Stereotypical hippocampal clustering predicts navigational success in virtualized real-world environments.

Abstract

Structural differences along the hippocampal long-axis have long been believed to underlie meaningful functional differences. Recent findings show that data-driven parcellations of the hippocampus sub-divide the hippocampus into a 10-cluster map with anterior-medial, anterior-lateral, and posteroanterior-lateral, middle, and posterior components. We tested whether task and experience could modulate this clustering using a spatial learning experiment where male and female participants were trained to virtually navigate a novel neighborhood in a Google Street View-like environment. Participants were scanned while navigating routes early in training and at the end of a two-week training period. Using the 10-cluster map as the ideal template, we find that participants who eventually learn the neighborhood well have hippocampal cluster-maps consistent with the ideal-even on their second day of learning-and their cluster mappings do not deviate over the two week training period. However, participants who eventually learn the neighborhood poorly begin with hippocampal cluster-maps inconsistent with the ideal template, though their cluster mappings may become more stereotypical after the two week training. Interestingly this improvement seems to be route-specific: after some early improvement, when a new route is navigated, participants' hippocampal maps revert back to less stereotypical organization. We conclude that hippocampal clustering is not dependent solely on anatomical structure, and instead is driven by a combination of anatomy, task, and importantly, experience. Nonetheless, while hippocampal clustering can change with experience, efficient navigation depends on functional hippocampal activity clustering in a stereotypical manner, highlighting optimal divisions of processing along the hippocampal anterior-posterior and medial-lateral-axes.Statement of Significance The hippocampus is a brain region important for memory and navigation. Recent research suggests that patterns of processing activity within the hippocampus when people are at rest can reveal distinct areas of processing within it. We extend this work by examining processing in the hippocampus while individuals are learning how to navigate in a new virtual reality environment. Our findings reveal that not only do patterns of activity in the hippocampus reliably separate the hippocampus into sub-components but also that clean functional segmentation of the hippocampus is related to stronger navigational performance. Thus, while individuals can use their hippocampi to process information in different ways, there may be an ideal template to support efficient spatial learning.