The occipital place area represents the local elements of scenes

Abstract

Neuroimaging studies have identified three scene-selective regions in human cortex: parahippocampal place area (PPA), retrosplenial complex (RSC), and occipital place area (OPA). However, precisely what scene information each region represents is not clear, especially for the least studied, more posterior OPA. Here we hypothesized that OPA represents local elements of scenes within two independent, yet complementary scene descriptors: spatial boundary (i.e., the layout of external surfaces) and scene content (e.g., internal objects). If OPA processes the local elements of spatial boundary information, then it should respond to these local elements (e.g., walls) themselves, regardless of their spatial arrangement. Indeed, we found that OPA, but not PPA or RSC, responded similarly to images of intact rooms and these same rooms in which the surfaces were fractured and rearranged, disrupting the spatial boundary. Next, if OPA represents the local elements of scene content information, then it should respond more when more such local elements (e.g., furniture) are present. Indeed, we found that OPA, but not PPA or RSC, responded more to multiple than single pieces of furniture. Taken together, these findings reveal that OPA analyzes local scene elements - both in spatial boundary and scene content representation - while PPA and RSC represent global scene properties.

Keywords: OPA; Parahippocampal Place Area (PPA); Retrosplenial Complex; Scene perception; Transverse Occipital Sulcus (TOS); fMRI.

Figure 1

Scene-selective regions of interest (ROIs) in a sample participant. Occipital Place Area (OPA), Parahippocampal Place Area (PPA), and Retrosplenial Complex (RSC), labeled accordingly. Using ‘Localizer’ scans, these ROIs were selected as those regions responding significantly more to scenes than objects (p < 0.0001, uncorrected). Responses of these ROIs to the experimental conditions were then tested using an independent set of data (Experimental scans).

Figure 2

Example stimuli used in the Experimental scans. From top row to bottom row: 1) intact, empty apartment rooms (intact rooms); 2) indoor rooms whose walls, floors, and ceilings were fractured and rearranged such that they no longer defined a coherent space (fractured rooms); 3) single, non-furniture objects (single objects); 4) single pieces of furniture (single furniture); and 5) multiple pieces of furniture (multiple furniture).

Figure 3

Average percent signal change in OPA, PPA, and RSC to the five conditions. Error bars indicate the standard error of the mean. (A) Spatial boundary representation in OPA, PPA, and RSC. A 3 (ROI: OPA, PPA, RSC) × 2 (room type: intact, fractured) repeated measures ANOVA revealed a significant interaction (F_{(2, 42)} = 33.66, p < 0.001), with OPA responding significantly more to fractured rooms relative to intact rooms, compared with both PPA and RSC (interaction contrasts, both p values < 0.001). (B) Scene content representation in OPA, PPA, and RSC. A 3 (ROI: OPA, PPA, RSC) × 3 (condition: single objects, single furniture, multiple furniture) repeated-measures ANOVA revealed a significant interaction (F_{(4, 84)} = 14.579, p < 0.001). In particular, both OPA and PPA responded more to single furniture than to single objects, relative to RSC (interaction contrasts, both p values < 0.005), and OPA responded more to multiple furniture than to single furniture, relative to both PPA and RSC (interaction contrasts, both p values < 0.05).

Figure 4

(A) Average percent signal change in OPA and FC to the five conditions. Error bars indicate the standard error of the mean. A 2 (ROI: OPA, FC) × 5 (condition: intact rooms, fractured rooms, single objects, single furniture, multiple furniture) repeated measures ANOVA revealed a significant interaction (F_(4,84) = 62.03, p < 0.001), indicating that the pattern of responses in OPA was not as expected for a retinotopic region. (B) Distribution of low (10% energy) and high (90% energy) spatial frequency information across the five conditions. (C) Average percent spatial envelope coverage in each condition. Importantly, while our stimuli were not precisely matched for spatial frequency content or spatial envelope coverage, none of these sources of low-level visual information predicts the pattern of responses observed in OPA.

Figure 5

Average percent signal change in OPA and object-selective LOC for all five conditions. Error bars depict the standard error of the mean. A 2 (ROI: OPA, LOC) × 5 (Condition: Intact rooms, Fractured Rooms, Single Objects, Single Furniture, Multiple Furniture) repeated-measures ANOVA revealed a significant interaction (F_{(4, 84)} = 151.59, p < 0.001), indicating that the pattern of activity in LOC across these conditions was indeed distinct from that in OPA.