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Attention promotes the neural encoding of prediction errors

Cooper A Smout, Matthew F Tang, Marta I Garrido and Jason B Mattingley

PLOS Biology, 2019, vol. 17, issue 2, 1-22

Abstract: The encoding of sensory information in the human brain is thought to be optimised by two principal processes: ‘prediction’ uses stored information to guide the interpretation of forthcoming sensory events, and ‘attention’ prioritizes these events according to their behavioural relevance. Despite the ubiquitous contributions of attention and prediction to various aspects of perception and cognition, it remains unknown how they interact to modulate information processing in the brain. A recent extension of predictive coding theory suggests that attention optimises the expected precision of predictions by modulating the synaptic gain of prediction error units. Because prediction errors code for the difference between predictions and sensory signals, this model would suggest that attention increases the selectivity for mismatch information in the neural response to a surprising stimulus. Alternative predictive coding models propose that attention increases the activity of prediction (or ‘representation’) neurons and would therefore suggest that attention and prediction synergistically modulate selectivity for ‘feature information’ in the brain. Here, we applied forward encoding models to neural activity recorded via electroencephalography (EEG) as human observers performed a simple visual task to test for the effect of attention on both mismatch and feature information in the neural response to surprising stimuli. Participants attended or ignored a periodic stream of gratings, the orientations of which could be either predictable, surprising, or unpredictable. We found that surprising stimuli evoked neural responses that were encoded according to the difference between predicted and observed stimulus features, and that attention facilitated the encoding of this type of information in the brain. These findings advance our understanding of how attention and prediction modulate information processing in the brain, as well as support the theory that attention optimises precision expectations during hierarchical inference by increasing the gain of prediction errors.Author summary: The human brain is theorised to operate like a sophisticated hypothesis tester, using past experience to generate a model of the external world, testing predictions of this model against incoming sensory evidence, and generating a ‘prediction error’ signal that updates the model when predictions and sensory evidence do not match. In addition to predicting the content of sensory signals, an optimal system should also predict the reliability (or ‘precision’) of those signals to minimise the influence of unreliable sensory information. It has been proposed that attention optimises this process by boosting prediction error signals, which are coded as the difference (or ‘mismatch’) between predicted and observed stimulus features. Accordingly, this theory predicts that attention should increase the selectivity for mismatch information in the neural response to surprising stimuli. We tested this hypothesis in human participants by training a decoding algorithm to identify ‘mismatch information’ in the brain, recorded by electroencephalography (EEG), following the presentation of surprising stimuli that were either attended or ignored. We found that attention did indeed increase the selectivity for mismatch information in the neural response, supporting the notion that attention and prediction are intricately related processes.

Date: 2019
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pbio00:2006812

DOI: 10.1371/journal.pbio.2006812

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