Feature-specific prediction errors for visual mismatch

• Published in: NeuroImage (Orlando, Fla.) Vol. 196; pp. 142 - 151
• Main Authors: Stefanics, Gabor, Stephan, Klaas Enno, Heinzle, Jakob
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.08.2019; Elsevier Limited
• Subjects: Adult; Attention; Attention - physiology; Attention task; Bayes Theorem; Bayesian analysis; Brain - physiology; Brain Mapping; Cerebellum; Cognition; Color; Color perception; Color Perception - physiology; Computational neuroscience; Emotion recognition; Emotions; Facial Expression; Facial Recognition - physiology; Female; Functional magnetic resonance imaging; Humans; Magnetic Resonance Imaging; Male; Models, Neurological; Neural coding; Neural Pathways - physiology; Neuroimaging; Perception; Perceptual inference; Precision weighted prediction error; Prediction models; Predictive coding; Social environment; Visual perception; Young Adult; Perceptual inference; Predictive coding; Emotion recognition; Perception; Precision weighted prediction error; Color perception
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2019.04.020

Predictive coding (PC) theory posits that our brain employs a predictive model of the environment to infer the causes of its sensory inputs. A fundamental but untested prediction of this theory is that the same stimulus should elicit distinct precision weighted prediction errors (pwPEs) when different (feature-specific) predictions are violated, even in the absence of attention. Here, we tested this hypothesis using functional magnetic resonance imaging (fMRI) and a multi-feature roving visual mismatch paradigm where rare changes in either color (red, green), or emotional expression (happy, fearful) of faces elicited pwPE responses in human participants. Using a computational model of learning and inference, we simulated pwPE and prediction trajectories of a Bayes-optimal observer and used these to analyze changes in blood oxygen level dependent (BOLD) responses to changes in color and emotional expression of faces while participants engaged in a distractor task. Controlling for visual attention by eye-tracking, we found pwPE responses to unexpected color changes in the fusiform gyrus. Conversely, unexpected changes of facial emotions elicited pwPE responses in cortico-thalamo-cerebellar structures associated with emotion and theory of mind processing. Predictions pertaining to emotions activated fusiform, occipital and temporal areas. Our results are consistent with a general role of PC across perception, from low-level to complex and socially relevant object features, and suggest that monitoring of the social environment occurs continuously and automatically, even in the absence of attention. [Display omitted] •Changes in color or emotion of physically identical faces elicit prediction errors.•Prediction errors to such different features arise in distinct neuronal circuits.•Predictions pertaining to emotions are represented in multiple cortical areas.•Feature-specific prediction errors support predictive coding theories of perception.