yu & Frank Visser & Cheryl Breiteneder & Leonardo Molina & Baljit S. Khakh & Minh Dang Nguyen & Roger J. Tho, 2022. "Astrocytes amplify neurovascular coupling to sustained activation of neocortex in awake mice," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    12. Domenic H. Cerri & Daniel L. Albaugh & Lindsay R. Walton & Brittany Katz & Tzu-Wen Wang & Tzu-Hao Harry Chao & Weiting Zhang & Randal J. Nonneman & Jing Jiang & Sung-Ho Lee & Amit Etkin & Catherine N., 2024. "Distinct neurochemical influences on fMRI response polarity in the striatum," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    13. Weidong Cai & Jalil Taghia & Vinod Menon, 2024. "A multi-demand operating system underlying diverse cognitive tasks," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    14. Rodrigo G. Fernandez Lahore & Niccolò P. Pampaloni & Enrico Schiewer & M.-Marcel Heim & Linda Tillert & Johannes Vierock & Johannes Oppermann & Jakob Walther & Dietmar Schmitz & David Owald & Andrew J, 2022. "Calcium-permeable channelrhodopsins for the photocontrol of calcium signalling," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    15. Colin W. Hoy & David R. Quiroga-Martinez & Eduardo Sandoval & David King-Stephens & Kenneth D. Laxer & Peter Weber & Jack J. Lin & Robert T. Knight, 2023. "Asymmetric coding of reward prediction errors in human insula and dorsomedial prefrontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    16. Thomas Hainmueller & Aurore Cazala & Li-Wen Huang & Marlene Bartos, 2024. "Subfield-specific interneuron circuits govern the hippocampal response to novelty in male mice," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    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_s41467-023-36616-8. 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.