Spatial learning in multi-scale environments: Roles of hippocampus, orbitofrontal cortex, and retrosplenial cortex

Abstract

Navigation cognition involves the learning of multi-scale environments and the formation of cognitive maps. How do humans build cognitive maps in multi-scale environments? Cognitive maps are thought to be organized hierarchically, with local representations for subareas and global representations for the entire environment. However, it remains unclear how spatial learning influences the representations of multi-scale environments and their underlying neural mechanisms across different levels of representation. In the current study, we built a virtual environment (VE) with four orthogonally positioned rectangular rooms, each containing eight objects at the corners. Twenty-three healthy subjects completed a four-session spatial memory experiment conducted over two weeks. We measured their brain activity by using BOLD-fMRI at two stages: pre-learning stage and post-learning, when they were judging the relative direction between the objects within the VE. We found that with the progression of learning, the subjects shifted from relying on local, directional cues to using more global representations of the environment. At the neural level, the hippocampus (HIP), retrosplenial cortex (RSC), and orbitofrontal cortex (OFC) played distinct roles in encoding spatial information across the two learning stages. Specifically, after learning, the HIP shifted from local to global representations, while the RSC and OFC supported the integration of spatial information across these representational levels. In addition, the anterior cingulate cortex was involved in forming global representations, facilitating efficient spatial processing as learning advanced. These findings revealed how spatial learning leads to adaptive shifts in brain activity, contributing to the formation of cognitive maps in complex, multi-scale environments. HighlightsO_LIUsing fMRI to study neural mechanisms of cognitive map formation in a multi-scale environment. C_LIO_LIDetected that local and global spatial representations coexist and evolve during spatial learning. C_LIO_LIFound that learning progress is associated with activation changes in the entorhinal cortex, hippocampus, and retrosplenial cortex. C_LIO_LIRevealed the complementary roles of hippocampus and orbitofrontal cortex in representing the environment. C_LIO_LIShowed that the retrosplenial cortex improves both local and global representations, supporting the integration of multi-scale spatial information. C_LI