Stimulus effects dwarf task effects in human visual cortex

Abstract

Task context affects stimulus representations in human visual cortex, suggesting that visual representations are flexible. However, this interpretation is at odds with a major computational goal of the human visual system: creating a perceptually stable representation of the external visual environment. How does the visual system balance stability and flexibility? Here, human participants (71 percent females) categorized object images and written words according to different task rules, while brain responses were measured with fMRI. Using an ANOVA-based modeling strategy, we precisely quantified the relative contributions of stimulus, task, and their interaction in explaining representational variance across the cortical hierarchy. Our results show that stimulus effects account for the overwhelming majority of explainable representational variance across the ventral visual system: > 95 percent in V1 and V2, and > 90 percent in higher-level visual cortex. In prefrontal cortex, the relative contributions reverse: task effects dominate stimulus effects, accounting for 80 percent of explainable representational variance. In parietal cortex, contributions of stimulus and task are approximately equal. Our findings suggest that population coding in sensory cortex is optimized for representational stability to allow a consistent interpretation of the external environment. Population coding in parietal and frontal multiple-demand cortex, by contrast, is optimized for representational flexibility to accommodate changing behavioral goals and support flexible cognition and action. Significance statementStimulus representations in human visual cortex are affected by behavioral goals and are therefore thought to be flexible. However, this view is inconsistent with a major computational goal of the human visual system: creating a perceptually stable representation of the external environment. Here, we show that modulatory effects of behavioral goals on stimulus representations in visual cortex are surprisingly small. In contrast, behavioral goals strongly affect representations in parietal and frontal multiple-demand cortex. Our findings suggest that population coding in sensory cortex is optimized for stable perception, while population coding in parietal and frontal multiple-demand cortex is optimized for flexible cognition.