Principles of coarse-scale functional organization in occipitotemporal cortex

Occipitotemporal cortex is known to process visually-perceived objects, but identifying general principles underlying its coarse-scale functional organization has remained challenging for two reasons. First, much previous work has left open whether proposed organizational dimensions, such as animacy or real-world size, are useful for characterizing high-level vision and to what degree they would generalize to more diverse and naturalistic stimuli. Second, many natural object properties are highly intercorrelated, making it challenging to determine which dimensions, if any, dominate the coarse-scale representational organization of the visual system. To address these challenges, we carried out detailed analyses of the cortical topography underlying 15 object properties, using a densely-sampled fMRI dataset with responses to thousands of natural images. We focused our investigation around the properties animacy and real-world size, given their established prominence as candidate organizational dimensions. While our results confirm many characteristics of the purported animacy-size organization, they revealed distinctions that challenge dominant notions of this organization, highlighting the importance of generalizing to large-scale naturalistic data. Moving beyond animacy and size, our results demonstrate that many of the 15 candidate properties can alternatively serve as organizational dimensions underlying the coarse-scale functional topography of occipitotemporal cortex, but that none of them clearly stand out in the representational organization. This suggests that trying to reduce the coarse-scale functional organization of occipitotemporal cortex to individual conceptual dimensions may be the wrong goal. Rather, our results suggest that occipitotemporal cortex may provide a foundation for the flexible read-out of a wide range of object properties. SignificanceThere has been a long tradition in cognitive neuroscience of reducing brain response profiles to a small number of unifying principles. The extent to which this approach also applies to the structure of representations remains largely untested. Using the widely discussed putative organizational principles of animacy and size as test cases, we examined their generality using densely-sampled fMRI data and behavioral ratings along 15 object properties. Our results demonstrate a more complex organization of animacy and size representations than assumed by prevailing accounts, and hierarchical partitioning revealed that none of the 15 properties dominated representations. These findings challenge the pivotal role often assigned to individual properties, indicating that the dominant approach oversimplifies the role of individual principles in visual representations.