Neural foundations of emerging route knowledge in complex spatial environments

Abstract

Behavioral evidence suggests that spatial knowledge derived from ground-level navigation can consist of both route and survey knowledge. Neuroimaging and lesion studies aiming to identify the neural structures responsible for topographical learning in humans have yielded partially inconsistent results, probably due to the lack of an effective behavioral parameter allowing for a reliable distinction between different representations. Therefore, we employed a novel virtual reality environment that provides accuracy and reaction time measures precisely indicating the emergence of route vs. survey knowledge. Functional magnetic resonance imaging (fMRI) was used to localize brain regions involved in the acquisition of pure route knowledge in the form of associations between consecutive landmark views and the direction of intermediate movements. Participants were scanned during repeated encoding of the complex environment from a first-person, ground-level perspective. Behavioral data revealed emerging route knowledge in 11 out of 14 subjects. Overall comparisons between encoding and control conditions identified activation in medial frontal gyrus, retrosplenial cortex and posterior inferior parietal cortex. Most importantly, only posterior inferior parietal regions showed increasing activation across sessions, thus paralleling behavioral measures of route expertise. Given the established role of the posterior parietal cortex in spatial processing, this area is thought to provide the pivotal spatial link between two landmarks encountered in immediate temporal succession.