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Published April 28, 2015 | Supplemental Material + Published
Journal Article Open

Neural Computations Mediating One-Shot Learning in the Human Brain

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.

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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Published - journal.pbio.1002137.pdf

Supplemental Material - journal.pbio.1002137.s001.XLSX

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Additional details

Created:
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