IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26977-3.html
   My bibliography  Save this article

A distributed fMRI-based signature for the subjective experience of fear

Author

Listed:
  • Feng Zhou

    (University of Electronic Science and Technology of China
    Dartmouth College
    Southwest University)

  • Weihua Zhao

    (University of Electronic Science and Technology of China)

  • Ziyu Qi

    (University of Electronic Science and Technology of China)

  • Yayuan Geng

    (University of Electronic Science and Technology of China)

  • Shuxia Yao

    (University of Electronic Science and Technology of China)

  • Keith M. Kendrick

    (University of Electronic Science and Technology of China)

  • Tor D. Wager

    (Dartmouth College)

  • Benjamin Becker

    (University of Electronic Science and Technology of China)

Abstract

The specific neural systems underlying the subjective feeling of fear are debated in affective neuroscience. Here, we combine functional MRI with machine learning to identify and evaluate a sensitive and generalizable neural signature predictive of the momentary self-reported subjective fear experience across discovery (n = 67), validation (n = 20) and generalization (n = 31) cohorts. We systematically demonstrate that accurate fear prediction crucially requires distributed brain systems, with important contributions from cortical (e.g., prefrontal, midcingulate and insular cortices) and subcortical (e.g., thalamus, periaqueductal gray, basal forebrain and amygdala) regions. We further demonstrate that the neural representation of subjective fear is distinguishable from the representation of conditioned threat and general negative affect. Overall, our findings suggest that subjective fear, which exhibits distinct neural representation with some other aversive states, is encoded in distributed systems rather than isolated ‘fear centers’.

Suggested Citation

  • Feng Zhou & Weihua Zhao & Ziyu Qi & Yayuan Geng & Shuxia Yao & Keith M. Kendrick & Tor D. Wager & Benjamin Becker, 2021. "A distributed fMRI-based signature for the subjective experience of fear," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26977-3
    DOI: 10.1038/s41467-021-26977-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26977-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-26977-3?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. Choong-Wan Woo & Leonie Koban & Ethan Kross & Martin A. Lindquist & Marie T. Banich & Luka Ruzic & Jessica R. Andrews-Hanna & Tor D. Wager, 2014. "Separate neural representations for physical pain and social rejection," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    2. Leonie Koban & Marieke Jepma & Marina López-Solà & Tor D. Wager, 2019. "Different brain networks mediate the effects of social and conditioned expectations on pain," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Paul T E Cusack, 2020. "On Pain," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 31(3), pages 24253-24254, October.
    4. Ralph Adolphs & Frederic Gosselin & Tony W. Buchanan & Daniel Tranel & Philippe Schyns & Antonio R. Damasio, 2005. "A mechanism for impaired fear recognition after amygdala damage," Nature, Nature, vol. 433(7021), pages 68-72, January.
    5. Choong-Wan Woo & Mathieu Roy & Jason T Buhle & Tor D Wager, 2015. "Distinct Brain Systems Mediate the Effects of Nociceptive Input and Self-Regulation on Pain," PLOS Biology, Public Library of Science, vol. 13(1), pages 1-14, January.
    6. Rotem Botvinik-Nezer & Felix Holzmeister & Colin F. Camerer & Anna Dreber & Juergen Huber & Magnus Johannesson & Michael Kirchler & Roni Iwanir & Jeanette A. Mumford & R. Alison Adcock & Paolo Avesani, 2020. "Variability in the analysis of a single neuroimaging dataset by many teams," Nature, Nature, vol. 582(7810), pages 84-88, June.
    7. Patricia H. Janak & Kay M. Tye, 2015. "From circuits to behaviour in the amygdala," Nature, Nature, vol. 517(7534), pages 284-292, January.
    8. Corrado Corradi-Dell’Acqua & Anita Tusche & Patrik Vuilleumier & Tania Singer, 2016. "Cross-modal representations of first-hand and vicarious pain, disgust and fairness in insular and cingulate cortex," Nature Communications, Nature, vol. 7(1), pages 1-12, April.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Zhenfu Wen & Edward F. Pace-Schott & Sara W. Lazar & Jörgen Rosén & Fredrik Åhs & Elizabeth A. Phelps & Joseph E. LeDoux & Mohammed R. Milad, 2024. "Distributed neural representations of conditioned threat in the human brain," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Xiqin Liu & Guojuan Jiao & Feng Zhou & Keith M. Kendrick & Dezhong Yao & Qiyong Gong & Shitong Xiang & Tianye Jia & Xiao-Yong Zhang & Jie Zhang & Jianfeng Feng & Benjamin Becker, 2024. "A neural signature for the subjective experience of threat anticipation under uncertainty," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    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. Daniel Niederer & Juliane Mueller, 2020. "Sustainability effects of motor control stabilisation exercises on pain and function in chronic nonspecific low back pain patients: A systematic review with meta-analysis and meta-regression," PLOS ONE, Public Library of Science, vol. 15(1), pages 1-21, January.
    2. Sana Sadiq & Khadija Anasse & Najib Slimani, 2022. "The impact of mobile phones on high school students: connecting the research dots," Technium Social Sciences Journal, Technium Science, vol. 30(1), pages 252-270, April.
    3. Jitka Vseteckova, 2020. "Psychological Therapy for ICT Literate Older Adults in the Time of COVID-19 - Perceptions on the Acceptability of Online Versus Face to Face Versions of a Mindfulness for Later Life Group," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 31(1), pages 23912-23916, October.
    4. Khalid Ahmed Al-Ansari & Ahmet Faruk Aysan, 2021. "More than ten years of Blockchain creation: How did we use the technology and which direction is the research heading? [Plus de dix ans de création Blockchain : Comment avons-nous utilisé la techno," Working Papers hal-03343048, HAL.
    5. Ling, Gabriel Hoh Teck & Suhud, Nur Amiera binti Md & Leng, Pau Chung & Yeo, Lee Bak & Cheng, Chin Tiong & Ahmad, Mohd Hamdan Haji & Matusin, AK Mohd Rafiq AK, 2021. "Factors Influencing Asia-Pacific Countries’ Success Level in Curbing COVID-19: A Review Using a Social–Ecological System (SES) Framework," SocArXiv b9f2w, Center for Open Science.
    6. Benedict E. DeDominicis, 2021. "Multinational Enterprises And Economic Nationalism: A Strategic Analysis Of Culture," Global Journal of Business Research, The Institute for Business and Finance Research, vol. 15(1), pages 19-66.
    7. Robert J. R. Elliott & Ingmar Schumacher & Cees Withagen, 2020. "Suggestions for a Covid-19 Post-Pandemic Research Agenda in Environmental Economics," Environmental & Resource Economics, Springer;European Association of Environmental and Resource Economists, vol. 76(4), pages 1187-1213, August.
    8. Rafał Krupiński, 2020. "Virtual Reality System and Scientific Visualisation for Smart Designing and Evaluating of Lighting," Energies, MDPI, vol. 13(20), pages 1-17, October.
    9. Werner Hölzl & Michael Böheim & Klaus S. Friesenbichler & Agnes Kügler & Thomas Leoni, 2021. "Staatliche Hilfsmaßnahmen für Unternehmen in der COVID-19-Krise. Eine begleitende Analyse operativer Aspekte und Unternehmenseinschätzungen," WIFO Studies, WIFO, number 66624, April.
    10. Thorbecke, Willem & Chen, Chen & Salike, Nimesh, 2021. "China’s exports in a protectionist world," Journal of Asian Economics, Elsevier, vol. 77(C).
    11. Ilicic, Jasmina & Baxter, Stacey M. & Kulczynski, Alicia, 2016. "White eyes are the window to the pure soul: Metaphorical association and overgeneralization effects for spokespeople with limbal rings," International Journal of Research in Marketing, Elsevier, vol. 33(4), pages 840-855.
    12. Óscar Chiva-Bartoll & Honorato Morente-Oria & Francisco Tomás González-Fernández & Pedro Jesús Ruiz-Montero, 2020. "Anxiety and Bodily Pain in Older Women Participants in a Physical Education Program. A Multiple Moderated Mediation Analysis," Sustainability, MDPI, vol. 12(10), pages 1-12, May.
    13. Gigi Foster, 2020. "The behavioural economics of government responses to COVID-19," Journal of Behavioral Economics for Policy, Society for the Advancement of Behavioral Economics (SABE), vol. 4(S3), pages 11-43, December.
    14. Reza Salajegheh & Edward C Nemergut & Terran M Rice & Roy Joseph & Siny Tsang & Bethany M Sarosiek & C Paige Muthusubramanian & Katelyn M Hipwell & Kate B Horton & Bhiken I Naik, 2020. "Impact of a perioperative oral opioid substitution protocol during the nationwide intravenous opioid shortage: A single center, interrupted time series with segmented regression analysis," PLOS ONE, Public Library of Science, vol. 15(6), pages 1-13, June.
    15. Jaroslav Flegr & Radim Kuba & Robin Kopecký, 2020. "Rhesus-minus phenotype as a predictor of sexual desire and behavior, wellbeing, mental health, and fecundity," PLOS ONE, Public Library of Science, vol. 15(7), pages 1-11, July.
    16. Tonata Dengeingei & Laura Uusiku & Olivia N Tuhadeleni & Alice Lifalaza, 2020. "Assessing Knowledge and Practice Regarding the Management of Dysmenorrhea Among Students at University of Namibia Rundu Campus," Global Journal of Health Science, Canadian Center of Science and Education, vol. 12(9), pages 105-105, August.
    17. Christoph Huber & Christian König-Kersting, 2022. "Experimenting with Financial Professionals," Working Papers 2022-07, Faculty of Economics and Statistics, Universität Innsbruck.
    18. Nick Huntington‐Klein & Andreu Arenas & Emily Beam & Marco Bertoni & Jeffrey R. Bloem & Pralhad Burli & Naibin Chen & Paul Grieco & Godwin Ekpe & Todd Pugatch & Martin Saavedra & Yaniv Stopnitzky, 2021. "The influence of hidden researcher decisions in applied microeconomics," Economic Inquiry, Western Economic Association International, vol. 59(3), pages 944-960, July.
    19. Craig C Kage & Mohsen Akbari-Shandiz & Mary H Foltz & Rebekah L Lawrence & Taycia L Brandon & Nathaniel E Helwig & Arin M Ellingson, 2020. "Validation of an automated shape-matching algorithm for biplane radiographic spine osteokinematics and radiostereometric analysis error quantification," PLOS ONE, Public Library of Science, vol. 15(2), pages 1-15, February.
    20. Piotr Raźniak & György Csomós & Sławomir Dorocki & Anna Winiarczyk-Raźniak, 2021. "Exploring the Shifting Geographical Pattern of the Global Command-and-Control Function of Cities," Sustainability, MDPI, vol. 13(22), pages 1-15, 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:12:y:2021:i:1:d:10.1038_s41467-021-26977-3. 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.