The “Parahippocampal Place Area” Responds Preferentially to High Spatial Frequencies in Humans and Monkeys

Abstract

Defining the exact mechanisms by which the brain processes visual objects and scenes remains an unresolved challenge. Valuable clues to this process have emerged from the demonstration that clusters of neurons (“modules”) in inferior temporal cortex apparently respond selectively to specific categories of visual stimuli, such as places/scenes. However, the higher-order “category-selective” response could also reflect specific lower-level spatial factors. Here we tested this idea in multiple functional MRI experiments, in humans and macaque monkeys, by systematically manipulating the spatial content of geometrical shapes and natural images. These tests revealed that visual spatial discontinuities (as reflected by an increased response to high spatial frequencies) selectively activate a well-known place-selective region of visual cortex (the “parahippocampal place area”) in humans. In macaques, we demonstrate a homologous cortical area, and show that it also responds selectively to higher spatial frequencies. The parahippocampal place area may use such information for detecting object borders and scene details during spatial perception and navigation. Many reports suggest that different categories of visual stimuli are processed in correspondingly specific “modules” in the visual cortex. For instance, images of faces are processed in one cortical module (the “fusiform face area”), while images of scenes are processed in an adjacent module (the “parahippocampal place area,” or PPA). How does the PPA encode for such high-level, complex visual scenes? In this study, we show that at least part of the PPA response is due to a lower-level variable, reflected as higher spatial frequencies. These are prominent in the edges and details of scenes, but less prominent in faces and other stimuli. When we altered standard images of faces and places so that they only contained low, medium, or high spatial frequencies, we found that the PPA responded strongly to images containing high spatial frequencies. Importantly, using the same stimuli as for the human studies, we also demonstrated a homolog of human PPA in macaque temporal cortex (“mPPA”). As in humans, mPPA responds selectively to higher spatial frequencies. This demonstration of PPA in macaques paves the way for carrying out further electrophysiological and anatomical studies that may help elucidate the neural mechanisms for place selectivity in the human visual cortex.