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Covert valuation for information sampling and choice

James L Butler, Timothy H. Muller, Sebastijan Veselic, W. M. Nishantha Malalasekera, Laurence T. Hunt, Timothy E.J. Behrens, Steven W. Kennerley
doi: https://doi.org/10.1101/2021.10.08.463476
James L Butler
1Department of Clinical and Movement Neurosciences, University College London, London, WC1N 3BG, United Kingdom
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Timothy H. Muller
1Department of Clinical and Movement Neurosciences, University College London, London, WC1N 3BG, United Kingdom
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Sebastijan Veselic
1Department of Clinical and Movement Neurosciences, University College London, London, WC1N 3BG, United Kingdom
2Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3AR, UK
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W. M. Nishantha Malalasekera
1Department of Clinical and Movement Neurosciences, University College London, London, WC1N 3BG, United Kingdom
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Laurence T. Hunt
3Department of Psychiatry, University of Oxford, Oxford OX3 7JX, United Kingdom
4Wellcome Centre for Integrative Neuroimaging, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, UK
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Timothy E.J. Behrens
3Department of Psychiatry, University of Oxford, Oxford OX3 7JX, United Kingdom
4Wellcome Centre for Integrative Neuroimaging, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, UK
5Sainsbury Wellcome Centre for Neural Circuits and Behaviour, UCL, London W1T 4JG, UK
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Steven W. Kennerley
1Department of Clinical and Movement Neurosciences, University College London, London, WC1N 3BG, United Kingdom
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  • For correspondence: s.kennerley@ucl.ac.uk
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Abstract

We use our eyes to assess the value of objects around us and carefully fixate options that we are about to choose. Neurons in the prefrontal cortex reliably encode the value of fixated options, which is essential for decision making. Yet as a decision unfolds, it remains unclear how prefrontal regions determine which option should be fixated next. Here we show that anterior cingulate cortex (ACC) encodes the value of options in the periphery to guide subsequent fixations during economic choice. In an economic decision-making task involving four simultaneously presented cues, we found rhesus macaques evaluated cues using their peripheral vision. This served two distinct purposes: subjects were more likely to fixate valuable peripheral cues, and more likely to choose valuable options whose cues were never even fixated. ACC, orbitofrontal cortex, dorsolateral prefrontal cortex, and ventromedial prefrontal cortex neurons all encoded cue value post-fixation. ACC was unique, however, in also encoding the value of cues before fixation and even cues that were never fixated. This pre-saccadic value encoding by ACC predicted which cue was next fixated during the decision process. ACC therefore conducts simultaneous processing of peripheral information to guide information sampling and choice during decision making.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 09, 2021.
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Covert valuation for information sampling and choice
James L Butler, Timothy H. Muller, Sebastijan Veselic, W. M. Nishantha Malalasekera, Laurence T. Hunt, Timothy E.J. Behrens, Steven W. Kennerley
bioRxiv 2021.10.08.463476; doi: https://doi.org/10.1101/2021.10.08.463476
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Covert valuation for information sampling and choice
James L Butler, Timothy H. Muller, Sebastijan Veselic, W. M. Nishantha Malalasekera, Laurence T. Hunt, Timothy E.J. Behrens, Steven W. Kennerley
bioRxiv 2021.10.08.463476; doi: https://doi.org/10.1101/2021.10.08.463476

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