Pupil dilation signals uncertainty and surprise in a learning gambling task

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.

[1]  A. Savitzky,et al.  Smoothing and Differentiation of Data by Simplified Least Squares Procedures. , 1964 .

[2]  J. Beatty Task-evoked pupillary responses, processing load, and the structure of processing resources. , 1982, Psychological bulletin.

[3]  J. Beatty,et al.  The pupil and stimulus probability. , 1985, Psychophysiology.

[4]  L. Walrath,et al.  Eye movement and pupillary response indices of mental workload during visual search of symbolic displays. , 1992, Applied ergonomics.

[5]  G. Aston-Jones,et al.  Locus coeruleus activity in monkey: Phasic and tonic changes are associated with altered vigilance , 1994, Brain Research Bulletin.

[6]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[7]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[8]  E. Granholm,et al.  Pupillary responses index cognitive resource limitations. , 1996, Psychophysiology.

[9]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[10]  Gregory G. Brown,et al.  Brain activation and pupil response during covert performance of the Stroop Color Word task , 1999, Journal of the International Neuropsychological Society.

[11]  Adrian R. Willoughby,et al.  The Medial Frontal Cortex and the Rapid Processing of Monetary Gains and Losses , 2002, Science.

[12]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[13]  Wolzt,et al.  World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. , 2003, The Journal of the American College of Dentists.

[14]  Christiane,et al.  World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. , 2004, Journal international de bioethique = International journal of bioethics.

[15]  E. Weber,et al.  Predicting Risk-Sensitivity in Humans and Lower Animals: Risk as Variance or Coefficient of Variation , 2004, Psychological review.

[16]  E. Crone,et al.  Heart rate and skin conductance analysis of antecendents and consequences of decision making. , 2004, Psychophysiology.

[17]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[18]  Angela J. Yu,et al.  Uncertainty, Neuromodulation, and Attention , 2005, Neuron.

[19]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

[20]  José M. Martínez-Selva,et al.  Mecanismos cerebrales de la toma de decisiones , 2006 .

[21]  A. Bechara,et al.  [Brain mechanisms involved in decision-making]. , 2006, Revista de neurologia.

[22]  Johannes Hewig,et al.  Decision-making in Blackjack: an electrophysiological analysis. , 2007, Cerebral cortex.

[23]  Theodore D. Satterthwaite,et al.  Dissociable but inter-related systems of cognitive control and reward during decision making: Evidence from pupillometry and event-related fMRI , 2007, NeuroImage.

[24]  S. Steinhauer,et al.  Blink before and after you think: blinks occur prior to and following cognitive load indexed by pupillary responses. , 2008, Psychophysiology.

[25]  C. Koch,et al.  Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry , 2008, Proceedings of the National Academy of Sciences.

[26]  Zhong-Lin Lu,et al.  Neural correlates of risk prediction error during reinforcement learning in humans , 2009, NeuroImage.

[27]  Peter N. C. Mohr,et al.  Neural Processing of Risk , 2010, The Journal of Neuroscience.

[28]  Tinka Welke,et al.  I spy with my little eye: detection of temporal violations in event sequences and the pupillary response. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[29]  W. Einhäuser,et al.  Pupil Dilation Signals Surprise: Evidence for Noradrenaline’s Role in Decision Making , 2011, Front. Neurosci..

[30]  Sander Nieuwenhuis,et al.  Pupil Diameter Predicts Changes in the Exploration–Exploitation Trade-off: Evidence for the Adaptive Gain Theory , 2011, Journal of Cognitive Neuroscience.

[31]  Guillaume Thierry,et al.  N400 Amplitude Reduction Correlates with an Increase in Pupil Size , 2011, Front. Hum. Neurosci..

[32]  Peter Bossaerts,et al.  The Neural Representation of Unexpected Uncertainty during Value-Based Decision Making , 2013, Neuron.