A network linking scene perception and spatial memory systems in posterior cerebral cortex

Abstract

The neural systems supporting scene-perception and spatial-memory systems of the human brain are well-described. But how do these neural systems interact? Here, using fine-grained individual-subject fMRI, we report three cortical areas of the human brain, each lying immediately anterior to a region of the scene perception network in posterior cerebral cortex, that selectively activate when recalling familiar real-world locations. Despite their close proximity to the scene-perception areas, network analyses show that these regions constitute a distinct functional network that interfaces with spatial memory systems during naturalistic scene understanding. These "place-memory areas" offer a new framework for understanding how the brain implements memory-guided visual behaviors, including navigation.

Fig. 1. Distinct topography of place-memory and scene-perception activity in posterior cerebral cortex.

In all participants, three place-memory areas were observed, each located significantly anterior to one region of the scene-perception network. One example participant in Experiment 1 is shown (See Supplementary Fig. 1 and Supplementary Video 1 for thresholded and unthresholded activation maps for all participants (n = 14)). The participant’s scene perception ROIs are outlined in white, and place-memory activity is shown in warm colors. The scene-perception network (parahippocampal place area [PPA], occipital place area [OPA], and medial place area [MPA]) was localized by comparing the BOLD response when participants viewed images of scenes versus with faces (outlined in white, thresholded at vertex-wise p < 0.001). Place-memory areas on each surface were localized in separate fMRI runs by comparing the BOLD response when participants recalled personally familiar places versus people (warm colors, thresholded at vertex-wise p < 0.001). Polar plots: for each cortical surface, the center of mass of place-memory activation was significantly anterior to the center of mass of scene-perception activation in all participants (all ts > 5, p < 0.001). In contrast, face memory activation was spatially co-localized with the face-selective fusiform face area (FFA) on the ventral surface, and no anterior shift was observed (cool colors, t₉ = 0.1211, p = 0.906). Statistical analyses revealed no difference between the hemispheres, so, for clarity, only right hemisphere is shown. Inset: while the activation during place memory was systematically anterior to activation during scene perception, the spatial overlap between perception and memory activation varied across the cortical surfaces. Note that the axes (posterior-anterior) of each polar plot are aligned to its associated cortical surface. The data in the polar plot reflects distance in millimeters.

Fig. 2. Location of place-memory activity in relation to known functional and anatomical landmarks.

a The place-memory areas are anterior to and have minimal overlap with retinotopic cortex. We conducted a group analysis of the place-memory localizer (place > people memory recall; thresholded at vertex-wise t > 7.3, p = 1e−6) and compared the resulting activation to the most probable location of the cortical retinotopic maps using the atlas (overlaid) from Wang et al. (2015). The peak of place-memory activity was anterior toretinotopic maps on the lateral and ventral surfaces and there was very little overlap between place-memory activity and retinotopic maps. b The place-memory areas fall at the intersection between anatomical parcels known to be involved in visual processing and those associated with spatial memory. Comparing the peaks of place-memory activity with parcels from Glasser et al. (overlaid) revealed that the place-memory areas fell at the intersection of parcels associated with visual and spatial processing. Activation maps are replotted in panels a and b to allow comparison between parcellations.

Fig. 3. The place-memory areas respond preferentially to familiar stimuli .

a, b The place-memory areas preferentially activate familiar stimuli. a. Experiment 3. Participants viewed viewing panning movies of personally familiar places versus unfamiliar places, tailored to each participant using Google StreetView (see Supplementary Videos 2–5). The cortical surface depicts the contrast of BOLD activity for a single participant, thresholded at vertex-wise p < 0.001. Only significant vertices within the scene perception (white) and place-memory (burgundy) areas are shown. b Average t-statistic of vertices in the scene-perception (open bars) and place-memory areas (filled bars) when viewing videos of personally familiar places compared to unfamiliar places. On each cortical surface, the place-memory areas showed an enhanced response to familiar stimuli compared to the scene-perception areas (all ts > 2.6, ps < 0.01). Connected points depict individual participants. The hippocampus also showed a preferential response to familiar compared to unfamiliar place movies (Supplementary Fig. 9a). The amygdala (Supplementary Fig. 9b) and early visual cortex (Supplementary Fig. 10) did not show a preferential response to familiar place movies, arguing against a purely attentional account of this effect. OPA—occipital place area, LPMA—lateral place-memory area, PPA—parahippocampal place area, VPMA—ventral place-memory area, MPA—medial place area, MPMA—medial place-memory area.

Fig. 4. The place-memory areas constitute a distinct function network and associate closely with the hippocampus.

a Experiment 2. To assess whether the place-memory areas and scene-perception areas form distinct functional networks, participants watched an 11-minute video designed to elicit naturalistic scene understanding, comprised of several college admissions videos, real-estate listings, and architectural tours. For each participant (n = 13), the average time series from the scene-perception areas (pink, parahippocampal place area [PPA], occipital place area [OPA], and medial place area [MPA], the place-memory areas (burgundy, medial, ventral, and lateral place-memory areas [MPMA, LPMA, VPMA]), and the pairwise partial correlation was calculated. The correlation matrix depicts the average partial correlation of each area from all participants (ordered by Ward similarity). b The average pairwise partial correlation of within-network activity (Scene-perception network × Scene-perception network [SPN × SPN] and place-memory network × place-memory network [PMN × PMN]) was significantly higher than the correlation of between network activity (SPN × PMN) (F_(2,60) = 50.915, p < 0.001). c The scene-perception and place-memory areas differentially associate with the brain’s visual and memory systems (F_(3,84) = 55.5, p < 0.001). The scene-perception areas were more correlated with early visual cortex (t₁₂ = 6.05, p < 0.001), while the place-memory areas were more correlated with the hippocampus (t₁₂ = 10.64, p < 0.001), which is further evidence for their roles in perception and memory, respectively. In all plots, n.s., p > 0.05; *p < 0.05; **p < 0.01; ***p < 0.001.

Fig. 5. Perception and explicit memory recall (i.e. mental imagery) differentially engage the scene-perception and place-memory areas.

a In Experiment 4, participants (n = 14) saw panning movies of unfamiliar places (perception trials) or performed explicit memory recall (i.e. mental imagery) of personally familiar places (mental imagery trials). b BOLD activation during mental imagery of places compared to baseline for a representative subject. Below baseline activation within the perceptual areas PPA (ventral) and OPA (lateral) are highlighted. Only vertices within the scene-perception network (SPN; white) and place-memory network (PMN; burgundy) are shown. c The scene-perception areas and place-memory areas are differentially engaged during scene perception and mental imagery. Activation versus baseline of the scene-perception (open bars) and place-memory areas (filled bars) during perception of places (pink) or mental imagery of places (red). A linear mixed effects model analysis revealed that on each cortical surface, there was a significant dissociation in activation during perception and mental imagery, where the scene perception areas were significantly more active during perception, while the place-memory areas were significantly more active during mental imagery of places (ROI × Task interaction—Lateral: F_(1,91) = 237.37; p < 0.001; Ventral: F_(1,91) = 78.19; p < 0.001; Medial: F_(1,91) = 28.96; p < 0.001). Early visual cortex (Supplementary Fig. 11) and amygdala (Supplementary Fig. 12) also showed below baseline responses during mental imagery; hippocampus responded more to perception compared to imagery, but positively in both conditions (Supplementary Fig. 12). In all plots, n.s., p > 0.05; *p < 0.05; **p < 0.01; ***p < 0.001. OPA—occipital place area, LPMA—lateral place-memory area, PPA—parahippocampal plaace area, VPMA—ventral place-memory area, MPA—medial place area, MPMA—medial place-memory area.