Confidence-guided updating of choice bias during perceptual decisions is a widespread behavioral phenomenon
- University College London, United Kingdom
- MIT, United States
- Doshisha University, Japan
- Cold Spring Harbor Laboratory, United States
- University Medical Center Hamburg-Eppendorf, Germany
- The Picower Institute for Learning and Memory, RIKEN-MIT Center for Neural Circuit Genetics, Massachusetts Institute of Technology, United States
- Harvard University, United States
Abstract
Learning from past successes and failures improves decisions to produce appropriate actions in each perceived situation. However, reinforcement learning is not thought to be engaged during well-trained perceptual decision tasks, —after task acquisition is complete and performance is stable—, since choice accuracy is limited by perception. We report a novel form of reinforcement learning during perceptual decisions: past rewards bias future perceptual choices specifically when the previous stimulus was difficult to judge, and the confidence in obtaining the reward was low. We identified this phenomenon in six datasets from four laboratories, across mice, rats and humans, and sensory modalities from olfaction and audition to vision. We show that reinforcement learning models incorporating decision confidence into their teaching signal explain this choice updating. Thus, reinforcement learning mechanisms are continually engaged to produce systematic adjustments of choices even in well-learned perceptual decisions in order to optimize behavior in an uncertain world.
Data availability
The data used in this study is available at http://dx.doi.org/10.6084/m9.figshare.4300043
Article and author information
Author details
Funding
Wellcome (106101)
- Armin Lak
Wellcome (213465)
- Armin Lak
National Institutes of Health (R01 MH110404)
- Naoshige Uchida
National Institutes of Health (R01MH097061 and R01DA038209)
- Naoshige Uchida
Wellcome (205093)
- Matteo Carandini
Deutsche Forschungsgemeinschaft (DO 1240/2-1 and DO 1240/3-1)
- Tobias H Donner
RIKEN-CBS
- Emily Hueske
- Susumu Tonegawa
JPB Foundation
- Emily Hueske
- Susumu Tonegawa
Howard Hughes Medical Institute
- Emily Hueske
- Susumu Tonegawa
German Academic Exchange Service
- Anne E Urai
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: The experimental procedures were approved by Institutional committees at Cold Spring Harbor Laboratory (for experiments on rats), MIT and Harvard University (for mice auditory experiments) and were in accordance with National Institute of Health standards (project ID: 18-14-11-08-1). Experiments on mice visual decisions were approved by the home Office of the United Kingdom (license 70/8021). Experiments in humans were approved by the ethics committee at the University of Amsterdam (project ID: 2014-BC-3376).
Human subjects: The ethics committee at the University of Amsterdam approved the study, and all observers gave their informed consent.project ID: 2014-BC-3376
Reviewing Editor
- Emilio Salinas, Wake Forest School of Medicine, United States
Version history
- Received: July 1, 2019
- Accepted: April 9, 2020
- Accepted Manuscript published: April 14, 2020 (version 1)
- Accepted Manuscript updated: April 15, 2020 (version 2)
- Version of Record published: May 11, 2020 (version 3)
Copyright
© 2020, Lak et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Confidence-guided updating of choice bias during perceptual decisions is a widespread behavioral phenomenon
eLife 9:e49834.
https://doi.org/10.7554/eLife.49834
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