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.

Mobile brain/body imaging of landmark-based navigation with high-density EEG

“…Accordingly, we found a cluster located in or near the posterior cingulate cortex (cluster 1), anatomically close to the RSC proper (BA29/30) and often included in the retrosplenial complex (Epstein, 2008). fMRI studies have consistently shown that the human RSC encodes heading direction (Marchette et al ., 2014; Shine et al ., 2016) anchored onto local visual cues, like stable landmarks, by using a first-person perspective (Auger et al ., 2012; Marchette et al ., 2015; Auger & Maguire, 2018), and that RSC is involved in the interaction between allocentric and egocentric navigation during landmark-based spatial tasks (Julian et al ., 2018; Mitchell et al ., 2018). Moreover, the RSC is embedded in a network of somatosensory areas that were also partially retrieved in our cluster analysis.…”

“…The neural substrates of landmark-based navigation form a network spanning medial temporal areas (e.g., hippocampus, para-hippocampal cortex) and medial parietal regions (Epstein & Vass, 2014), such as the retrosplenial cortex (RSC). Here, we expect the RSC to play a role in mediating spatial orientation through the encoding and retrieval of visual landmarks (Spiers & Maguire, 2006; Auger et al ., 2012, 2015; Marchette et al ., 2015; Auger & Maguire, 2018; Julian et al ., 2018). RSC is indeed implicated in the coding of landmark-based representations in both egocentric and allocentric reference frames (Vann et al ., 2009; Marchette et al ., 2014; Shine et al ., 2016; Sulpizio et al ., 2016; Mitchell et al ., 2018; Page & Jeffery, 2018).…”

Stable Encoding of Visual Cues in the Mouse Retrosplenial Cortex

“…One emergent issue relates to evidence that the RSC may be involved in the identification of stable landmarks in an environment ( Auger et al. 2012 , 2015 ; Auger and Maguire 2018 ; Mitchell et al. 2018 ).…”

Retrosplenial cortex and its role in spatial cognition

“…They then showed that this RSC permanence encoding also occurred when subjects learned about artificial, abstract landmarks in a featureless Fog World ( Auger et al, 2015 ), demonstrating that the RSC is involved in new learning of landmarks and their spatial stability and also that such learning correlates with navigation ability ( Auger et al, 2017 ). Puzzlingly, however, the involvement of RSC seems better correlated with the stability per se than with the orientational relevance of the landmarks ( Auger and Maguire, 2018a ).…”

“…This viewpoint supposes a particular role for landmarks in the ongoing formation and updating of spatial representations and is consistent with the close relationship of RSC to visual areas as well as to the hippocampal spatial system. Recently, Auger and Maguire suggested that RSC processing of landmarks may be more to do with permanence and stability than orientation relevance, and indeed that RSC’s role in permanence may extend beyond landmarks to other domains ( Auger and Maguire 2018a , 2018b ).…”