title: Surprise signals in the supplementary eye field: rectified prediction errors drive exploration-exploitation transitions.
abstract: Visual search is coordinated adaptively by monitoring and predicting the environment. The supplementary eye field (SEF) plays a role in oculomotor control and outcome evaluation. However, it is not clear whether the SEF is involved in adjusting behavioral modes based on preceding feedback. We hypothesized that the SEF drives exploration-exploitation transitions by generating "surprise signals" or rectified prediction errors, which reflect differences between predicted and actual outcomes. To test this hypothesis, we introduced an oculomotor two-target search task in which monkeys were required to find two valid targets among four identical stimuli. After they detected the valid targets, they exploited their knowledge of target locations to obtain a reward by choosing the two valid targets alternately. Behavioral analysis revealed two distinct types of oculomotor search patterns: exploration and exploitation. We found that two types of SEF neurons represented the surprise signals. The error-surprise neurons showed enhanced activity when the monkey received the first error feedback after the target pair change, and this activity was followed by an exploratory oculomotor search pattern. The correct-surprise neurons showed enhanced activity when the monkey received the first correct feedback after an error trial, and this increased activity was followed by an exploitative, fixed-type search pattern. Our findings suggest that error-surprise neurons are involved in the transition from exploitation to exploration and that correct-surprise neurons are involved in the transition from exploration to exploitation.
authors.affiliation: Department of Physiology, Tohoku University School of Medicine, Seiryo-machi, Aoba-ku, Sendai, Japan; Department of Neurology, Tohoku University School of Medicine, Seiryo-machi, Aoba-ku, Sendai, Japan;
authors.forename: Norihiko
authors.initials: N
authors.lastname: Kawaguchi
authors.affiliation: Research Institute of Electrical Communication, Tohoku University, Katahira, Aoba-ku, Sendai, Japan; and.
authors.forename: Kazuhiro
authors.initials: K
authors.lastname: Sakamoto
authors.affiliation: Department of Physiology, Tohoku University School of Medicine, Seiryo-machi, Aoba-ku, Sendai, Japan;
authors.forename: Naohiro
authors.initials: N
authors.lastname: Saito
authors.affiliation: Department of Physiology, Tohoku University School of Medicine, Seiryo-machi, Aoba-ku, Sendai, Japan;
authors.forename: Yoshito
authors.initials: Y
authors.lastname: Furusawa
authors.affiliation: Department of Physiology, Tohoku University School of Medicine, Seiryo-machi, Aoba-ku, Sendai, Japan;
authors.forename: Jun
authors.initials: J
authors.lastname: Tanji
authors.affiliation: Department of Neurology, Tohoku University School of Medicine, Seiryo-machi, Aoba-ku, Sendai, Japan;
authors.forename: Masashi
authors.initials: M
authors.lastname: Aoki
authors.affiliation: Department of Physiology, Tohoku University School of Medicine, Seiryo-machi, Aoba-ku, Sendai, Japan; Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Tokyo, Japan hmushiak@med.tohoku.ac.jp.
authors.forename: Hajime
authors.initials: H
authors.lastname: Mushiake
mesh_terms: D000818:Animals; D005106:Exploratory Behavior; D025461:Feedback, Physiological; D005625:Frontal Lobe / Q000166:cytology / Q000502:physiology*; D008251:Macaca; D009474:Neurons / Q000502:physiology; D014796:Visual Perception
keywords: exploration-exploitation transition; monkey; oculomotor search; supplementary eye field; surprise signal