Hippocampus, Retrosplenial and Parahippocampal Cortices Encode Multicompartment 3D Space in a Hierarchical Manner

Abstract

Humans commonly operate within 3D environments such as multifloor buildings and yet there is a surprising dearth of studies that have examined how these spaces are represented in the brain. Here, we had participants learn the locations of paintings within a virtual multilevel gallery building and then used behavioral tests and fMRI repetition suppression analyses to investigate how this 3D multicompartment space was represented, and whether there was a bias in encoding vertical and horizontal information. We found faster response times for within-room egocentric spatial judgments and behavioral priming effects of visiting the same room, providing evidence for a compartmentalized representation of space. At the neural level, we observed a hierarchical encoding of 3D spatial information, with left anterior hippocampus representing local information within a room, while retrosplenial cortex, parahippocampal cortex, and posterior hippocampus represented room information within the wider building. Of note, both our behavioral and neural findings showed that vertical and horizontal location information was similarly encoded, suggesting an isotropic representation of 3D space even in the context of a multicompartment environment. These findings provide much-needed information about how the human brain supports spatial memory and navigation in buildings with numerous levels and rooms.

Figure 1.

Stimuli and experimental design. (A) Top panel, overview of the virtual gallery building with transparent walls for display purposes. Bottom panel, overview of one room with transparent walls for display purposes. (B) On each trial, participants were virtually transported to one of the paintings from a corridor, and then the participant performed a spatial memory task. During the prescan egocentric judgment test, they were asked to make spatial judgments about the locations of other paintings, for example, “Is the pig on your left?” (mean RT 3.2 s). During the scanning test, they were asked to indicate whether the painting was the correct one or not for that location, “Is this picture correct?” (mean RT 1.3 s). (C) An example layout of 16 paintings located in the 4 rooms of the gallery. The within, vertical, horizontal and diagonal rooms were defined relative to a participant’s current location. In this example, the participant was standing in front of the turtle painting (blue arrow). (D) Spatial judgments were significantly faster for the within-room (Within) condition. There were no differences between vertical (Ver), horizontal (Hor), or diagonal (Diag) rooms. Error bars are SEM adjusted for a within-subjects design (Morey 2008). *P < 0.05.

Figure 2.

Analysis overview. (A) A floor plan of the virtual building. The 4 rooms are labeled as “Rm101,” “Rm102,” “Rm201,” “Rm202” and the 4 corners as “A,” “B,” “C,” “D” for the purposes of explanation here. Participants were not told of any explicit labels during the experiment. (B) An example trial sequence. For the behavioral and fMRI repetition suppression analyses, each trial was labeled based on its spatial relationship with the preceding trial, for example, the second trial belongs to the “same room, different corner” condition. Of note, this trial definition is used for analysis only and participants were not asked to pay attention to the preceding trial. (C) Predictions for the fMRI signals. If some brain regions encode corner information, lower fMRI signal is expected for the same corner condition compared with the different corner condition. If room information is encoded, fMRI signal is expected to be lower for the same room condition compared with the different room condition.

Figure 3.

The behavioral priming effect of room during the scanning task. (A) Accuracy was significantly higher for the same room condition compared with all other rooms. There was no significant difference between the different room types. (B) RT was significantly reduced for the same room condition compared with all other conditions. There was no significant difference between different room types. Error bars are SEM adjusted for a within-subjects design (Morey 2008). *P < 0.05.

Figure 4.

Corner encoding regions. The whole brain contrast “same corner < different corner” revealed only the left anterior hippocampus (peak MNI = [−33, −19, −16], t[29] = 5.31, P < 0.001). The thresholded map is overlaid on the group average structural MRI scan (P < 0.001, uncorrected for display purposes). No other brain region survived multiple comparison correction.

Figure 5.

Room encoding regions. (A) The whole brain contrast “same room < different room” revealed bilateral RSC (RSC_R, RSC_L), right parahippocampal cortex (PHC_R) and bilateral posterior HC (postHC_R, postHC_L). Given our a priori interest in RSC and posterior hippocampus, their clusters are shown with a small volume corrected threshold level (t[29] > 3.67, t[29] > 3.75), while the parahippocampal cortex cluster is shown with a whole-brain corrected threshold (t[29] > 6.01). The peak MNI coordinate is shown below each cluster. (B) Comparison of mean activity for 3 different room types (vertical/horizontal/diagonal) at each cluster (5 mm sphere at peak voxel). The “same” condition (in yellow) is shown for reference purposes. The response to the diagonal condition was significantly larger than for the vertical condition in all regions except the left RSC. There was no significant difference between the vertical and horizontal conditions. Error bars are SEM adjusted for a within-subjects design (Morey 2008). *P < 0.05.