A New Role for the Parahippocampal Cortex in Representing Space

Abstract

The debate surrounding the function of the human posterior parahippocampal cortex (PHC) is currently dominated by two competing theories. The spatial layout hypothesis proposes that PHC processes information about the shape of space embodied in layout-defining scene features. The contextual association hypothesis rejects this notion, proposing instead that PHC responds to highly contextualized, but not necessarily spatial, stimuli. Here we present a novel concept that suggests PHC is primarily concerned with any representation that depicts three-dimensional local space, be it scenes or even single objects. Specifically, we identified space-defining (SD) and space-ambiguous (SA) single objects, where SD objects consistently evoke a strong sense of the surrounding space while SA objects do not, in the absence of any background, spatial layout, or context. We found that participants could easily identify and distinguish between SD and SA objects. This distinction was subsequently affirmed at a neural level, where visualizing or viewing single SD objects compared with SA objects engaged PHC, despite these single SD objects offering no information about the shape or layout of the space. Moreover, this PHC response was robust and not accounted for by other factors, including contextual associations. Instead, it was linked to intrinsic object properties, specifically a combination of perceived object size and portability. By showing that PHC is responsive to the awareness of surrounding local space suggests its role in scene processing is basic and fundamental, such that it is not dependent on complex scene properties such as geometric structure, scene schema, or contextual associations.