IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-30855-x.html
   My bibliography  Save this article

Altered predictive control during memory suppression in PTSD

Author

Listed:
  • Giovanni Leone

    (Neuropsychologie et Imagerie de la Mémoire Humaine)

  • Charlotte Postel

    (Neuropsychologie et Imagerie de la Mémoire Humaine)

  • Alison Mary

    (Neuropsychologie et Imagerie de la Mémoire Humaine
    Université libre de Bruxelles (ULB))

  • Florence Fraisse

    (Neuropsychologie et Imagerie de la Mémoire Humaine)

  • Thomas Vallée

    (Neuropsychologie et Imagerie de la Mémoire Humaine)

  • Fausto Viader

    (Neuropsychologie et Imagerie de la Mémoire Humaine)

  • Vincent Sayette

    (Neuropsychologie et Imagerie de la Mémoire Humaine)

  • Denis Peschanski

    (CNRS)

  • Jaques Dayan

    (Neuropsychologie et Imagerie de la Mémoire Humaine
    Université Rennes 1)

  • Francis Eustache

    (Neuropsychologie et Imagerie de la Mémoire Humaine)

  • Pierre Gagnepain

    (Neuropsychologie et Imagerie de la Mémoire Humaine)

Abstract

Aberrant predictions of future threat lead to maladaptive avoidance in individuals with post-traumatic stress disorder (PTSD). How this disruption in prediction influences the control of memory states orchestrated by the dorsolateral prefrontal cortex is unknown. We combined computational modeling and brain connectivity analyses to reveal how individuals exposed and nonexposed to the 2015 Paris terrorist attacks formed and controlled beliefs about future intrusive re-experiencing implemented in the laboratory during a memory suppression task. Exposed individuals with PTSD used beliefs excessively to control hippocampal activity during the task. When this predictive control failed, the prediction-error associated with unwanted intrusions was poorly downregulated by reactive mechanisms. This imbalance was linked to higher severity of avoidance symptoms, but not to general disturbances such as anxiety or negative affect. Conversely, trauma-exposed participants without PTSD and nonexposed individuals were able to optimally balance predictive and reactive control during the memory suppression task. These findings highlight a potential pathological mechanism occurring in individuals with PTSD rooted in the relationship between the brain’s predictive and control mechanisms.

Suggested Citation

  • Giovanni Leone & Charlotte Postel & Alison Mary & Florence Fraisse & Thomas Vallée & Fausto Viader & Vincent Sayette & Denis Peschanski & Jaques Dayan & Francis Eustache & Pierre Gagnepain, 2022. "Altered predictive control during memory suppression in PTSD," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30855-x
    DOI: 10.1038/s41467-022-30855-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-30855-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-30855-x?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. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    2. Neir Eshel & Michael Bukwich & Vinod Rao & Vivian Hemmelder & Ju Tian & Naoshige Uchida, 2015. "Arithmetic and local circuitry underlying dopamine prediction errors," Nature, Nature, vol. 525(7568), pages 243-246, September.
    3. Taylor W. Schmitz & Marta M. Correia & Catarina S. Ferreira & Andrew P. Prescot & Michael C. Anderson, 2017. "Hippocampal GABA enables inhibitory control over unwanted thoughts," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    4. Archy O. de Berker & Robb B. Rutledge & Christoph Mathys & Louise Marshall & Gemma F. Cross & Raymond J. Dolan & Sven Bestmann, 2016. "Computations of uncertainty mediate acute stress responses in humans," Nature Communications, Nature, vol. 7(1), pages 1-11, April.
    5. Jean Daunizeau & Hanneke E M den Ouden & Matthias Pessiglione & Stefan J Kiebel & Klaas E Stephan & Karl J Friston, 2010. "Observing the Observer (I): Meta-Bayesian Models of Learning and Decision-Making," PLOS ONE, Public Library of Science, vol. 5(12), pages 1-10, December.
    6. Justin C. Hulbert & Richard N. Henson & Michael C. Anderson, 2016. "Inducing amnesia through systemic suppression," Nature Communications, Nature, vol. 7(1), pages 1-9, April.
    7. Jean Daunizeau & Vincent Adam & Lionel Rigoux, 2014. "VBA: A Probabilistic Treatment of Nonlinear Models for Neurobiological and Behavioural Data," PLOS Computational Biology, Public Library of Science, vol. 10(1), pages 1-16, January.
    8. Will D Penny & Klaas E Stephan & Jean Daunizeau & Maria J Rosa & Karl J Friston & Thomas M Schofield & Alex P Leff, 2010. "Comparing Families of Dynamic Causal Models," PLOS Computational Biology, Public Library of Science, vol. 6(3), pages 1-14, March.
    9. Neir Eshel & Michael Bukwich & Vinod Rao & Vivian Hemmelder & Ju Tian & Naoshige Uchida, 2015. "Erratum: Arithmetic and local circuitry underlying dopamine prediction errors," Nature, Nature, vol. 527(7578), pages 398-398, November.
    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. Fabien Vinckier & Lionel Rigoux & Irma T Kurniawan & Chen Hu & Sacha Bourgeois-Gironde & Jean Daunizeau & Mathias Pessiglione, 2019. "Sour grapes and sweet victories: How actions shape preferences," PLOS Computational Biology, Public Library of Science, vol. 15(1), pages 1-24, January.
    2. Dimitrije Marković & Jan Gläscher & Peter Bossaerts & John O’Doherty & Stefan J Kiebel, 2015. "Modeling the Evolution of Beliefs Using an Attentional Focus Mechanism," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-34, October.
    3. Andreea O Diaconescu & Christoph Mathys & Lilian A E Weber & Jean Daunizeau & Lars Kasper & Ekaterina I Lomakina & Ernst Fehr & Klaas E Stephan, 2014. "Inferring on the Intentions of Others by Hierarchical Bayesian Learning," PLOS Computational Biology, Public Library of Science, vol. 10(9), pages 1-19, September.
    4. Hachi E. Manzur & Ksenia Vlasov & You-Jhe Jhong & Hung-Yen Chen & Shih-Chieh Lin, 2023. "The behavioral signature of stepwise learning strategy in male rats and its neural correlate in the basal forebrain," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Falk Lieder & Klaas E Stephan & Jean Daunizeau & Marta I Garrido & Karl J Friston, 2013. "A Neurocomputational Model of the Mismatch Negativity," PLOS Computational Biology, Public Library of Science, vol. 9(11), pages 1-14, November.
    6. Ayaka Kato & Kenji Morita, 2016. "Forgetting in Reinforcement Learning Links Sustained Dopamine Signals to Motivation," PLOS Computational Biology, Public Library of Science, vol. 12(10), pages 1-41, October.
    7. Lauren Faget & Lucie Oriol & Wen-Chun Lee & Vivien Zell & Cody Sargent & Andrew Flores & Nick G. Hollon & Dhakshin Ramanathan & Thomas S. Hnasko, 2024. "Ventral pallidum GABA and glutamate neurons drive approach and avoidance through distinct modulation of VTA cell types," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Zijian Zhu & Michael C. Anderson & Yingying Wang, 2022. "Inducing forgetting of unwanted memories through subliminal reactivation," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    9. Marie Devaine & Jean Daunizeau, 2017. "Learning about and from others' prudence, impatience or laziness: The computational bases of attitude alignment," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-28, March.
    10. Jean Daunizeau & Kerstin Preuschoff & Karl Friston & Klaas Stephan, 2011. "Optimizing Experimental Design for Comparing Models of Brain Function," PLOS Computational Biology, Public Library of Science, vol. 7(11), pages 1-18, November.
    11. Marie Devaine & Guillaume Hollard & Jean Daunizeau, 2014. "The Social Bayesian Brain: Does Mentalizing Make a Difference When We Learn?," PLOS Computational Biology, Public Library of Science, vol. 10(12), pages 1-14, December.
    12. Min Jung Kim & Daniel J. Gibson & Dan Hu & Tomoko Yoshida & Emily Hueske & Ayano Matsushima & Ara Mahar & Cynthia J. Schofield & Patlapa Sompolpong & Kathy T. Tran & Lin Tian & Ann M. Graybiel, 2024. "Dopamine release plateau and outcome signals in dorsal striatum contrast with classic reinforcement learning formulations," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    13. Jean Daunizeau & Vincent Adam & Lionel Rigoux, 2014. "VBA: A Probabilistic Treatment of Nonlinear Models for Neurobiological and Behavioural Data," PLOS Computational Biology, Public Library of Science, vol. 10(1), pages 1-16, January.
    14. Payam Piray & Nathaniel D. Daw, 2021. "A model for learning based on the joint estimation of stochasticity and volatility," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    15. Alizée Lopez-Persem & Lionel Rigoux & Sacha Bourgeois-Gironde & Jean Daunizeau & Mathias Pessiglione, 2017. "Choose, rate or squeeze: Comparison of economic value functions elicited by different behavioral tasks," PLOS Computational Biology, Public Library of Science, vol. 13(11), pages 1-18, November.
    16. Chih-Chung Ting & Nahuel Salem-Garcia & Stefano Palminteri & Jan B. Engelmann & Maël Lebreton, 2023. "Neural and computational underpinnings of biased confidence in human reinforcement learning," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    17. Antoine Collomb-Clerc & Maëlle C. M. Gueguen & Lorella Minotti & Philippe Kahane & Vincent Navarro & Fabrice Bartolomei & Romain Carron & Jean Regis & Stephan Chabardès & Stefano Palminteri & Julien B, 2023. "Human thalamic low-frequency oscillations correlate with expected value and outcomes during reinforcement learning," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    18. Joshua M. Diamond & Julio I. Chapeton & Weizhen Xie & Samantha N. Jackson & Sara K. Inati & Kareem A. Zaghloul, 2024. "Focal seizures induce spatiotemporally organized spiking activity in the human cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Corgnet, Brice & Hernán-González, Roberto & Kujal, Praveen, 2020. "On booms that never bust: Ambiguity in experimental asset markets with bubbles," Journal of Economic Dynamics and Control, Elsevier, vol. 110(C).
    20. Kyerl Park & Yoonsoo Yeo & Kisung Shin & Jeehyun Kwag, 2024. "Egocentric neural representation of geometric vertex in the retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, 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:13:y:2022:i:1:d:10.1038_s41467-022-30855-x. 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.