In this study, we identified four scale-related brain activation patterns during the processing of spatial navigation, with significant differences in brain activation patterns across scales. These findings indicate the existence of unique human navigation strategies at four spatial scales, namely the small scale (between rooms), medium scale (between buildings), large scale (between blocks) and huge scale (between cities, countries and continents). The findings and implications are summarized as below.
First, the results of the comparison between the task and baseline conditions indicated that the middle occipital gyrus was the most important brain region for completing the tasks in this experiment. A previous study reported that the middle occipital gyrus is specialized in processing Chinese characters28. Thus, the observed activation in this region may have been caused by requiring participants to read Chinese words during the experiment. However, another study reported that activation in the middle occipital gyrus was strongly related to successful navigation29. In addition, some previous research suggests that the middle occipital gyrus is involved in object processing30–32, indicating that participants processed knowledge of landmarks located in the navigation scenarios. Furthermore, the middle occipital gyrus is also reported that it plays a role in processing objects at different levels of specificity33, suggesting that participants processed landmarks at different scales with the involvement of the middle occipital gyrus, and that the specification of processed landmarks is dependent on the scale of the navigation scenario. Taken together with these previous findings, the current results suggest that the middle occipital gyrus is a scale-free brain region for human navigation.
The parahippocampal gyrus is an important brain region in spatial processing. The results indicate that activation of the parahippocampal gyrus at the medium scale was significantly greater than that at the small and larger scales. The parahippocampal gyrus is considered to play an important role in view encoding in spatial navigation, particularly for views of buildings34, which may have caused the greater activation observed at the building scale in the current study. Hassabis et al. reported that activation in the parahippocampal gyrus discriminated between different environments35, in accord with the current results, suggesting that the medium scale is a key demarcation in human spatial navigation. These studies provide evidence suggesting that the parahippocampal gyrus discriminates between processing views at different spatial scales. Moreover, the parahippocampal gyrus was reported to be involved in the process of perceiving and using landmarks18, and was strongly activated when participants attempted to increase navigational accuracy36. The current findings suggest that participants paid substantially more attention to retrieving and reusing landmarks based on their memory of routes to complete navigation tasks at the medium scale. In addition, the parahippocampal gyrus is considered to be responsible for the processing of global information about the environment in humans37, receiving egocentric information and converting it to allocentric representations, and helping navigation in an allocentric view36,38. The current findings suggest that participants tended to use an allocentric reference to complete the navigation tasks.
The cingulate gyrus is also a scale-dependent brain region. We found significant differences in anterior cingulate gyrus activation between the medium and huge scales, but not between the small and large scales. Previous studies reported that the anterior cingulate gyrus is related to backtracking strategy39. The anterior cingulate gyrus is also reported to exhibit more activation when participants experience difficulties in navigation tasks36. Therefore, our findings suggest that participants experienced more difficulty and performed more backtracking at the small to large scales. In contrast, at the huge scale, navigation appeared to be easier and more direct. We also found significant differences in posterior cingulate gyrus activation between the medium scale and above, but no differences between the small and medium scales. The posterior cingulate gyrus is thought to be involved in transforming allocentric references to egocentric references40. The current findings and our oral investigation of the route training sessions indicate that, at the small to large scale, participants tended to imagine an abstract structure of the entire environment using an allocentric reference. In addition, at the small to medium scales, participants also switched spatial references frequently. Thus, participants may have been imagining real processes of navigation and processing local information with an egocentric reference.
Activation was influenced by spatial scale in several other brain regions. First, we found a scale-dependent difference in activation in the parietal gyrus. The results indicated that activation in parietal gyrus increased monotonically with spatial scale, in accordance with a previous report by Peers et al. that stated that the parietal gyrus exhibited more activation at large scales6. The parietal gyrus is involved in processing egocentric references41,42. Therefore, our findings suggested that, at the huge scale, participants completed navigation by imagining maps in an egocentric reference frame, in which routes were simplified on the basis of the paths of flights or ships. Second, we found that the temporal gyrus was strongly activated at the huge scale. The temporal gyrus is related to the processing of spatial contextual information for route planning, and distinguishing between navigational episodes43. Some previous studies examining spatial navigation among patients with Alzheimer’s disease suggested that patients suffered from spatial disorientation due to neurodegeneration in the medial temporal gyrus and parietal gyrus44–47. In addition, several studies reported that the parietal gyrus is related to the processing of direction41,48. Therefore, although participants were able to easily plan and navigate along a route, they may have found it harder to determine accurate directions because they naturally retrieved and processed fewer details about the environment compared with the small to large scales.
At all of the scales we investigated, we observed a scale-dependent neural system for human spatial navigation, and there are four typical scale-dependent brain activation patterns and corresponded navigation strategies. In the current study, at the small scale, participants used both egocentric and allocentric references, but processed real and detailed scenario views more, indicating that participants mainly used egocentric references during navigation. At the medium scale, participants used both egocentric and allocentric references, with no obvious differences, and tended to switch reference type frequently to cope with different scenarios during a single navigation task. Participants processed both specific landmark information and abstract route networks. This type of navigation strategy enabled participants to process information comprehensively and navigate more accurately, but also naturally led to a higher level of difficulty in completing tasks. At the large scale, participants mainly used an allocentric reference and processed abstract spatial information, because the amount of information at this spatial scale was overly large for participants to process, and they had to rely on abstract information by simplifying the spatial information into route networks and several key decision points. At the huge scale, participants mainly used an egocentric reference to process undetailed and abstract mental maps. Our findings are consistent with the multiple system theory for spatial representation11, and also verify the fact that human activate a specific neural system6 to accomplish different navigation strategies proper to spatial scales49.
In conclusion, the current study provided whole-brain, voxel-based evidence supporting the role of various brain regions in scale-driven spatial navigation. The current results revealed, for the first time, a scale-dependent neural system that included the parahippocampus, cingulate, parietal and temporal gyrus, and revealed a neural-based division of spatial scale: small scale (room), medium scale (building), large scale (block), and huge scale (city, country and continent). These four scales were associated with obvious differences from the perspective of spatial information processing and spatial referencing, revealing the neuronal basis of the influence of scale on human navigation and spatial cognition. In addition, activity in the middle occipital gyrus was found to be independent of scale in human spatial navigation. Furthermore, this finding provides potentially useful information regarding the design of auto-adapted navigation systems for multi-scale navigation, contributing to the investigation of novel methods for detecting preclinical Alzheimer’s disease via multi-scale navigation tests.