Literature DB >> 32286227

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

Armin Lak1,2, Emily Hueske3,4,5, Junya Hirokawa6,7, Paul Masset3,6,8, Torben Ott6,9, Anne E Urai6,10, Tobias H Donner10, Matteo Carandini2, Susumu Tonegawa4,11, Naoshige Uchida3, Adam Kepecs6,9.   

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.
© 2020, Lak et al.

Entities:  

Keywords:  human; mouse; neuroscience; rat; reinforcement learning; reward; sensory decision; uncertainty

Mesh:

Year:  2020        PMID: 32286227      PMCID: PMC7213979          DOI: 10.7554/eLife.49834

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  45 in total

1.  Representation of action-specific reward values in the striatum.

Authors:  Kazuyuki Samejima; Yasumasa Ueda; Kenji Doya; Minoru Kimura
Journal:  Science       Date:  2005-11-25       Impact factor: 47.728

Review 2.  The computational neurobiology of learning and reward.

Authors:  Nathaniel D Daw; Kenji Doya
Journal:  Curr Opin Neurobiol       Date:  2006-03-24       Impact factor: 6.627

3.  The relative influences of priors and sensory evidence on an oculomotor decision variable during perceptual learning.

Authors:  Joshua I Gold; Chi-Tat Law; Patrick Connolly; Sharath Bennur
Journal:  J Neurophysiol       Date:  2008-08-27       Impact factor: 2.714

4.  Midbrain Dopamine Neurons Signal Belief in Choice Accuracy during a Perceptual Decision.

Authors:  Armin Lak; Kensaku Nomoto; Mehdi Keramati; Masamichi Sakagami; Adam Kepecs
Journal:  Curr Biol       Date:  2017-03-09       Impact factor: 10.834

Review 5.  Neural basis of reinforcement learning and decision making.

Authors:  Daeyeol Lee; Hyojung Seo; Min Whan Jung
Journal:  Annu Rev Neurosci       Date:  2012-03-29       Impact factor: 12.449

6.  Adaptable history biases in human perceptual decisions.

Authors:  Arman Abrahamyan; Laura Luz Silva; Steven C Dakin; Matteo Carandini; Justin L Gardner
Journal:  Proc Natl Acad Sci U S A       Date:  2016-06-02       Impact factor: 11.205

7.  Pupil-linked arousal is driven by decision uncertainty and alters serial choice bias.

Authors:  Anne E Urai; Anke Braun; Tobias H Donner
Journal:  Nat Commun       Date:  2017-03-03       Impact factor: 14.919

8.  Post-decision biases reveal a self-consistency principle in perceptual inference.

Authors:  Long Luu; Alan A Stocker
Journal:  Elife       Date:  2018-05-15       Impact factor: 8.140

9.  High-Yield Methods for Accurate Two-Alternative Visual Psychophysics in Head-Fixed Mice.

Authors:  Christopher P Burgess; Armin Lak; Nicholas A Steinmetz; Peter Zatka-Haas; Charu Bai Reddy; Elina A K Jacobs; Jennifer F Linden; Joseph J Paton; Adam Ranson; Sylvia Schröder; Sofia Soares; Miles J Wells; Lauren E Wool; Kenneth D Harris; Matteo Carandini
Journal:  Cell Rep       Date:  2017-09-05       Impact factor: 9.423

10.  Post-decision processing in primate prefrontal cortex influences subsequent choices on an auditory decision-making task.

Authors:  Yale Cohen; Joshua I Gold; Joji Tsunada
Journal:  Elife       Date:  2019-06-06       Impact factor: 8.140

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  19 in total

1.  Control of adaptive action selection by secondary motor cortex during flexible visual categorization.

Authors:  Tian-Yi Wang; Jing Liu; Haishan Yao
Journal:  Elife       Date:  2020-06-24       Impact factor: 8.140

2.  Distinct temporal difference error signals in dopamine axons in three regions of the striatum in a decision-making task.

Authors:  Iku Tsutsui-Kimura; Hideyuki Matsumoto; Korleki Akiti; Melissa M Yamada; Naoshige Uchida; Mitsuko Watabe-Uchida
Journal:  Elife       Date:  2020-12-21       Impact factor: 8.140

3.  Value representations in the rodent orbitofrontal cortex drive learning, not choice.

Authors:  Kevin J Miller; Matthew M Botvinick; Carlos D Brody
Journal:  Elife       Date:  2022-08-17       Impact factor: 8.713

4.  Influence of Recent Trial History on Interval Timing.

Authors:  Taorong Xie; Can Huang; Yijie Zhang; Jing Liu; Haishan Yao
Journal:  Neurosci Bull       Date:  2022-10-08       Impact factor: 5.271

5.  Inferring learning rules from animal decision-making.

Authors:  Zoe C Ashwood; Nicholas A Roy; Ji Hyun Bak; Jonathan W Pillow
Journal:  Adv Neural Inf Process Syst       Date:  2020

6.  Dynamic task-belief is an integral part of decision-making.

Authors:  Cheng Xue; Lily E Kramer; Marlene R Cohen
Journal:  Neuron       Date:  2022-06-13       Impact factor: 18.688

7.  Mice alternate between discrete strategies during perceptual decision-making.

Authors:  Zoe C Ashwood; Nicholas A Roy; Iris R Stone; Anne E Urai; Anne K Churchland; Alexandre Pouget; Jonathan W Pillow
Journal:  Nat Neurosci       Date:  2022-02-07       Impact factor: 28.771

8.  Standardized and reproducible measurement of decision-making in mice.

Authors:  Valeria Aguillon-Rodriguez; Dora Angelaki; Hannah Bayer; Niccolo Bonacchi; Matteo Carandini; Fanny Cazettes; Gaelle Chapuis; Anne K Churchland; Yang Dan; Eric Dewitt; Mayo Faulkner; Hamish Forrest; Laura Haetzel; Michael Häusser; Sonja B Hofer; Fei Hu; Anup Khanal; Christopher Krasniak; Ines Laranjeira; Zachary F Mainen; Guido Meijer; Nathaniel J Miska; Thomas D Mrsic-Flogel; Masayoshi Murakami; Jean-Paul Noel; Alejandro Pan-Vazquez; Cyrille Rossant; Joshua Sanders; Karolina Socha; Rebecca Terry; Anne E Urai; Hernando Vergara; Miles Wells; Christian J Wilson; Ilana B Witten; Lauren E Wool; Anthony M Zador
Journal:  Elife       Date:  2021-05-20       Impact factor: 8.713

9.  A Push For Examining Subjective Experience in Value-Based Decision-Making.

Authors:  Drew C Schreiner; Ege A Yalcinbas; Christina M Gremel
Journal:  Curr Opin Behav Sci       Date:  2021-04-15

10.  Probabilistic discrimination of relative stimulus features in mice.

Authors:  Dmitry R Lyamzin; Ryo Aoki; Mohammad Abdolrahmani; Andrea Benucci
Journal:  Proc Natl Acad Sci U S A       Date:  2021-07-27       Impact factor: 11.205

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