Real-world navigation training enhances the stability of large-scale brain connectivity patterns

Spatial navigation involves both egocentric (body-centered) and allocentric (environment-centered) spatial representations, which are hosted in structurally and functionally segregated brain regions. The two types of representations are flexibly weighted in response to changing environmental cues and landmarks during the navigational process, thereby achieving a stable and robust neural code of the target location. However, it remains unknown whether and how improvements in real-world navigational proficiency are related to these two types of spatial representations. In the present study, participants who were unfamiliar with the campus layout (newly arrived university freshmen) received a real-world navigation training for 20 days. Before and after the training, participants received fMRI scanning when they performed a distance judgment task and a paper folding task (as a control). In addition, they were comprehensively tested for their navigational ability via several behavioral tasks (live pointing, offsite direction estimation and offsite distance estimation) outside the scanner. A control group comprised participants who underwent the same fMRI scanning and behavioral tests but did not receive any training. By comparing the training-induced changes in regional activation and task-based global functional connectivity (FC) patterns between the two groups, we investigated the neural correlates of the improvement in real-world navigation performance. We found that the real-world navigation training improved participants' performance during all the behavioral tasks. At the neural level, we observed significant training-induced activation enhancement in the right superior parietal lobule (rSPL), a core brain region that hosts egocentric representation. Moreover, the training increased the global FC pattern stability with the rSPL as the seed region during the distance judgment task, although it had no significant effects on the FC pattern stability during the baseline task. Finally, the increase in global FC pattern stability also predicted individual's improvement in behavioral performance during the distance judgment task. Notably, these effects were found only in the trained group; no similar effects were observed in the control group. These findings indicated that improvement in real-word navigation ability was associated with enhanced egocentric representation. Moreover, the navigation training consolidated the information exchange routes among brain regions, thereby enhancing the precision of cognitive map retrieval. In summary, our study highlights the importance of egocentric representation enhancement in rSPL in improving real-world navigation ability in unfamiliar environments. Furthermore, navigation training facilitates spatial information retrieval by reinforcing the information exchange pathways between the rSPL and other brain areas.