Largely intact memory for spatial locations during navigation in an individual with dense amnesia

Abstract

Spatial navigation and event memory (termed episodic memory) are thought to be heavily intertwined, both in terms of their cognitive processes and underlying neural systems. Some theoretical models posit that both memory for places during navigation and episodic memory depend on highly overlapping brain systems. Here, we assessed this relationship by testing navigation in an individual with severe retrograde and anterograde amnesia; the amnesia stemmed from bilateral lesions in the medial temporal lobes from two separate strokes. The individual with amnesia and age-matched controls were tested on their memories for the locations of previously seen objects relative to distal mountain cues in an immersive virtual environment involving free ambulation. All participants were tested from both repeated and novel start locations and when a single distal mountain cue was unknowingly moved to determine if they relied on a single (beacon) cue to a greater extent than the collection of all distal cues. Compared to age-matched controls, the individual with amnesia showed no significant deficits in navigation from either the repeated or novel start points, although both the individual with amnesia and controls performed well above chance at placing objects near their correct locations. The individual with amnesia also relied on a combination of distal cues in a manner comparable to age-matched controls. Despite largely intact memory for locations using distal cues, the individual with amnesia walked longer paths, rotated more, and took longer to complete trials. Our findings suggest that memory for places during navigation and episodic memory may involve partially dissociable brain circuits and that other brain regions outside of the medial temporal lobe partially support some aspects of navigation. At the same time, the fact that the individual with amnesia walked more circuitous paths and had dense amnesia for autobiographic events supports the idea that the hippocampus may be important for binding information as part of a larger role in memory.

Keywords: Allocentric; Amnesia; Episodic memory; Hippocampus; Lesion; Medial temporal lobe function; Spatial navigation.

Fig 1.. CT imaging of HML040’s lesions in the axial view.

The images track the lesions from ventral (top left) regions to those more dorsal (bottom right).

Fig 2.. Overview of the task setup.

(A). Participant fitted with wireless HMD, battery pack, two controllers, and two foot covers with trackers (B). Bird’s-eye-view of entire virtual environment, including the 4 distal mountains (entire environment approximately 750×750 m in size) (C). Bird’s-eye-view of navigable virtual environment (approximately 5×5 m in size), with all three targets visible (D). Point-of-view from the participant within the virtual environment (E). Trial list with corresponding targets and starting locations.

Fig 3.. Example paths.

Some example paths walked through the virtual environment by HML040 and five selected controls on repeated acquisition, novel acquisition, repeated probes, novel probes, and moved mountain trials. Response location is where participants marked where they believed the target was and distance error was the Euclidean distance between the response location and actual target location.

Fig 4.. HML040 versus Control Group accuracy on novel and repeated viewpoints in acquisition trials.

(A). Comparison of trials across targets 1, 2, and 3 and (B). trials collapsed across targets. Distance error is the Euclidean distance between where participants placed the targets and where they were located in the virtual environment. Novel locations were those in which a start location/target location pairing was new to the participants and Repeated trials were those in which a start location/target location pairing was previously seen. Grey dots represent the control group’s data (some points may overlap). All error bars are the standard error of the mean (SEM). There were no statistically significant differences between HML040 and controls.

Fig 5.. All trial responses made by HML040 and controls.

X’s correspond to responses in which participants were tasked with finding target 1 and marked where they thought it was, diamonds correspond to responses in which participants were tasked with finding target 2 and marked where they thought it was, and circles correspond to responses in which participants were tasked with finding target 3 and marked where they thought it was. All responses are centralized around (0,0).

Fig 6.. Accuracy in delayed probe trials between HML040 and Control Group.

(A). HML040 versus Control Group and Chance Group accuracy averaged across all delayed probes. There was no statistically significant difference between HML and controls although HML040 performed significantly better than chance, as indicated by the mixed surrogate chance group. (B). HML040 versus Control Group accuracy for novel and repeated trials. Despite having a smaller distance from the target on novel trials compared to the control group, for both repeated and novel trials, HML040 did not perform statistically different from the controls. Distance error is the Euclidean distance between where participants placed the targets and where they were actually located in the virtual environment. Novel locations were those in which a start location-target location pairing was new to the participants and Repeated trials were those in which a start location-target location pairing was previously seen. Grey dots represent the control group’s data (some points may overlap). All error bars are the standard error of the mean (SEM).

Fig 6.. Accuracy in delayed probe trials between HML040 and Control Group.

(A). HML040 versus Control Group and Chance Group accuracy averaged across all delayed probes. There was no statistically significant difference between HML and controls although HML040 performed significantly better than chance, as indicated by the mixed surrogate chance group. (B). HML040 versus Control Group accuracy for novel and repeated trials. Despite having a smaller distance from the target on novel trials compared to the control group, for both repeated and novel trials, HML040 did not perform statistically different from the controls. Distance error is the Euclidean distance between where participants placed the targets and where they were actually located in the virtual environment. Novel locations were those in which a start location-target location pairing was new to the participants and Repeated trials were those in which a start location-target location pairing was previously seen. Grey dots represent the control group’s data (some points may overlap). All error bars are the standard error of the mean (SEM).

Figure 7.. HML040 versus Control Group on the moved mountain weight values.

HML040 is not significantly different than the control group in terms of weighting beacon vs. allocentric cues based on the response distance from where the target would be if it moved with the mountain (EMM) over that same distance added to their response distance from the actual static location of the target (EMM + E3M). Grey dots represent the control group’s data (some points may overlap). All error bars are the standard error of the mean (SEM).