Landmarks are critical components of our internal representation of the environment, yet their specific properties are rarely studied, and little is known about how they are processed in the brain. Here we characterised a large set of landmarks along a range of features that included size, visual salience, navigational utility, and permanence. When human participants viewed images of these single landmarks during functional magnetic resonance imaging (fMRI), parahippocampal cortex (PHC) and retrosplenial cortex (RSC) were both engaged by landmark features, but in different ways. PHC responded to a range of landmark attributes, while RSC was engaged by only the most permanent landmarks. Furthermore, when participants were divided into good and poor navigators, the latter were significantly less reliable at identifying the most permanent landmarks, and had reduced responses in RSC and anterodorsal thalamus when viewing such landmarks. The RSC has been widely implicated in navigation but its precise role remains uncertain. Our findings suggest that a primary function of the RSC may be to process the most stable features in an environment, and this could be a prerequisite for successful navigation.

The retrosplenial cortex (RSC) is consistently engaged by a range of tasks that examine episodic memory, imagining the future, spatial navigation, and scene processing. Despite this, an account of its exact contribution to these cognitive functions remains elusive. Here, using functional MRI (fMRI) and multi-voxel pattern analysis (MVPA) we found that the RSC coded for the specific number of permanent outdoor items that were in view, that is, items which are fixed and never change their location. Moreover, this effect was selective, and was not apparent for other item features such as size and visual salience. This detailed detection of the number of permanent items in view was echoed in the parahippocampal cortex (PHC), although the two brain structures diverged when participants were divided into good and poor navigators. There was no difference in the responsivity of the PHC between the two groups, while significantly better decoding of the number of permanent items in view was possible from patterns of activity in the RSC of good compared to poor navigators. Within good navigators, the RSC also facilitated significantly better prediction of item permanence than the PHC. Overall, these findings suggest that the RSC in particular is concerned with coding the presence of every permanent item that is in view. This mechanism may represent a key building block for spatial and scene representations that are central to episodic memories and imagining the future, and could also be a prerequisite for successful navigation.

With experience we become accustomed to the types of environments that we normally encounter as we navigate in the world. But how does this fundamental knowledge develop in the first place and what brain regions are involved? To examine de novo environmental learning, we created an ‘alien’ virtual reality world populated with landmarks of which participants had no prior experience. They learned about this environment by moving within it during functional MRI (fMRI) scanning while we tracked their evolving knowledge. Retrosplenial cortex (RSC) played a central and highly selective role by representing only the most stable, permanent features in this world. Subsequently, increased coupling was noted between RSC and hippocampus, with hippocampus then expressing knowledge of permanent landmark locations and overall environmental layout. Studying how environmental representations emerge from scratch provided a new window into the information processing underpinning the brain's navigation system, highlighting the key influence of the RSC.DOI: http://dx.doi.org/10.7554/eLife.09031.001