Tonic exploration governs both flexibility and lapses

R. Becket Ebitz, Brianna J. Sleezer, Hank P. Jedema, Charles W. Bradberry, Benjamin Y. Hayden

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

In many cognitive tasks, lapses (spontaneous errors) are tacitly dismissed as the result of nuisance processes like sensorimotor noise, fatigue, or disengagement. However, some lapses could also be caused by exploratory noise: randomness in behavior that facilitates learning in changing environments. If so, then strategic processes would need only up-regulate (rather than generate) exploration to adapt to a changing environment. This view predicts that more frequent lapses should be associated with greater flexibility because these behaviors share a common cause. Here, we report that when rhesus macaques performed a set-shifting task, lapse rates were negatively correlated with perseverative error frequency across sessions, consistent with a common basis in exploration. The results could not be explained by local failures to learn. Furthermore, chronic exposure to cocaine, which is known to impair cognitive flexibility, did increase perseverative errors, but, surprisingly, also improved overall set-shifting task performance by reducing lapse rates. We reconcile these results with a state-switching model in which cocaine decreases exploration by deepening attractor basins corresponding to rule states. These results support the idea that exploratory noise contributes to lapses, affecting rule-based decision-making even when it has no strategic value, and suggest that one key mechanism for regulating exploration may be the depth of rule states.

Original languageEnglish (US)
Article numbere1007475
JournalPLoS computational biology
Volume15
Issue number11
DOIs
StatePublished - 2019

Bibliographical note

Funding Information:
Support provided by the National Institute on Drug Abuse (R01-DA038106, https://www.drugabuse.gov/) and the Brain & Behavior Research Foundation (NARSAD awards to BYH and RBE, https://www.bbrfoundation.org/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Publisher Copyright:
This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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