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Responses of human frontal cortex to surprising events are predicted by formal associative learning theory

Abstract

Learning depends on surprise and is not engendered by predictable occurrences. In this functional magnetic resonance imaging (fMRI) study of causal associative learning, we show that dorsolateral prefrontal cortex (DLPFC) is associated specifically with the adjustment of inferential learning on the basis of unpredictability. At the outset, when all associations were unpredictable, DLPFC activation was maximal. This response attenuated with learning but, subsequently, activation here was evoked by surprise violations of the learned association. Furthermore, the magnitude of DLPFC response to a surprise event was sensitive to the relationship that had been learned and was predictive of subsequent behavioral change. In short, the physiological response properties of right DLPFC satisfied specific predictions made by associative learning theory.

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Figure 1
Figure 2: Subjects' predictive tendencies on the three types of associative relationship.
Figure 3: Functional neuroimaging findings.

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Acknowledgements

We thank H. Matute, F. Arcediano and R.R. Miller for allowing us to use their drug and syndrome names. We also thank J.D. Pickard and members of the Wolfson Brain Imaging Center, Addenbrooke's Hospital, Cambridge. P.C.F. is supported by the Wellcome Trust. D.R.S. is supported by the UK Biotech and Biological Sciences Research Council.

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Correspondence to P. C. Fletcher.

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Fletcher, P., Anderson, J., Shanks, D. et al. Responses of human frontal cortex to surprising events are predicted by formal associative learning theory. Nat Neurosci 4, 1043–1048 (2001). https://doi.org/10.1038/nn733

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