Attention promotes the neural encoding of prediction errors

• Published in: PLoS biology 2019-02, Vol.17 (2), p.e2006812-e2006812
• Main Authors: Smout, Cooper A, Tang, Matthew F, Garrido, Marta I, Mattingley, Jason B
• Format: Article
• Language: English
• Subjects: Adolescent; Adult; Analysis; Attention; Attention - physiology; Biology and Life Sciences; Brain; Brain - physiology; Brain research; Coding; Coding theory; Cognition; Councils; Data processing; EEG; Electroencephalography; Encoding (Memory); Evoked Potentials - physiology; Female; Human performance; Humans; Hypotheses; Information processing; Male; Medicine and Health Sciences; Memory; Methods; Middle Aged; Neural coding; Neurons; Photic Stimulation; Physical Sciences; Predictions; Research and Analysis Methods; Selectivity; Senses and sensation; Social Sciences; Stimuli; Supervision; Time Factors; Visual observation; Visual tasks; Young Adult
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.2006812

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.