IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0062501.html
   My bibliography  Save this article

Learning to Attend to Threat Accelerates and Enhances Memory Consolidation

Author

Listed:
  • Rany Abend
  • Avi Karni
  • Avi Sadeh
  • Nathan A Fox
  • Daniel S Pine
  • Yair Bar-Haim

Abstract

Practice on a procedural task involves within-session learning and between-session consolidation of learning, with the latter requiring a minimum of about four hours to evolve due to involvement of slower cellular processes. Learning to attend to threats is vital for survival and thus may involve faster memory consolidation than simple procedural learning. Here, we tested whether attention to threat modulates the time-course and magnitude of learning and memory consolidation effects associated with skill practice. All participants (N = 90) practiced in two sessions on a dot-probe task featuring pairs of neutral and angry faces followed by target probes which were to be discriminated as rapidly as possible. In the attend-threat training condition, targets always appeared at the angry face location, forming an association between threat and target location; target location was unrelated to valence in a control training condition. Within each attention training condition, duration of the between-session rest interval was varied to establish the time-course for emergence of consolidation effects. During the first practice session, we observed robust improvement in task performance (online, within-session gains), followed by saturation of learning. Both training conditions exhibited similar overall learning capacities, but performance in the attend-threat condition was characterized by a faster learning rate relative to control. Consistent with the memory consolidation hypothesis, between-session performance gains (delayed gains) were observed only following a rest interval. However, rest intervals of 1 and 24 hours yielded similar delayed gains, suggesting accelerated consolidation processes. Moreover, attend-threat training resulted in greater delayed gains compared to the control condition. Auxiliary analyses revealed that enhanced performance was retained over several months, and that training to attend to neutral faces resulted in effects similar to control. These results provide a novel demonstration of how attention to threat can accelerate and enhance memory consolidation effects associated with skill acquisition.

Suggested Citation

  • Rany Abend & Avi Karni & Avi Sadeh & Nathan A Fox & Daniel S Pine & Yair Bar-Haim, 2013. "Learning to Attend to Threat Accelerates and Enhances Memory Consolidation," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-9, April.
  • Handle: RePEc:plo:pone00:0062501
    DOI: 10.1371/journal.pone.0062501
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0062501
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0062501&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0062501?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 P. Walker & Tiffany Brakefield & J. Allan Hobson & Robert Stickgold, 2003. "Dissociable stages of human memory consolidation and reconsolidation," Nature, Nature, vol. 425(6958), pages 616-620, October.
    2. J. S. Morris & A. Öhman & R. J. Dolan, 1998. "Conscious and unconscious emotional learning in the human amygdala," Nature, Nature, vol. 393(6684), pages 467-470, June.
    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. Johannes Holz & Hannah Piosczyk & Nina Landmann & Bernd Feige & Kai Spiegelhalder & Dieter Riemann & Christoph Nissen & Ulrich Voderholzer, 2012. "The Timing of Learning before Night-Time Sleep Differentially Affects Declarative and Procedural Long-Term Memory Consolidation in Adolescents," PLOS ONE, Public Library of Science, vol. 7(7), pages 1-10, July.
    2. Heiko C Bergmann & Mark Rijpkema & Guillén Fernández & Roy P C Kessels, 2012. "The Effects of Valence and Arousal on Associative Working Memory and Long-Term Memory," PLOS ONE, Public Library of Science, vol. 7(12), pages 1-9, December.
    3. Gilles Le Garrec, 2007. "Moral sentiments, democracy and redistributive politics: between nature and culture," 2007 Meeting Papers 702, Society for Economic Dynamics.
    4. Xiang Huang & Hao Jiang & Ming Lv, 2023. "Unconscious Processing of Greenery in the Tourism Context: A Breaking Continuous Flash Suppression Experiment," IJERPH, MDPI, vol. 20(3), pages 1-12, January.
    5. Sho K Sugawara & Satoshi Tanaka & Shuntaro Okazaki & Katsumi Watanabe & Norihiro Sadato, 2012. "Social Rewards Enhance Offline Improvements in Motor Skill," PLOS ONE, Public Library of Science, vol. 7(11), pages 1-6, November.
    6. Roberta Patalano, 2007. "Mind-Dependence. The Past in the Grip of the Present," Journal of Bioeconomics, Springer, vol. 9(2), pages 85-107, August.
    7. Kathrin Müsch & Andreas K Engel & Till R Schneider, 2012. "On the Blink: The Importance of Target-Distractor Similarity in Eliciting an Attentional Blink with Faces," PLOS ONE, Public Library of Science, vol. 7(7), pages 1-10, July.
    8. Gilles Le Garrec, 2007. "Moral sentiments, democracy and redistributive politics : between nature and culture," SciencePo Working papers Main hal-00973047, HAL.
    9. Megan E. Speer & Sandra Ibrahim & Daniela Schiller & Mauricio R. Delgado, 2021. "Finding positive meaning in memories of negative events adaptively updates memory," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    10. Denis Ertelt & Karsten Witt & Kathrin Reetz & Wolfgang Frank & Klaus Junghanns & Jutta Backhaus & Vera Tadic & Antonello Pellicano & Jan Born & Ferdinand Binkofski, 2012. "Skill Memory Escaping from Distraction by Sleep—Evidence from Dual-Task Performance," PLOS ONE, Public Library of Science, vol. 7(12), pages 1-9, December.
    11. Benedikt Lauber & Jesper Lundbye-Jensen & Martin Keller & Albert Gollhofer & Wolfgang Taube & Christian Leukel, 2013. "Cross-Limb Interference during Motor Learning," PLOS ONE, Public Library of Science, vol. 8(12), pages 1-8, December.
    12. Bhavin R Sheth & Davit Janvelyan & Murtuza Khan, 2008. "Practice Makes Imperfect: Restorative Effects of Sleep on Motor Learning," PLOS ONE, Public Library of Science, vol. 3(9), pages 1-9, September.
    13. Roberta Patalano, 2007. "Mind-dependence. The past in the grip of the present," Discussion Papers 1_2007, D.E.S. (Department of Economic Studies), University of Naples "Parthenope", Italy.
    14. Kristoffer C Aberg & Michael H Herzog, 2010. "Does Perceptual Learning Suffer from Retrograde Interference?," PLOS ONE, Public Library of Science, vol. 5(12), pages 1-6, December.
    15. Ella Gabitov & Arnaud Boutin & Basile Pinsard & Nitzan Censor & Stuart M Fogel & Geneviève Albouy & Bradley R King & Julie Carrier & Leonardo G Cohen & Avi Karni & Julien Doyon, 2019. "Susceptibility of consolidated procedural memory to interference is independent of its active task-based retrieval," PLOS ONE, Public Library of Science, vol. 14(1), pages 1-19, January.
    16. Tamir Eisenstein & Edna Furman-Haran & Assaf Tal, 2024. "Early excitatory-inhibitory cortical modifications following skill learning are associated with motor memory consolidation and plasticity overnight," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    17. Wenli Qian & Qianli Meng & Lin Chen & Ke Zhou, 2012. "Emotional Modulation of the Attentional Blink Is Awareness-Dependent," PLOS ONE, Public Library of Science, vol. 7(9), pages 1-6, September.
    18. Adam Safron, 2019. "Multilevel evolutionary developmental optimization (MEDO): A theoretical framework for understanding preferences and selection dynamics," Papers 1910.13443, arXiv.org, revised Nov 2019.
    19. Elżbieta A Bajcar & Wacław M Adamczyk & Karolina Wiercioch-Kuzianik & Przemysław Bąbel, 2020. "Nocebo hyperalgesia can be induced by classical conditioning without involvement of expectancy," PLOS ONE, Public Library of Science, vol. 15(5), pages 1-20, May.
    20. Asaad H. Almohammad, 2016. "Toward a Theory of Political Emotion Causation," SAGE Open, , vol. 6(3), pages 21582440166, August.

    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:plo:pone00:0062501. 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: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    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.