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The Journal of Neuroscience, March 12, 2008, 28(11):2745-2752; doi:10.1523/JNEUROSCI.4286-07.2008

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Behavioral/Systems/Cognitive
Human Insula Activation Reflects Risk Prediction Errors As Well As Risk

Kerstin Preuschoff,^1,4 Steven R. Quartz,^1,2 and Peter Bossaerts^1,2,3

¹Computation and Neural Systems Program and ²Division of Humanities and Social Sciences, Caltech, Pasadena, California 91125, ³Ecole Polytechnique Fédérale Lausanne, CH-1015 Lausanne, Switzerland, and ⁴Institute for Empirical Research in Economics, University of Zurich, CH-8006 Zurich, Switzerland

Correspondence should be addressed to Kerstin Preuschoff, Institute for Empirical Research in Economics, Bluemlisalpstrasse 10, CH-8006 Zurich, Switzerland.

Understanding how organisms deal with probabilistic stimulus-reward associations has been advanced by a convergence between reinforcement learning models and primate physiology, which demonstrated that the brain encodes a reward prediction error signal. However, organisms must also predict the level of risk associated with reward forecasts, monitor the errors in those risk predictions, and update these in light of new information. Risk prediction serves a dual purpose: (1) to guide choice in risk-sensitive organisms and (2) to modulate learning of uncertain rewards. To date, it is not known whether or how the brain accomplishes risk prediction. Using functional imaging during a simple gambling task in which we constantly changed risk, we show that an early-onset activation in the human insula correlates significantly with risk prediction error and that its time course is consistent with a role in rapid updating. Additionally, we show that activation previously associated with general uncertainty emerges with a delay consistent with a role in risk prediction. The activations correlating with risk prediction and risk prediction errors are the analogy for risk of activations correlating with reward prediction and reward prediction errors for reward expectation. As such, our findings indicate that our understanding of the neural basis of reward anticipation under uncertainty needs to be expanded to include risk prediction.

Key words: risk prediction; insula; risk; uncertainty; reinforcement learning; reward prediction

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Received Sept. 19, 2007; revised Jan. 11, 2008; accepted Jan. 14, 2008.

Correspondence should be addressed to Kerstin Preuschoff, Institute for Empirical Research in Economics, Bluemlisalpstrasse 10, CH-8006 Zurich, Switzerland.

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