Retrosplenial cortex codes for permanent landmarks

Abstract

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.

Figure 1. Examples of the stimuli.

Example items are shown from the 280 stimuli used in the fMRI study. Level of permanence (from low to high) is shown from left to right. Shown vertically from bottom to top, variation (from low to high) in terms of the non-permanence factor. For further examples of the stimuli see Figure S2.

Figure 2. Brain regions engaged by the non-permanence and permanence components of the factor analysis.

Activations are displayed on sagittal views of the structural MRI brain scan of one participant chosen at random. The colour bars indicate the Z-scores associated with each voxel. (A) The PHC and posterior visual areas were activated by increasing values of the non-permanence factor. (B) RSC, along with PHC, was activated by the permanence factor.

Figure 3. Response profiles of the PHC and RSC.

The fMRI BOLD response to the non-permanence (blue) and permanence (orange) factors are shown for (A) the PHC and (B) the RSC. Mean scores are plotted +/−1 SEM. Landmarks were grouped into 5 bins according to the values of their factor score estimates, and these were approximately equivalent to the five rating values, e.g. for the permanence factor ‘low’ means landmarks that were not at all permanent, ranging to ‘high’ meaning permanent landmarks. Note that the response profiles of these two factors bore close relation to those of the individual features from which they were composed in the principal components analysis, and so provide a reliable summary of all the features. (C) Brain areas more active for landmarks rated as high compared to low in permanence. Activations are displayed on sagittal views of the structural MRI brain scan of one participant chosen at random. The colour bars indicate the Z-scores associated with each voxel.

Figure 4. Landmark feature ratings segregated according to navigation ability.

Good navigators are shown in green and poor navigators in red. (A) The number of landmarks where at least 75% of participants within each group gave the same rating. It is clear that the only difference between good and poor navigators was for permanence and portability. (B) Focussing on the permanence ratings, we examined how often each participant gave a rating which was different to the most common rating for each item (i.e. the mode). Good and poor navigators did not differ in rating items which were most commonly scored 1 to 4 for permanence, however, there was a significant difference between the groups for rating number 5, landmarks that were the most permanent and never moved. (C) This difference for the most permanent landmarks was replicated in the independent group of fMRI participants. *P<0.05; graphs show the means +/−1 SEM.

Figure 5. Examples of landmarks where good but not poor navigators had at least 75% agreement about their ‘never moves’ permanence rating.

Figure 6. Brain regions more active in good than poor navigators when viewing the most permanent landmarks.

(A) Good navigators had greater activity in RSC and anterodorsal thalamus than poor navigators when viewing the most permanent items but not the less permanent ones. Activations are displayed on sagittal views of the structural MRI brain scan of one participant chosen at random. The colour bars indicate the Z-scores associated with each voxel. (B) The mean (+/−1 SEM) response in active RSC voxels to the most permanent items was significantly greater in good (green) than in poor (red) navigators. *P<0.05.