Which way was I going? Contextual retrieval supports the disambiguation of well learned overlapping navigational routes

Abstract

Groundbreaking research in animals has demonstrated that the hippocampus contains neurons that distinguish between overlapping navigational trajectories. These hippocampal neurons respond selectively to the context of specific episodes despite interference from overlapping memory representations. The present study used functional magnetic resonance imaging in humans to examine the role of the hippocampus and related structures when participants need to retrieve contextual information to navigate well learned spatial sequences that share common elements. Participants were trained outside the scanner to navigate through 12 virtual mazes from a ground-level first-person perspective. Six of the 12 mazes shared overlapping components. Overlapping mazes began and ended at distinct locations, but converged in the middle to share some hallways with another maze. Non-overlapping mazes did not share any hallways with any other maze. Successful navigation through the overlapping hallways required the retrieval of contextual information relevant to the current navigational episode. Results revealed greater activation during the successful navigation of the overlapping mazes compared with the non-overlapping mazes in regions typically associated with spatial and episodic memory, including the hippocampus, parahippocampal cortex, and orbitofrontal cortex. When combined with previous research, the current findings suggest that an anatomically integrated system including the hippocampus, parahippocampal cortex, and orbitofrontal cortex is critical for the contextually dependent retrieval of well learned overlapping navigational routes.

Figure 1.

Virtual maze design. a, Overhead layout of the 12 mazes used in the task. The non-overlapping mazes (NOL) are depicted on the left and the overlapping mazes (OL) are depicted on the right. Mazes began at the “∧” and end at the “X.” The colored, elongated segments represent the hallways of the paths. One color represents one path. The gray segments represent the incorrect “foil” hallways. The black squares represent intersections between hallways. The yellow segments in the overlapping mazes represent overlapping hallways. The final hallway of an overlapping segment before the paths split apart (indicated with “*”) was labeled the critical hall. b, Perspective of NOL5 from the beginning of the first hall. This image is representative of how participants viewed the mazes.

Figure 2.

Scanning day behavioral performance. Error bars reflect the SEM. Significant differences are indicated with an asterisk. The OL condition is represented in gray, and the NOL condition is represented in white. a, Proportion of correct trials for the first hall period. b, Reaction times (RTs) in milliseconds for the first hall period. c, Proportion of correct trials for the critical hall period. d, RTs in milliseconds for the first hall period.

Figure 3.

Medial temporal lobe activation during the overlapping first hall period. Statistical parametric map of the OL > NOL contrast for the first hall period. The image is FDR corrected to p < 0.05 with a voxel extent of 30. The green arrows indicate bilateral hippocampal clusters of activation. The blue arrows indicate bilateral parahippocampal clusters of activation.

Figure 4.

Greater activation in the critical hall period for overlapping mazes. a, Statistical parametric map of the OL > NOL contrast for the critical hall period. The image is FDR corrected to p < 0.05 with a voxel extent of 30. The green arrow indicates the right hippocampal cluster of activation. The blue arrow indicates the right parahippocampal cluster of activation. b, Statistical parametric map of the OL > NOL contrast for the critical hall period. The image is FDR corrected to p < 0.05 with a voxel extent of 30. The blue arrows indicate bilateral orbitofrontal clusters of activation.

Figure 5.

Breakdown of the individual components of the non-overlapping and overlapping mazes. The same colors denote comparable components across mazes (i.e., both the overlapping and non-overlapping mazes contain non-overlapping first halls). Note that the OL1 mazes only have one overlapping hallway, and therefore they do not have any noncritical overlapping halls.