Pupil diameter predicts changes in the exploration-exploitation trade-off: evidence for the adaptive gain theory

J Cogn Neurosci. 2011 Jul;23(7):1587-96. doi: 10.1162/jocn.2010.21548. Epub 2010 Jul 28.

Abstract

The adaptive regulation of the balance between exploitation and exploration is critical for the optimization of behavioral performance. Animal research and computational modeling have suggested that changes in exploitative versus exploratory control state in response to changes in task utility are mediated by the neuromodulatory locus coeruleus-norepinephrine (LC-NE) system. Recent studies have suggested that utility-driven changes in control state correlate with pupil diameter, and that pupil diameter can be used as an indirect marker of LC activity. We measured participants' pupil diameter while they performed a gambling task with a gradually changing payoff structure. Each choice in this task can be classified as exploitative or exploratory using a computational model of reinforcement learning. We examined the relationship between pupil diameter, task utility, and choice strategy (exploitation vs. exploration), and found that (i) exploratory choices were preceded by a larger baseline pupil diameter than exploitative choices; (ii) individual differences in baseline pupil diameter were predictive of an individual's tendency to explore; and (iii) changes in pupil diameter surrounding the transition between exploitative and exploratory choices correlated with changes in task utility. These findings provide novel evidence that pupil diameter correlates closely with control state, and are consistent with a role for the LC-NE system in the regulation of the exploration-exploitation trade-off in humans.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Psychological / physiology
  • Adolescent
  • Adult
  • Choice Behavior / physiology
  • Exploratory Behavior / physiology*
  • Female
  • Games, Experimental*
  • Humans
  • Learning / physiology
  • Locus Coeruleus / physiology*
  • Male
  • Models, Psychological
  • Norepinephrine / physiology
  • Predictive Value of Tests
  • Pupil / physiology*
  • Reflex, Pupillary / physiology*
  • Young Adult

Substances

  • Norepinephrine