A central role for the retrosplenial cortex in de novo environmental learning

Abstract

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.

Keywords: fMRI; human; navigation; neuroscience; virtual reality.

Figure 1.. The virtual reality environment ‘Fog World’.

(A) Examples of the ‘alien’ landmarks. (B) Landmarks positioned within the virtual world. (C) An overhead perspective of the environment showing the five different coloured, intersecting paths—note this aerial view was never seen by participants during learning. DOI: http://dx.doi.org/10.7554/eLife.09031.003

Figure 2.. The Experimental paradigm.

While undergoing functional MRI (fMRI) scanning, subjects were presented with videos travelling along the various paths. (A) An example sequence of video frames with a landmark emerging through the fog, the camera turning towards it before returning back to the middle of the path—see also Video 1. (B) After viewing videos of each of the five paths once, subjects answered a series of questions about individual landmarks to test their learning throughout the experiment. A learning ‘sweep’ consisted of one round of videos of the five paths and the questioning period which followed. There were 12 learning sweeps. DOI: http://dx.doi.org/10.7554/eLife.09031.004

Figure 3.. Changes in the brain regions engaged by different landmark features over the course of learning.

(A) The loading values of each landmark feature to the four principal component factors. Values above 0.5 are highlighted in bold. Factor 1 was strongly related to landmark permanence, factor 2 to their memorableness, factor 3 to their size and factor 4 to the visual salience of landmarks. (B) The bar graphs to the left show how strongly each of the four factors was related to the various features rated by subjects in the post-scan debrief. The associated brain regions responding to these four factors in the first and last quarters of learning are shown to the right. All activations are shown on a structural MRI brain scan of single representative subject. Each factor's activations are shown on the same sagittal slice and using a whole brain uncorrected threshold of p < 0.00001 for display purposes. The colour bars indicate the Z-score associated with each voxel. DOI: http://dx.doi.org/10.7554/eLife.09031.007

Figure 4.. Brain regions more engaged by permanent than transient landmarks by the end of learning.

(A) Shows activations in retrosplenial cortex (RSC) and posterior parieto-occipital sulcus (POS) at the default threshold of p < 0.05 (FWE). The colour bar indicates Z-score associated with each voxel. (B) Shows a plot of mean blood oxygenation level-dependent (BOLD) responses (±1 SEM) within the RSC cluster (circled in green). In the first two quarters of scanning, responses to permanent (blue) and transient (red) landmarks did not differ, but as subjects learned landmark permanence, BOLD responses increased for permanent landmarks with a corresponding decrease for transient landmarks. DOI: http://dx.doi.org/10.7554/eLife.09031.008

Figure 5.. Response profile in POS.

(A) POS responded to memorable landmarks (those with higher factor 2 values) in the first quarter of learning (red) and permanent ones (with higher values for factor 1) in the final quarter (blue). The overlap of these activations is shown in purple. (B) The response profile of the overlapping (purple) voxels for the two factors throughout whole scan. Responses were initially greater for memorable landmarks but then switched over the course of learning to eventually become responsive to permanence. Plots show mean BOLD responses ±1 SEM. Activations are shown on a structural MRI brain scan of single representative subject at the default threshold of p < 0.05 (FWE). DOI: http://dx.doi.org/10.7554/eLife.09031.009

Figure 6.. Examples of permanence learning curves and the associated fMRI response.

Data from three examples subjects are shown. Learning curves were calculated and used to create subject-specific parametric regressors corresponding to the amount of permanence knowledge acquired throughout the scan. A whole brain comparison of fMRI responses to permanent vs transient landmarks according to how well subjects knew their permanence revealed responses only in RSC which were directly related to these curves. The learning curves show the estimated learning state (coloured line) and the 95% confidence interval (coloured shaded area). The activation is shown on a structural MRI brain scan of single representative subject using a whole brain uncorrected threshold of p < 0.001 for display purposes. The colour bars indicate the Z-score associated with each voxel. DOI: http://dx.doi.org/10.7554/eLife.09031.010

Figure 7.. Multivariate Bayes analysis of responses which mapped onto knowledge of permanent landmark locations.

The log model evidence values for response patterns within the RSC (blue), posterior POS (red), hippocampus (HC; green) and parahippocampal cortex (PHC; purple) relating to knowledge of permanent landmark locations are shown in each of the four quarters of scanning. By the final quarter of learning, the pattern of activity in the HC mapped onto the amount subjects knew about where permanent landmarks were located in the environment. The dashed black line indicates the threshold at which log model evidence values are considered to be strong (see ‘Materials and methods’). DOI: http://dx.doi.org/10.7554/eLife.09031.011