Capturing the temporal evolution of choice across prefrontal cortex

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Abstract

Activity in prefrontal cortex (PFC) has been richly described using economic models of choice. Yet such descriptions fail to capture the dynamics of decision formation. Describing dynamic neural processes has proven challenging due to the problem of indexing the internal state of PFC and its trial-by-trial variation. Using primate neurophysiology and human magnetoencephalography, we here recover a single-trial index of PFC internal states from multiple simultaneously recorded PFC subregions. This index can explain the origins of neural representations of economic variables in PFC. It describes the relationship between neural dynamics and behavior in both human and monkey PFC, directly bridging between human neuroimaging data and underlying neuronal activity. Moreover, it reveals a functionally dissociable interaction between orbitofrontal cortex, anterior cingulate cortex and dorsolateral PFC in guiding cost-benefit decisions. We cast our observations in terms of a neural network model of choice, providing formal links to mechanistic dynamical accounts of decision-making.

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Laurence Tudor Hunt

Sobell Department of Motor Neuroscience, University College London, London, United Kingdom

For correspondence
laurence.hunt@ucl.ac.uk

Competing interests
No competing interests declared.
Timothy EJ Behrens

Wellcome Trust Centre for Neuroimaging, University College London, London, United Kingdom

Competing interests
Timothy EJ Behrens, Senior editor, eLife.
Takayuki Hosokawa

Helen Wills Neuroscience Institute, Department of Psychology, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Jonathan D Wallis

Helen Wills Neuroscience Institute, Department of Psychology, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Steven Wayne Kennerley

Sobell Department of Motor Neuroscience, University College London, London, United Kingdom

Competing interests
No competing interests declared.

Ethics

Animal experimentation: Ethical approval was obtained for this study. All procedures were in accord with the National Institute of Health guidelines (Assurance Number A3084-01) and the recommendations of the U.C. Berkeley Animal Care and Use Committee (Protocol Number R283).

Human subjects: All human subjects provided informed consent, including consent to publish. Ethical approval for this study was obtained from NHS Oxfordshire Research Ethics Committee C, approval reference 08/H0606/46.

Copyright

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.