Hippocampal size predicts rapid learning of a cognitive map in humans

Abstract

The idea that humans use flexible map-like representations of their environment to guide spatial navigation has a long and controversial history. One reason for this enduring controversy might be that individuals vary considerably in their ability to form and utilize cognitive maps. Here we investigate the behavioral and neuroanatomical signatures of these individual differences. Participants learned an unfamiliar campus environment over a period of three weeks. In their first visit, they learned the position of different buildings along two routes in separate areas of the campus. During the following weeks, they learned these routes for a second and third time, along with two paths that connected both areas of the campus. Behavioral assessments after each learning session indicated that subjects formed a coherent representation of the spatial structure of the entire campus after learning a single connecting path. Volumetric analyses of structural MRI data and voxel-based morphometry (VBM) indicated that the size of the right posterior hippocampus predicted the ability to use this spatial knowledge to make inferences about the relative positions of different buildings on the campus. An inverse relationship between gray matter volume and performance was observed in the caudate. These results suggest that (i) humans can rapidly acquire cognitive maps of large-scale environments and (ii) individual differences in hippocampal anatomy may provide the neuroanatomical substrate for individual differences in the ability to learn and flexibly use these cognitive maps. © 2013 Wiley Periodicals, Inc.

Figure 1

Study area: Temple University’s Ambler campus. Participants learned the campus over a period of three weeks. Buildings from route A were not visible from route B and vice-versa. Buildings within route A were separated by small woodland such that participants standing in building A4 (east most building) could not simultaneously see the other three buildings in the route. All buildings in route B were simultaneously visible to participants. In their first visit, they were guided along two separate routes and were asked to remember the name and position of the four buildings on each route (blue and orange buildings). Specifically, when standing in front of each building (black circles) they memorized the locations of the front door. In the second and third sessions, participants were again guided along the two routes, and they were also guided along 1 of 2 connecting routes that linked the two areas of the campus through a short (green) or longer (red) path. Participants’ spatial knowledge of the campus was investigated at the end of each session by asking them to complete onsite and offsite direction estimates, distance estimates and the drawing of a sketchmap of the campus.

Figure 2

Behavioral results for the 4 spatial tasks across the three sessions. (a) Mean pointing error (and SEM) for the onsite and offsite pointing tasks. (b) Mean accuracy for the distance (% correct) and sketchmap (r² * 100) tasks. Performance on all tasks improved in the second session after participants learned one of the two connection routes with the exception of the onsite within pointing task where landmarks were simultaneously visible to participants. No further improvement was observed in session three after learning a second connecting route.

Figure 3

Volumetry results. (a) The right hippocampus was larger in subjects who were more accurate in the offsite pointing task. (b) The center-of-mass of the right hippocampus was located more posteriorly in these subjects. (c) The right caudate was larger in subjects who were less accurate when pointing to buildings within the same route in the offsite pointing task.

Figure 4

Mediation results. Mediation analysis that takes into account the effect of perspective taking ability on the relationship between hippocampal size and offsite pointing error. The total effect of right posterior hippocampal size on offsite pointing error that was mediated by perspective taking ability was 35%. These findings indicate that perspective-taking ability partially (but incompletely) mediates the effect of hippocampal size on offsite pointing performance.

Figure 5

Voxel Based Morphometry (VBM) results. (a) Negative correlation between gray matter volume in the right superior parietal lobe and offsite pointing accuracy. (b) Positive correlation between gray matter volume in the right hippocampus and offsite pointing accuracy. Note that the increase gray matter is located in the tail of the right hippocampus. (c) Negative correlation between gray matter volume in the caudate (bilateral) and offsite pointing accuracy. Threshold in (a) is p < 0.05 corrected for multiple comparisons across the entire brain; thresholds in (b) and (c) are p < 0.05 uncorrected.