IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43747-5.html
   My bibliography  Save this article

Neural substrates of parallel devaluation-sensitive and devaluation-insensitive Pavlovian learning in humans

Author

Listed:
  • Eva R. Pool

    (University of Geneva
    California Institute of Technology)

  • Wolfgang M. Pauli

    (California Institute of Technology
    California Institute of Technology)

  • Logan Cross

    (California Institute of Technology
    Stanford University)

  • John P. O’Doherty

    (California Institute of Technology
    California Institute of Technology)

Abstract

We aim to differentiate the brain regions involved in the learning and encoding of Pavlovian associations sensitive to changes in outcome value from those that are not sensitive to such changes by combining a learning task with outcome devaluation, eye-tracking, and functional magnetic resonance imaging in humans. Contrary to theoretical expectation, voxels correlating with reward prediction errors in the ventral striatum and subgenual cingulate appear to be sensitive to devaluation. Moreover, regions encoding state prediction errors appear to be devaluation insensitive. We can also distinguish regions encoding predictions about outcome taste identity from predictions about expected spatial location. Regions encoding predictions about taste identity seem devaluation sensitive while those encoding predictions about an outcome’s spatial location seem devaluation insensitive. These findings suggest the existence of multiple and distinct associative mechanisms in the brain and help identify putative neural correlates for the parallel expression of both devaluation sensitive and insensitive conditioned behaviors.

Suggested Citation

  • Eva R. Pool & Wolfgang M. Pauli & Logan Cross & John P. O’Doherty, 2023. "Neural substrates of parallel devaluation-sensitive and devaluation-insensitive Pavlovian learning in humans," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43747-5
    DOI: 10.1038/s41467-023-43747-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43747-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43747-5?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. Daniel J. Schad & Michael A. Rapp & Maria Garbusow & Stephan Nebe & Miriam Sebold & Elisabeth Obst & Christian Sommer & Lorenz Deserno & Milena Rabovsky & Eva Friedel & Nina Romanczuk-Seiferth & Hans-, 2020. "Dissociating neural learning signals in human sign- and goal-trackers," Nature Human Behaviour, Nature, vol. 4(2), pages 201-214, February.
    2. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    3. Eva R. Pool & Wolfgang M. Pauli & Carolina S. Kress & John P. O’Doherty, 2019. "Behavioural evidence for parallel outcome-sensitive and outcome-insensitive Pavlovian learning systems in humans," Nature Human Behaviour, Nature, vol. 3(3), pages 284-296, March.
    4. Nikos K. Logothetis & Jon Pauls & Mark Augath & Torsten Trinath & Axel Oeltermann, 2001. "Neurophysiological investigation of the basis of the fMRI signal," Nature, Nature, vol. 412(6843), pages 150-157, July.
    5. Nikos K. Logothetis, 2008. "What we can do and what we cannot do with fMRI," Nature, Nature, vol. 453(7197), pages 869-878, June.
    6. James D. Howard & Thorsten Kahnt, 2018. "Identity prediction errors in the human midbrain update reward-identity expectations in the orbitofrontal cortex," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    7. Wolfgang M. Pauli & Giovanni Gentile & Sven Collette & Julian M. Tyszka & John P. O’Doherty, 2019. "Evidence for model-based encoding of Pavlovian contingencies in the human brain," 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. Qingfang Liu & Yao Zhao & Sumedha Attanti & Joel L. Voss & Geoffrey Schoenbaum & Thorsten Kahnt, 2024. "Midbrain signaling of identity prediction errors depends on orbitofrontal cortex networks," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Olsen, Carmen & Gold, Anna, 2018. "Future research directions at the intersection between cognitive neuroscience research and auditors’ professional skepticism," Journal of Accounting Literature, Elsevier, vol. 41(C), pages 127-141.
    3. 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.
    4. Rita Gil & Mafalda Valente & Noam Shemesh, 2024. "Rat superior colliculus encodes the transition between static and dynamic vision modes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. JANSSENS, Jochen & DE CORTE, Annelies & SÖRENSEN, Kenneth, 2016. "Water distribution network design optimisation with respect to reliability," Working Papers 2016007, University of Antwerp, Faculty of Business and Economics.
    6. Raymond Hernandez & Elizabeth A. Pyatak & Cheryl L. P. Vigen & Haomiao Jin & Stefan Schneider & Donna Spruijt-Metz & Shawn C. Roll, 2021. "Understanding Worker Well-Being Relative to High-Workload and Recovery Activities across a Whole Day: Pilot Testing an Ecological Momentary Assessment Technique," IJERPH, MDPI, vol. 18(19), pages 1-17, October.
    7. Christopher Hassall & Michael Nisbet & Evan Norcliffe & He Wang, 2024. "The Potential Health Benefits of Urban Tree Planting Suggested through Immersive Environments," Land, MDPI, vol. 13(3), pages 1-12, February.
    8. Jie Zhao & Ji Chen & Damien Beillouin & Hans Lambers & Yadong Yang & Pete Smith & Zhaohai Zeng & Jørgen E. Olesen & Huadong Zang, 2022. "Global systematic review with meta-analysis reveals yield advantage of legume-based rotations and its drivers," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    9. Elisabeth Beckmann & Lukas Olbrich & Joseph Sakshaug, 2024. "Multivariate assessment of interviewer-related errors in a cross-national economic survey (Lukas Olbrich, Elisabeth Beckmann, Joseph W. Sakshaug)," Working Papers 253, Oesterreichische Nationalbank (Austrian Central Bank).
    10. F J Heather & D Z Childs & A M Darnaude & J L Blanchard, 2018. "Using an integral projection model to assess the effect of temperature on the growth of gilthead seabream Sparus aurata," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-19, May.
    11. Valentina Krenz & Arjen Alink & Tobias Sommer & Benno Roozendaal & Lars Schwabe, 2023. "Time-dependent memory transformation in hippocampus and neocortex is semantic in nature," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Morán-Ordóñez, Alejandra & Ameztegui, Aitor & De Cáceres, Miquel & de-Miguel, Sergio & Lefèvre, François & Brotons, Lluís & Coll, Lluís, 2020. "Future trade-offs and synergies among ecosystem services in Mediterranean forests under global change scenarios," Ecosystem Services, Elsevier, vol. 45(C).
    13. Jack McDonnell & Thomas McKenna & Kathryn A. Yurkonis & Deirdre Hennessy & Rafael Andrade Moral & Caroline Brophy, 2023. "A Mixed Model for Assessing the Effect of Numerous Plant Species Interactions on Grassland Biodiversity and Ecosystem Function Relationships," Journal of Agricultural, Biological and Environmental Statistics, Springer;The International Biometric Society;American Statistical Association, vol. 28(1), pages 1-19, March.
    14. Ana Pinto & Tong Yin & Marion Reichenbach & Raghavendra Bhatta & Pradeep Kumar Malik & Eva Schlecht & Sven König, 2020. "Enteric Methane Emissions of Dairy Cattle Considering Breed Composition, Pasture Management, Housing Conditions and Feeding Characteristics along a Rural-Urban Gradient in a Rising Megacity," Agriculture, MDPI, vol. 10(12), pages 1-18, December.
    15. Damian M. Herz & Manuel Bange & Gabriel Gonzalez-Escamilla & Miriam Auer & Keyoumars Ashkan & Petra Fischer & Huiling Tan & Rafal Bogacz & Muthuraman Muthuraman & Sergiu Groppa & Peter Brown, 2022. "Dynamic control of decision and movement speed in the human basal ganglia," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    16. Kathrin Stenchly & Marc Victor Hansen & Katharina Stein & Andreas Buerkert & Wilhelm Loewenstein, 2018. "Income Vulnerability of West African Farming Households to Losses in Pollination Services: A Case Study from Ouagadougou, Burkina Faso," Sustainability, MDPI, vol. 10(11), pages 1-12, November.
    17. Dongyan Liu & Chongran Zhou & John K. Keesing & Oscar Serrano & Axel Werner & Yin Fang & Yingjun Chen & Pere Masque & Janine Kinloch & Aleksey Sadekov & Yan Du, 2022. "Wildfires enhance phytoplankton production in tropical oceans," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    18. Zhaogeng Yang & Yanhui Li & Peijin Hu & Jun Ma & Yi Song, 2020. "Prevalence of Anemia and its Associated Factors among Chinese 9-, 12-, and 14-Year-Old Children: Results from 2014 Chinese National Survey on Students Constitution and Health," IJERPH, MDPI, vol. 17(5), pages 1-10, February.
    19. Marco Lopez-Cruz & Fernando M. Aguate & Jacob D. Washburn & Natalia Leon & Shawn M. Kaeppler & Dayane Cristina Lima & Ruijuan Tan & Addie Thompson & Laurence Willard Bretonne & Gustavo los Campos, 2023. "Leveraging data from the Genomes-to-Fields Initiative to investigate genotype-by-environment interactions in maize in North America," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    20. Baumann, Elias & Kern, Jana & Lessmann, Stefan, 2019. "Usage Continuance in Software-as-a-Service," IRTG 1792 Discussion Papers 2019-005, Humboldt University of Berlin, International Research Training Group 1792 "High Dimensional Nonstationary Time Series".

    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_s41467-023-43747-5. 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.