Exploration Disrupts Choice-Predictive Signals and Alters Dynamics in Prefrontal Cortex

R. Becket Ebitz, Eddy Albarran, Tirin Moore

Research output: Contribution to journalArticlepeer-review

16 Scopus citations

Abstract

In uncertain environments, decision-makers must balance two goals: they must “exploit” rewarding options but also “explore” in order to discover rewarding alternatives. Exploring and exploiting necessarily change how the brain responds to identical stimuli, but little is known about how these states, and transitions between them, change how the brain transforms sensory information into action. To address this question, we recorded neural activity in a prefrontal sensorimotor area while monkeys naturally switched between exploring and exploiting rewarding options. We found that exploration profoundly reduced spatially selective, choice-predictive activity in single neurons and delayed choice-predictive population dynamics. At the same time, reward learning was increased in brain and behavior. These results indicate that exploration is related to sudden disruptions in prefrontal sensorimotor control and rapid, reward-dependent reorganization of control dynamics. This may facilitate discovery through trial and error. Exploratory choices permit the discovery of new rewarding options. Ebitz et al. report that spatially selective, choice-predictive neurons in the prefrontal cortex do not predict choice before exploratory decisions. Reduced prefrontal control may underlie flexible decision-making and trial-and-error discovery.

Original languageEnglish (US)
Pages (from-to)450-461.e9
JournalNeuron
Volume97
Issue number2
DOIs
StatePublished - Jan 17 2018

Bibliographical note

Funding Information:
The authors would like to thank Daniel Takahashi, Tatiana Engel, Sam McClure, and Nathaniel Daw for invaluable scientific discussion; Alireza Soltani, Marc Zirnsak, Becca Krock, and Nick Steinmetz for technical help; Ben Hayden, Tim Buschman, and Vince McGinty for comments on the manuscript; and Shellie Hyde and Doug Aldrich for assistance with animal care and husbandry. Support was provided by the National Eye Institute (R01-EY014924) and a NEI T32 postdoctoral training grant, a NIMH NRSA (F32-MH102049), and a CV Starr Foundation Fellowship to R.B.E.

Publisher Copyright:
© 2017 Elsevier Inc.

Keywords

  • attention
  • control dynamics
  • decision-making
  • exploration
  • frontal eye fields
  • goal states
  • indeterminacy
  • learning
  • prefrontal cortex
  • sensorimotor control

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