Neuropsychology of environmental navigation in humans: review and meta-analysis of FMRI studies in healthy participants

Abstract

In the past 20 years, many studies in the cognitive neurosciences have analyzed human ability to navigate in recently learned and familiar environments by investigating the cognitive processes involved in successful navigation. In this study, we reviewed the main experimental paradigms and made a cognitive-oriented meta-analysis of fMRI studies of human navigation to underline the importance of the experimental designs and cognitive tasks used to assess navigational skills. We performed a general activation likelihood estimation (ALE) meta-analysis of 66 fMRI experiments to identify the neural substrates underpinning general aspects of human navigation. Four individual ALE analyses were performed to identify the neural substrates of different experimental paradigms (i.e., familiar vs. recently learned environments) and different navigational strategies (allocentric vs. egocentric). Results of the general ALE analysis highlighted a wide network of areas with clusters in the occipital, parietal, frontal and temporal lobes, especially in the parahippocampal cortex. Familiar environments seem to be processed by an extended temporal-frontal network, whereas recently learned environments require activation in the parahippocampal cortex and the parietal and occipital lobes. Allocentric strategy is subtended by the same areas as egocentric strategy, but the latter elicits greater activation in the right precuneus, middle occipital lobe and angular gyrus. Our results suggest that different neural correlates are involved in recalling a well-learned or recently acquired environment and that different networks of areas subtend egocentric and allocentric strategies.

Fig. 1

a Results of general ALE meta-analysis: a widespread network of areas seems to subtend the human ability to orient navigation. This network includes the medial temporal lobe, parietal and occipital areas, as well as the cerebellum and frontal lobe. b Areas showing activation in both egocentric and allocentric spatial strategies span from the occipital to the frontal lobe, as revealed by conjunction analysis egocentric [AND] allocentric strategies. c Areas showing activation for both familiar and recently learned environments, as revealed by conjunction analysis F [AND] RL environments

Fig. 2

a Areas showing higher activation for familiar environments than recently learned ones, as revealed in the contrast between F vs. RL environments. This network of areas includes a cluster in the middle temporal gyrus in the right and posterior cingulate cortex, middle frontal gyrus and superior temporal gyrus of the left hemisphere. b Areas showing higher activation of RL than F environments, as revealed by the contrast between RL vs. F environments. This network includes the right parahippocampal gyrus, precuneus, insula and inferior parietal lobule, left cuneus, precuneus and lingual gyrus

Fig. 3

Areas showing higher activation for egocentric than allocentric strategies, as revealed by the contrast between ego vs. allo strategies. A parieto-occipital network that includes the right superior occipital gyrus, angular gyrus and precuneus subtends egocentric representation of space

Fig. 4

a Diagram shows the proposed network of human spatial navigation, as revealed by contrast analysis of paradigms (F vs. RL and RL vs. F). Green rectangle shows the subset of areas of navigation across F environments (MFG middle frontal gyrus, MTG middle temporal gyrus, PCC posterior cingulate cortex). Blue triangle shows the subset of areas involved in processing RL environments (IPL inferior parietal lobule, pCU precuneus, CU cuneus, LG lingual gyrus, PHG parahippocampal gyrus). b Diagram shows the proposed network of human spatial navigation, as revealed by contrast analysis of strategies (ego vs. allo). Red circle shows the subset of areas of egocentric representation of space (SOG superior occipital gyrus, AG angular gyrus, pCU precuneus)