Project Summary Everyday navigation behaviors that may seem mundane to healthy young adults are, at their core, quite complex. Seemingly rote navigation such as driving to the office require coordination of multiple streams of sensory information as well as memory for the global structure and layout of the environment (i.e., a “cognitive map”). Representations of space are often classified into two distinct frames of reference: egocentric – viewpoint-dependent relationships – and allocentric – observer-independent landmark relationships. The inability to reconcile egocentric and allocentric representations leads to disorientation, even in familiar spaces, and is associated with damage to spatial processing networks and regions of the brain including retrosplenial cortex (RSC). This type of disorientation also serves as a marker for preclinical stages of dementia. However, current spatial models of RSC function remain poorly connected with parallel lines of research from episodic memory. This narrow theoretical focus is problematic given the wide range of cognitive processes ascribed to RSC. The most prominent spatial model of RSC function, referred to as the BBB model, posits that RSC primarily supports the flexible use of egocentric and allocentric reference frames by translating between egocentric and allocentric spatial reference frames. Such spatial translator models of RSC are computationally plausible and generally compatible with findings in the navigation and spatial cognition literature, but there has been no direct test of this model in humans. Moreover, few functional neuroimaging studies are designed a priori to directly study RSC function. An alternative model posits that RSC is part of a predictive coding hierarchy. In this comparator model, a general function of RSC is to make predictions about the world based on learned experiences and evaluate the accuracy of these predictions against actual sensory information to resolve any discrepancies and update future predictions (i.e., Bayesian inference). Assumptions for each model will be evaluated during memory for previously learned spatial experiences (slow, Aim 1) as well as for the spatial demands of the previous trial (fast, Aim 2). To accomplish this, state-of-the-art immersive virtual reality techniques will be combined with functional magnetic resonance imaging (fMRI). Receiver operating characteristic approaches as well as advanced univariate and multivariate fMRI analyses will be used to analyze data from novel behavioral paradigms comprising episodic and spatial memory elements. Functional MRI will allow for accurate and non-invasive imaging of RSC during behavior, and novel task manipulations will pit the predictions of RSC comparator and translator models against one another. These experiments will challenge long-standing spatial theories that have not undergone a rigorous test in humans. The findings will close a gap between poorly connected theories of RSC function in spatial cognition and episodic memory.

Project Narrative Navigation is an important aspect of our everyday lives, and one of the key brain structures involved in navigation is the retrosplenial cortex, yet we know very little about its function. The proposed research will challenge classical models of retrosplenial cortex computations that support the flexible use of both viewer- centered and world-centered (map-like) representations in remembering and navigating learned spaces. Advancing theories in the cognitive and neural bases of retrosplenial cortex contributions to learning, memory and navigation will provide insight into disease pathologies associated with insult to this brain region.