Multivariate Patterns in Object-Selective Cortex Dissociate Perceptual and Physical Shape Similarity

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Abstract
Prior research has identified the lateral occipital complex (LOC) as a critical cortical region for the representation of object shape in humans. However, little is known about the nature of the representations contained in the LOC and their relationship to the perceptual experience of shape. We used human functional MRI to measure the physical, behavioral, and neural similarity between pairs of novel shapes to ask whether the representations of shape contained in subregions of the LOC more closely reflect the physical stimuli themselves, or the perceptual experience of those stimuli. Perceptual similarity measures for each pair of shapes were obtained from a psychophysical same-different task; physical similarity measures were based on stimulus parameters; and neural similarity measures were obtained from multivoxel pattern analysis methods applied to anterior LOC (pFs) and posterior LOC (LO). We found that the pattern of pairwise shape similarities in LO most closely matched physical shape similarities, whereas shape similarities in pFs most closely matched perceptual shape similarities. Further, shape representations were similar across participants in LO but highly variable across participants in pFs. Together, these findings indicate that activation patterns in subregions of object-selective cortex encode objects according to a hierarchy, with stimulus-based representations in posterior regions and subjective and observer-specific representations in anterior regions. As early as 1031 a.d., the Arab scholar Ibn al-Haytham suggested that visual experience was not veridical, but inherently subjective. During the last few decades, this observation has given rise to one of the core questions in visual neuroscience: how does the subjective experience of visual stimuli relate to their neural representations in the brain? It is well-known that visual shape is represented in a brain region called lateral occipital complex (LOC). However, do these representations reflect physical or perceptual stimulus characteristics? We presented observers with a set of complex visual stimuli and obtained three measures of similarity for these stimuli: a physical similarity measure based on stimulus parameters; a behavioral similarity measure based on discrimination performance; and finally a neural similarity measure based on multivariate pattern analyses in LOC. We found that in anterior LOC, neural stimulus similarities correlated with subjective perceptual similarities, but not with physical stimulus similarities; the reverse was true in posterior LOC. In addition, neural similarities were consistent across participants in posterior LOC, but highly variable across participants in anterior LOC. Together these findings suggest a two-part answer to the question of how cortical object representations relate to subjective experience: anterior regions appear to contain subjective, individually variable shape representations, whereas posterior regions contain stimulus-based shape representations.