Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition

Abstract

A key component of spatial navigation is the ability to use visual information to ascertain where one is located and how one is oriented in the world. We used functional magnetic resonance imaging to examine the neural correlates of this phenomenon in humans. Subjects were scanned while retrieving different kinds of topographical and nontopographical information in response to visual scenes. In the three critical conditions, they viewed images of a familiar college campus, and reported either the location of the place depicted in the image (location task), the compass direction that the camera was facing when the image was taken (orientation task), or whether the location was on campus or not (familiarity task). Our analyses focused on the retrosplenial cortex (RSC)/parietal-occipital sulcus region and the parahippocampal place area (PPA), which previous studies indicate play a critical role in place recognition. RSC activity depended on the type of information retrieved, with the strongest response in the location task. In contrast, PPA activity did not depend on the retrieval task. Additional analyses revealed a strong effect of familiarity in RSC but not in the PPA, with the former region responding much more strongly to images of the familiar campus than to images of an unfamiliar campus. These results suggest that the PPA and RSC play distinct but complementary roles in place recognition. In particular, the PPA may primarily support perception of the immediate scene, whereas RSC may support memory retrieval mechanisms that allow the scene to be localized within the broader spatial environment.

Figure 1.

Experimental design. In the location condition, subjects viewed pictures of the University of Pennsylvania campus and reported whether depicted locations were east or west of 36th Street. In the orientation condition, subjects viewed the same set of photographs and reported whether they were taken by a camera facing east or west. In the familiarity condition, subjects reported whether photographs depicted a location on the Penn campus or not. (Responses to the Penn and not Penn images were measured separately in this condition.) In the object condition, subjects viewed images of nonscene objects and made vehicle/nonvehicle judgments.

Figure 2.

fMRI response in the PPA and RSC. The PPA showed no effect of retrieval task or familiarity, responding equally strongly in all four conditions in which scenes were shown. The RSC response was affected by both retrieval task and familiarity. Specifically, response was marginally stronger during location retrieval than during orientation retrieval, which in turn elicited a stronger response than simple familiarity judgments on the same photographs (Penn). Furthermore, when making familiarity judgments, response was stronger for images of the familiar campus (Penn) than for images of the unfamiliar campus (not Penn). Anatomical loci for the PPA and RSC are shown in Figure 5d. Error bars are ± 1 SEM.

Figure 3.

RSC response as a function of RT. Trials are divided into quintiles based on RT, and the fMRI response for each quintile and condition is plotted. There is a clear increase in fMRI response with longer RTs. However, the differences between the location versus orientation and Penn versus not Penn conditions appear to be consistent across RT. Error bars are ± 1 SEM.

Figure 4.

Responses in PPA and RSC as a function of image repetition. The same set of Penn images was used to construct location A, orientation A, and Penn conditions. As such, each image in this set was shown three times during the experiment (P1, P2, P3). The graph shows how responses to these images were reduced by image repetition in the PPA (blue) and RSC (red). For comparison, response in the not Penn (NP) condition is also plotted; each image in this condition was shown only once. Error bars are ± 1 SEM.

Figure 5.

Whole-brain analyses. a, Location versus Penn. Voxels responding more strongly (p < 0.001, uncorrected) during location judgments (Location) than during familiarity judgments (Penn) are plotted in orange on an inflated version of the cortex. Blue voxels exhibited the opposite pattern (Penn > Location). From left to right, the four views depict the left hemisphere (medial surface), left hemisphere (lateral surface), right hemisphere (lateral surface), right hemisphere (medial surface). Gyri are light gray on the inflated surface, whereas sulci are dark gray. Location judgments more strongly recruited the superior frontal gyrus/sulcus (sfg/sfs), intraparietal sulcus (ips), thalamus (thal), and RSC/POS region, whereas familiarity judgments more strongly recruited regions in the anterior temporal and medial frontal lobes. b, Orientation versus Penn. Many of the same regions were activated for the orientation vs Penn contrast as for the Location versus Penn contrast, with the notable exception of the RSC/pos region. c, Penn versus not Penn. Several regions in the medial and lateral parietal cortex, including the RSC/pos region, precuneus (precun), and inferior parietal lobe (ipl) were more active when subjects made familiarity judgments on images of familiar location (Penn) than when subjects made familiarity judgments on images of unfamiliar locations (not Penn). d, Scenes versus objects. For purposes of comparison, regions responding differentially to scenes versus objects during the functional localizer scans are shown. These regions include the PPA, RSC, and transverse occipital sulcus (tos), which were defined in individual subjects for the ROI analyses. Note the striking correspondence between the RSC/pos region that responds more strongly to scenes than to objects and the RSC/pos region that responds more strongly during location judgments than familiarity judgments in a.