Combining patient-lesion and big data approaches to reveal hippocampal contributions to spatial memory and navigation

Abstract

Classic findings of impaired allocentric spatial learning and memory following hippocampal lesions indicate that the hippocampus supports cognitive maps of one's environment. Many studies assess navigation in vista space virtual reality environments and compare hippocampal-lesioned individuals' performance to that of small control samples, potentially stifling detection of preserved and impaired performance. Using the mobile app Sea Hero Quest, we examined navigation in diverse complex environments in two individuals with hippocampal lesions relative to demographically matched controls (N = 17,734). We found surprisingly accurate navigation in several environments, particularly those containing a constrained set of sub-goals, paths, and/or turns. Areas of impaired performance may reflect a role for the hippocampus in anterograde memory and more flexible and/or precise spatial representations, even when the need for allocentric processing is minimal. The results emphasize the value of combining single cases with big data and illustrate navigation performance profiles in individuals with hippocampal compromise.

Keywords: Biological sciences; Cognitive neuroscience; Neuroscience.

Graphical abstract

Figure 1

D.A.’s and B.L.’s Distance Performance Compared to Controls Map difficulty is derived from entropy, geometric and level-specific features. Distance percentile is the distance traveled during navigation compared to matched control participants.

Figure 2

D.A.’s and B.L.’s Distance Performance by Map Visibility Data are represented as mean +/− standard error of measurement.

Figure 3

Number of Backtracks by D.A. and B.L. Compared to Controls Data are represented as mean +/− standard error of measurement.

Figure 4

Representative MR images of the Medial Temporal Lobe in D.A. and B.L. (A) MR image of D.A.’s medial temporal lobes (MTLs) in a coronal view showing loss of volume bilaterally, most prominently in the right hemisphere. Image adapted from Kwan et al. (2013). (B) MR image of B.L.’s MTLs in a coronal view, with hippocampal segmentation visible to show the greatest volume loss within the dentate gyrus and partial volume loss in the CA3 subfield. Image adapted from Baker et al. (2016).

Figure 5

Examples of gameplay on Sea Hero Quest (A) Example of gameplay during wayfinding levels. (B) Example of gameplay during path integration levels, where participants had to navigate within a maze and when reaching a flare, shoot it back toward the start location. Images from Coutrot et al. (2019).

Figure 6

Distance Performance in B.L. and D.A. on Each Level of Sea Hero Quest Graph depicts distance performance in percentiles for D.A. and B.L. relative to their respective controls for each map level, which vary in difficulty and level characteristics (see Tables S1 and S2 for images). Higher percentile indicates better performance. Findings show that individuals with amnesia have performance that is comparable to controls when demands on anterograde memory are lower, which differs depending on level characteristics.