Reinforcement biases subsequent perceptual decisions when confidence is low, a widespread behavioral phenomenon

Author:

Lak Armin12ORCID,Hueske Emily345,Hirokawa Junya67ORCID,Masset Paul368ORCID,Ott Torben69,Urai Anne E610ORCID,Donner Tobias H10ORCID,Carandini Matteo2ORCID,Tonegawa Susumu411,Uchida Naoshige3ORCID,Kepecs Adam69

Affiliation:

1. Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom

2. UCL Institute of Ophthalmology, University College London, London, United Kingdom

3. Department of Molecular and Cellular Biology and Center for Brain Science, Harvard University, Cambridge, United States

4. RIKEN-MIT Laboratory at the Picower Institute for Learning and Memory at Department of Biology and Department of Brain and Cognitive Science, Massachusetts Institute of Technology, Cambridge, United States

5. McGovern Institute for Brain Research at Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States

6. Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

7. Graduate School of Brain Science, Doshisha University, Kyotanabe, Kyoto, Japan

8. Watson School of Biological Sciences, Cold Spring Harbor, United States

9. Departments of Neuroscience and Psychiatry, Washington University School of Medicine, St. Louis, United States

10. Department of Neurophysiology, University Medical Center, Hamburg-Eppendorf, Hamburg, Germany

11. Howard Hughes Medical Institute at Massachusetts Institute of Technology, Cambridge, United States

Abstract

Learning from successes and failures often improves the quality of subsequent decisions. Past outcomes, however, should not influence purely perceptual decisions after task acquisition is complete since these are designed so that only sensory evidence determines the correct choice. Yet, numerous studies report that outcomes can bias perceptual decisions, causing spurious changes in choice behavior without improving accuracy. Here we show that the effects of reward on perceptual decisions are principled: past rewards bias future choices specifically when previous choice was difficult and hence decision confidence 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 this choice-updating strategy can be explained by reinforcement learning models incorporating statistical decision confidence into their teaching signals. 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.

Funder

Wellcome

National Institutes of Health

Deutsche Forschungsgemeinschaft

RIKEN

JPB Foundation

Howard Hughes Medical Institute

German Academic Exchange Service

Harvard University

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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