Pupil dilation signals uncertainty and surprise in a learning gambling task

Claudio Lavín,Eduardo Rosales Jubal,René San Martín

doi:10.3389/fnbeh.2013.00218

Abstract

Pupil dilation under constant illumination is a physiological marker where modulation is related to several cognitive functions involved in daily decision making. There is evidence for a role of pupil dilation change during decision-making tasks associated with uncertainty, reward-prediction errors and surprise. However, while some work suggests that pupil dilation is mainly modulated by reward predictions, others point out that this marker is related to uncertainty signaling and surprise. Supporting the latter hypothesis, the neural substrate of this marker is related to noradrenaline (NA) activity which has been also related to uncertainty signaling. In this work we aimed to test whether pupil dilation is a marker for uncertainty and surprise in a learning task. We recorded pupil dilation responses in 10 participants performing the Iowa Gambling Task (IGT), a decision-making task that requires learning and constant monitoring of outcomes’ feedback, which are important variables within the traditional study of human decision making. Results showed that pupil dilation changes were modulated by learned uncertainty and surprise regardless of feedback magnitudes. Interestingly, greater pupil dilation changes were found during positive feedback (PF) presentation when there was lower uncertainty about a future negative feedback (NF); and by surprise during NF presentation. These results support the hypothesis that pupil dilation is a marker of learned uncertainty, and may be used as a marker of NA activity facing unfamiliar situations in humans.

Highlights

Deciding is a daily activity that involves a series of complex cognitive processes
Pupil dilation has been linked to Locus Coeruleus (LC)— Noradrenaline (NA) activity (Aston-Jones and Cohen, 2005; Einhauser et al, 2008; Jepma and Nieuwenhuis, 2011; Kuipers and Thierry, 2011) which in turn has been related to uncertainty signaling (Rajkowski et al, 1994; Yu and Dayan, 2005)
While some evidence indicates that there is greater pupil dilation facing uncertainty, violation of expectations and negative outcome feedback (Satterthwaite et al, 2007), others using different tasks point out that pupil dilation changes are greater facing less uncertainty regardless of outcome valence (Preuschoff et al, 2011). This second interpretation is in line with the mentioned role of NA in uncertainty signaling, and suggests that as dopamine plays an important role in the reward pathway (Holroyd and Coles, 2002), NA is involved in a less studied circuit of uncertainty signaling involved in the learning processes of decision making in unknown environments (Nieuwenhuis et al, 2005; Yu and Dayan, 2005; Preuschoff et al, 2011; Payzan-Lenestour et al, 2013)

Summary

Introduction

Deciding is a daily activity that involves a series of complex cognitive processes. The complexities are related to the lack of information and unknown environments that people usually face when making decisions. While some evidence indicates that there is greater pupil dilation facing uncertainty, violation of expectations and negative outcome feedback (Satterthwaite et al, 2007), others using different tasks point out that pupil dilation changes are greater facing less uncertainty regardless of outcome valence (Preuschoff et al, 2011) This second interpretation is in line with the mentioned role of NA in uncertainty signaling, and suggests that as dopamine plays an important role in the reward pathway (Holroyd and Coles, 2002), NA is involved in a less studied circuit of uncertainty signaling involved in the learning processes of decision making in unknown environments (Nieuwenhuis et al, 2005; Yu and Dayan, 2005; Preuschoff et al, 2011; Payzan-Lenestour et al, 2013). In order to test this hypothesis, we studied pupil dilation responses in the Iowa Gambling Task (IGT; Bechara et al, 1994), a decision-making task that requires active learning from participants

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Conclusion