Partially segregated neural networks for spatial and contextual memory in virtual navigation

Finding our way in a previously learned, ecologically valid environment concurrently involves spatial and contextual cognitive operations. The former process accesses a cognitive map representing the spatial interactions between all paths in the environment. The latter accesses stored associations between landmark objects and their milieu. Here, we aimed at dissociating their neural basis in the context of memory-based virtual navigation. To do so, subjects freely explored a virtual town for 1 h, then were scanned using fMRI while retrieving their way between two locations, under four navigation conditions designed to probe separately or jointly the spatial and contextual memory components. Besides prominent commonalities found in a large hippocampo-neocortical network classically involved in topographical navigation, results yield evidence for a partial dissociation between the brain areas supporting spatial and contextual components of memory-based navigation. Performance-related analyses indicate that hippocampal activity mostly supports the spatial component, whereas parahippocampal activity primarily supports the contextual component. Additionally, the recruitment of contextual memory during navigation was associated with higher frontal, posterior parietal and lateral temporal activity. These results provide evidence for a partial segregation of the neural substrates of two crucial memory components in human navigation, whose combined involvement eventually leads to efficient navigation behavior within a learned environment.