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The ability to use environmental stimuli to predict impending harm is critical for survival. Such predictions should be available as early as they are reliable. In pavlovian conditioning, chains of successively earlier predictors are studied in terms of higher-order relationships, and have inspired computational theories such as temporal difference learning. However, there is at present no adequate neurobiological account of how this learning occurs. Here, in a functional magnetic resonance imaging (fMRI) study of higher-order aversive conditioning, we describe a key computational strategy that humans use to learn predictions about pain. We show that neural activity in the ventral striatum and the anterior insula displays a marked correspondence to the signals for sequential learning predicted by temporal difference models. This result reveals a flexible aversive learning process ideally suited to the changing and uncertain nature of real-world environments. Taken with existing data on reward learning, our results suggest a critical role for the ventral striatum in integrating complex appetitive and aversive predictions to coordinate behaviour.

Original publication

DOI

10.1038/nature02581

Type

Journal article

Journal

Nature

Publication Date

06/2004

Volume

429

Pages

664 - 667

Addresses

Wellcome Department of Imaging Neuroscience, 12 Queen Square, London WC1N 3BG, UK. bseymour@fil.ion.ucl.ac.uk

Keywords

Hand, Neostriatum, Humans, Pain, Magnetic Resonance Imaging, Electric Stimulation, Learning, Conditioning, Classical, Cues, Punishment, Models, Neurological, Time Factors