Dissociating Landmark Stability from Orienting Value Using Functional Magnetic Resonance Imaging

Abstract

Retrosplenial cortex (RSC) plays a role in using environmental landmarks to help orientate oneself in space. It has also been consistently implicated in processing landmarks that remain fixed in a permanent location. However, it is not clear whether the RSC represents the permanent landmarks themselves or instead the orienting relevance of these landmarks. In previous functional magnetic resonance imaging (fMRI) studies, these features have been conflated-stable landmarks were always useful for orienting. Here, we dissociated these two key landmark attributes to investigate which one best reflects the function of the RSC. Before scanning, participants learned the features of novel landmarks about which they had no prior knowledge. During fMRI scanning, we found that the RSC was more engaged when people viewed permanent compared with transient landmarks and was not responsive to the orienting relevance of landmarks. Activity in RSC was also related to the amount of landmark permanence information a person had acquired and, as knowledge increased, the more the RSC drove responses in the anterior thalamus while viewing permanent landmarks. In contrast, the angular gyrus and the hippocampus were engaged by the orienting relevance of landmarks, but not their permanence, with the hippocampus also sensitive to the distance between relevant landmarks and target locations. We conclude that the coding of permanent landmarks in RSC may drive processing in regions like anterior thalamus, with possible implications for the efficacy of functions such as navigation.

Figure 1.. The four experimental conditions. Landmarks varied in terms of their permanence and orienting relevance. For each condition, four example computer screens are shown to represent four different occasions when this stimulus was presented during learning. Permanent landmarks (left/blue) were always positioned in the exact same screen location. Transient landmarks (right/red) appeared in a different place every time. Relevant landmarks (top/darker) could always be used to locate where a treasure chest would be, whereas irrelevant landmarks (bottom/lighter) could not be used to locate the treasure chest.

Figure 2.. The testing phase during fMRI scanning. An item appeared on the screen, and participants were asked about its permanence and also its relevance for locating the treasure chest. The order of questions was randomized, and the way in which the permanence and relevance questions were asked also varied. There was then a jittered 2- to 4-sec interval before the next trial.

Figure 3.. Brain areas responsive to landmark permanence and relevance—whole-brain univariate analysis. (A) The RSC and posterior parts of POS were more engaged by permanent than transient landmarks. (B) Bilateral clusters in the angular gyrus were more active when people viewed a relevant than an irrelevant landmark. Activations are displayed on a sagittal (A) and axial (B) section of a single representative participant's structural MRI brain scan. The color bars indicate each voxel's associated Z score.

Figure 4.. Hippocampal processing of distance to the treasure and orienting relevance. (A) The hippocampus increased its engagement for landmarks that were associated with a more distant target treasure location. Activations are displayed on sagittal sections of a single representative participant's structural MRI brain scan. The color bar indicates each voxel's Z score. (B) Only the hippocampus had patterns of fMRI activity, which could be used to decode whether a relevant landmark's associated treasure was nearby or farther away. The green dashed line indicates the chance level (50%) for this two-way classification; error bars show the SEM, and * denotes classifications that are significantly above chance (p < .05). RSC = retrosplenial cortex; HC = hippocampus; PHC = parahippocampal cortex; POS = parieto-occipital sulcus; AThal = anterior thalamus.

Figure 5.. RSC connectivity associated with individual differences in permanence knowledge. RSC = retrosplenial cortex; AThal = anterior thalamus. (A) A gPPI analysis showed that, when participants viewed an image of a permanent landmark, the better they had learned landmark permanence, then the more their RSC interacted with AThal. (B) To examine the nature of this RSC–AThal interaction in relation to learning of landmark permanence, we performed a PEB DCM analysis. The winning model (Model 1) indicates that RSC drove activity in AThal in accordance with individuals' learning of landmark permanence.

Figure 6.. MVPA analysis of landmark permanence and relevance. (A) The classification accuracy for decoding between the four types of landmark in each of the ROIs. RSC = retrosplenial cortex; HC = hippocampus; PHC = parahippocampal cortex; POS = parieto-occipital sulcus; AThal = anterior thalamus. Above chance classification was only possible for RSC and hippocampus. To determine which feature each region was particularly sensitive to, additional two-way classifications of landmark permanence and relevance were performed in RSC (B) and hippocampus (C). RSC responses could be used to classify landmark permanence but not relevance, whereas hippocampal activity could be used to classify orienting relevance but not permanence of landmarks. Dashed lines indicate each classification's chance level, error bars show the SEM, and * denotes classifications that are significantly above chance (p < .05).