Hippocampal volume reduction in humans predicts impaired allocentric spatial memory in virtual-reality navigation

Abstract

The extent to which navigational spatial memory depends on hippocampal integrity in humans is not well documented. We investigated allocentric spatial recall using a virtual environment in a group of patients with severe hippocampal damage (SHD), a group of patients with “moderate” hippocampal damage (MHD), and a normal control group. Through four learning blocks with feedback, participants learned the target locations of four different objects in a circular arena. Distal cueswerepresent throughout the experiment to provide orientation.Acircular boundary as well as an intra-arena landmark provided spatial reference frames. During a subsequent test phase, recall of all four objects was tested with only the boundary or the landmark being present. Patients with SHD were impaired in both phases of this task. Across groups, performanceonboth types of spatial recallwashighly correlated withmemoryquotient(MQ),but not with intelligence quotient (IQ), age, or sex. However, both measures of spatial recall separated experimental groupsbeyondwhatwouldbe expected basedonMQ,a widely usedmeasureof generalmemoryfunction. Boundary-based and landmark-based spatial recall were both strongly related to bilateral hippocampal volumes, but not to volumes of the thalamus, putamen, pallidum, nucleus accumbens, or caudate nucleus. The results show that boundary-based and landmark-based allocentric spatial recall are similarly impaired in patients with SHD, that both types of recall are impaired beyond that predicted by MQ, and that recall deficits are best explained by a reduction in bilateral hippocampal volumes.