Expectation and Surprise Determine Neural Population Responses in the Ventral Visual Stream

• Published in: The Journal of neuroscience Vol. 30; no. 49; pp. 16601 - 16608
• Main Authors: Egner, Tobias, Monti, Jim M., Summerfield, Christopher
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 08.12.2010
• Subjects: Adult; Analysis of Variance; Brain Mapping; Computer Simulation; Female; Humans; Image Processing, Computer-Assisted - methods; Magnetic Resonance Imaging - methods; Male; Models, Neurological; Oxygen - blood; Photic Stimulation - methods; Predictive Value of Tests; Reaction Time - physiology; Sensory Receptor Cells - physiology; Signal Detection, Psychological - physiology; Visual Cortex - blood supply; Visual Cortex - cytology; Visual Cortex - physiology; Visual Pathways - blood supply; Visual Pathways - physiology; Visual Perception - physiology; Young Adult
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.2770-10.2010

Visual cortex is traditionally viewed as a hierarchy of neural feature detectors, with neural population responses being driven by bottom-up stimulus features. Conversely, “predictive coding” models propose that each stage of the visual hierarchy harbors two computationally distinct classes of processing unit: representational units that encode the conditional probability of a stimulus and provide predictions to the next lower level; and error units that encode the mismatch between predictions and bottom-up evidence, and forward prediction error to the next higher level. Predictive coding therefore suggests that neural population responses in category-selective visual regions, like the fusiform face area (FFA), reflect a summation of activity related to prediction (“face expectation”) and prediction error (“face surprise”), rather than a homogenous feature detection response. We tested the rival hypotheses of the feature detection and predictive coding models by collecting functional magnetic resonance imaging data from the FFA while independently varying both stimulus features (faces vs houses) and subjects' perceptual expectations regarding those features (low vs medium vs high face expectation). The effects of stimulus and expectation factors interacted, whereby FFA activity elicited by face and house stimuli was indistinguishable under high face expectation and maximally differentiated under low face expectation. Using computational modeling, we show that these data can be explained by predictive coding but not by feature detection models, even when the latter are augmented with attentional mechanisms. Thus, population responses in the ventral visual stream appear to be determined by feature expectation and surprise rather than by stimulus features per se.