Selectivity for large nonmanipulable objects in scene-selective visual cortex does not require visual experience

Abstract

The principles that determine the organization of object representations in ventral temporal cortex (VTC) remain elusive. Here, we focus on the parahippocampal place area (PPA), a region in medial VTC that has been shown to respond selectively to pictures of scenes. Recent studies further observed that this region also shows a preference for large nonmanipulable objects relative to other objects, which might reflect the suitability of large objects for navigation. The mechanisms underlying this selectivity remain poorly understood. We examined the extent to which PPA selectivity requires visual experience. Fourteen congenitally blind and matched sighted participants were tested on an auditory size judgment experiment involving large nonmanipulable objects, small objects (tools), and animals. Sighted participants additionally participated in a picture-viewing experiment. Replicating previous work, we found that the PPA responded selectively to large nonmanipulable objects, relative to tools and animals, in the sighted group viewing pictures. Importantly, this selectivity was also observed in the auditory experiment in both sighted and congenitally blind groups. In both groups, selectivity for large nonmanipulable objects was additionally observed in the retrosplenial complex (RSC) and the transverse occipital sulcus (TOS), regions previously implicated in scene perception and navigation. Finally, in both groups the PPA showed resting-state functional connectivity with TOS and RSC. These results provide new evidence that large object selectivity in PPA, and the intrinsic connectivity between PPA and other navigation-relevant regions, do not require visual experience. More generally, they show that the organization of object representations in VTC can develop, at least partly, without visual experience.