Persistent posterior and transient anterior medial temporal lobe activity during navigation

Abstract

A functional segregation along the posterior-anterior axis of the medial temporal lobe (MTL) has been suggested. In brief, it is thought that the posterior hippocampus represents environmental detail and/or encodes space, whereas the anterior part represents the environment more as a whole and/or subserves behavior. Different phases of navigation should thus recruit different structures within the MTL. Based on animal studies and neuroimaging data from humans, the initial phase of navigation, i.e., self-localization, target localization and path planning, should depend on the anterior MTL independent of upcoming navigational demands, whereas posterior MTL should be active throughout navigation. We tested this prediction using fMRI with navigation in a learned large-scale virtual office landscape with numerous complex landmarks under different navigational conditions. The initial navigational phase specifically engaged the anterior MTL. Increased activity was found bilaterally in the rostral and caudal entorhinal cortex. This is, to our knowledge, the first report of entorhinal activity in virtual navigation detected in a direct comparison. Also bilateral anterior hippocampus and anterior parahippocampal cortex were significantly more active during the initial phase. Activity lasting throughout the navigational period was found in the right posterior hippocampus and parahippocampal cortex. Hippocampal activity for the entire navigation period was only detected when the virtual environment remained unaltered. Navigational success was positively correlated with activity in the anterior right hippocampus for the initial phase, and more posteriorly in the hippocampus for the whole navigation period. Plots of the BOLD signal time course demonstrated that activity in the anterior hippocampus was transient whereas activity in the posterior hippocampus peaked regularly throughout the entire navigation period. These results support a functional segregation within the MTL with regard to navigational phases. The anterior MTL appears to complete associations related to the environment at large and provide a behavioral plan for navigation, whereas the posterior part keeps track of current location.