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Neural Computations Mediating One-Shot Learning in the Human Brain

Lee, Sang Wan and O'Doherty, John P. and Shimojo, Shinsuke (2015) Neural Computations Mediating One-Shot Learning in the Human Brain. PLoS Biology, 13 (4). Art. No. e1002137. ISSN 1544-9173. PMCID PMC4412411. https://resolver.caltech.edu/CaltechAUTHORS:20150428-110311461

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[img] MS Excel (S1 Data provides anonymized behavioral data from the experiments plotted in Figs 3–6) - Supplemental Material
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[img] Archive (ZIP) ( S2 Data contains the SPM8 images of the group statistical maps for Fig 5A (familiarity)) - Supplemental Material
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[img] Archive (ZIP) (S3 Data contains the SPM8 images of the group statistical maps for Fig 5A (causal uncertainty)) - Supplemental Material
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[img] Archive (ZIP) (S4 Data contains the SPM8 images of the group statistical maps for Fig 5B (OS-IC)) - Supplemental Material
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[img] Image (TIFF) (S1 Fig. The learning process of the causal uncertainty model (BayesU) minimizes the total amount of uncertainty) - Supplemental Material
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[img] Image (TIFF) (S2 Fig. Balancing out control of learning rate serves to minimize the amount of total uncertainty) - Supplemental Material
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[img] Image (TIFF) (S3 Fig. Relationship between the learning rate threshold and incremental/one-shot learning) - Supplemental Material
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[img] Image (TIFF) (S4 Fig. Occurrence of one-shot learning events across non-novel and novel stimuli) - Supplemental Material
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[img] Image (TIFF) (S5 Fig. Performance comparison) - Supplemental Material
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[img] Image (TIFF) (S6 Fig. Models’ ratings and one-shot effect, categorized by round types) - Supplemental Material
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[img] Image (TIFF) (S7 Fig. Neural activity in subregions of hippocampus increases only if the learning rate is very high) - Supplemental Material
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[img] Image (TIFF) (S8 Fig. Summary of imaging results shown in Fig 5A and Fig 5B, using an analysis in which serial orthogonalization is disabled) - Supplemental Material
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[img] Image (TIFF) (S9 Fig. Sifting the evidence for task structure learning—Behavioral analysis) - Supplemental Material
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[img] Image (TIFF) (S10 Fig. Sifting the evidence for task structure learning—Model-based analysis) - Supplemental Material
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[img] Image (TIFF) (S11 Fig. Effect of the number of cue occurrences on the posterior estimation) - Supplemental Material
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[img] Image (TIFF) (S1 Table. Computational models for causal inference) - Supplemental Material
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[img] Image (TIFF) (S2 Table. Neural signatures of causal learning system) - Supplemental Material
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Abstract

Incremental learning, in which new knowledge is acquired gradually through trial and error, can be distinguished from one-shot learning, in which the brain learns rapidly from only a single pairing of a stimulus and a consequence. Very little is known about how the brain transitions between these two fundamentally different forms of learning. Here we test a computational hypothesis that uncertainty about the causal relationship between a stimulus and an outcome induces rapid changes in the rate of learning, which in turn mediates the transition between incremental and one-shot learning. By using a novel behavioral task in combination with functional magnetic resonance imaging (fMRI) data from human volunteers, we found evidence implicating the ventrolateral prefrontal cortex and hippocampus in this process. The hippocampus was selectively “switched” on when one-shot learning was predicted to occur, while the ventrolateral prefrontal cortex was found to encode uncertainty about the causal association, exhibiting increased coupling with the hippocampus for high-learning rates, suggesting this region may act as a “switch,” turning on and off one-shot learning as required.


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http://dx.doi.org/10.1371/journal.pbio.1002137DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4412411/PubMed CentralArticle
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Additional Information:© 2015 Lee et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: October 17, 2014; Accepted: March 19, 2015; Published: April 28, 2015. This work was funded by NIH grant DA033077-01 (supported by OppNet, NIH’s Basic Behavioral and Social Science Opportunity Network; http://oppnet.nih.gov/index.asp) to JPOD, by funds from the Gordon and Betty foundation (http://www.moore.org/) to JPOD, by grants from JST-CREST (http://www.jst.go.jp/kisoken/crest/en/) to SS, and by the Caltech-Tamagawa gCOE (http://gcoe.tamagawa.ac.jp/index-e.html) to SS and JPOD. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Peter Bossaerts and Frederick Eberhardt for suggestions and insightful comments and Ralph Lee for his assistance. Author Contributions: Conceived and designed the experiments: SWL JPOD SS. Performed the experiments: SWL. Analyzed the data: SWL. Contributed reagents/materials/analysis tools: SWL. Wrote the paper: SWL JPOD SS. Competing interests: The authors have declared that no competing interests exist. Data Availability: All relevant data are within the paper and its Supporting Information files.
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Funding AgencyGrant Number
NIHDA033077-01
Gordon and Betty Moore FoundationUNSPECIFIED
JST-CRESTUNSPECIFIED
Caltech-Tamagawa gCOEUNSPECIFIED
Issue or Number:4
PubMed Central ID:PMC4412411
Record Number:CaltechAUTHORS:20150428-110311461
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20150428-110311461
Official Citation:Lee SW, O’Doherty JP, Shimojo S (2015) Neural Computations Mediating One-Shot Learning in the Human Brain. PLoS Biol 13(4): e1002137. doi:10.1371/journal.pbio.1002137
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:57045
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:28 Apr 2015 18:47
Last Modified:03 Oct 2019 08:20

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