This ALE meta-analysis clarified some important issues. First, our finding of converging evidence of a specific and dedicated network for spatial navigation in the human brain (Fig. 4) explains some of the discrepancies in neuroimaging studies and corroborates models of human navigation (Byrne and Becker 2007; Kravitz et al. 2011; Chrastil 2013). Second, going beyond the limitations of the single study approach, our results strongly support the hypothesis that there are different neural substrates for navigating in a well-learned, familiar environment and a recently learned environment. Finally, this analysis helps clarify the extent of the overlap between the brain networks of the egocentric and allocentric strategies employed in navigation (see table S6 in supplementary materials for more details).

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) Full size image

The results of the general ALE meta-analysis emphasize the role of the parahippocampal gyrus and retrosplenial cortex in navigation. Previously, both of these areas were often associated with navigational processes (Epstein 2008; Vann et al. 2009) and were hypothesized to play separate and complementary roles in human navigation (Epstein et al. 2007; Iaria et al. 2007), particularly in the retrieval and localization of visual scenes (Epstein 2008; Hirshhorn et al. 2011). Our findings also confirm involvement of the parietal lobes (Sack 2009) in human navigation as well as the middle occipital gyri bilaterally (Epstein et al. 2007; Rosenbaum et al. 2004) and the caudate nucleus. The importance of the frontal areas in human navigation was confirmed by bilateral activations in the middle frontal gyri, as evidenced by the general ALE. As most studies included in the meta-analysis (Rosenbaum et al. 2004; Spiers and Maguire 2006; Ekstrom and Bookheimer 2008) required that participants “find a way” to perform a navigational problem-solving task, we suggest that the frontal areas may have a significant role in planning navigation, especially when detours are required. As few studies have investigated this point, it is still unclear whether navigational planning and problem solving differ from other types of planning and problem solving from cognitive and neural perspectives. We also observed cerebellar activations, which need to be further investigated.

Paradigms: Recently Learned and Familiar Environments

The contrast between studies using paradigms of familiar environments and recently learned environments resulted in significant differences in both directions. A fronto-temporal-parietal network (including the middle frontal gyrus, posterior cingulate cortex and superior temporal gyrus) seems to be involved in processing F environments (familiar vs. recently learned environments, Fig. 2a), whereas activations of the parahippocampal formation, lingual gyrus and fusiform regions are evidenced by RL environment paradigms (recently learned vs. familiar environments, Fig. 2b). Hirshhorn et al. (2011) observed that degree of familiarity affects the networks involved in navigational tasks. This is also consistent with findings reported in the neuropsychological literature that lesions in the parahippocampal cortex cause anterograde disorientation (i.e., the inability to learn novel routes and create representations of novel environments) but do not affect the ability to orient and navigate in familiar environments, thus sparing spatial knowledge acquired before the lesion (Habib and Sirigu 1987; Aguirre and D’Esposito 1999). This result is also consistent with the Standard model of memory consolidation (Squire and Alvarez 1995), which posited a time-limited role of the hippocampus for declarative memories.

However, we cannot exclude that the possible role of the hippocampal formation in recalling a recently learned environment is consistent with its proposed role in novelty detection and orienting reactions (Vinogradova 2001; Kumaran and Maguire 2005, 2006, 2007). Indeed, according to the multiple trace theory recently acquired environments (at variance with familiar environments) may require further consolidation of memory traces by means of hippocampal activations. Also, as the RL environments are not yet completely consolidated, they may still make use of the hippocampus as a comparator, similar to novel environments when they are being acquired for the first time.

As to familiar environment paradigms, lesions in the posterior cingulate cortex, which is part of the fronto-temporo-parietal network identified in familiar environment paradigms, result in deficits in orienting and navigating in environments that were familiar before the lesion (Aguirre and D’Esposito 1999). Areas involved in the network that processes familiar environments are also strongly related to egocentric spatial representations (Galati et al. 2000) and the translation of representations from allocentric to egocentric formats and vice versa (Byrne and Becker 2007). Thus, lesions in these areas may affect the recall of knowledge about familiar environments and prevent its transformation from an allocentric format stored in long-term memory (Montello 1998) to an egocentric format used for driving actual navigation (Byrne and Becker 2007).

In conclusion, these results suggest that recently learned and familiar environments are processed by recruiting partially different networks. The first network includes the parahippocampal, fusiform and lingual gyri and is involved in processing memories relative to recently learned environments. The second network includes the middle frontal gyrus, posterior cingulate cortex and superior temporal gyrus and is involved in recalling familiar environments.

Spatial Strategies: Allocentric and Egocentric Representations

The ALE analysis of navigational strategies showed that different and only partially overlapping systems are involved in processing allocentric and egocentric strategies. Conjunction analysis between allocentric and egocentric strategies demonstrated that they share a common network of areas (i.e., fusiform gyrus, insula, lingual gyrus, precuneus, cuneus, superior frontal lobe bilaterally, right middle occipital gyrus, left precentral gyrus and middle frontal gyrus).

Interestingly, the individual ALE on allocentric strategies revealed a cluster in the left superior temporal gyrus. The role of this structure in allocentric strategies is consistent with the hypothesis that it contributes to the formation and use of allocentric representations through the processing of categorical spatial relations (van Asselen et al. 2008). In any case, the contrast between allocentric and egocentric studies failed to show any suprathreshold cluster, demonstrating that allocentric encoding recruits a subset of areas also by egocentric encoding, in agreement with Shelton and Gabrieli (2002).

Regarding egocentric strategies, the ALE analysis of egocentric vs. allocentric strategies (Fig. 3) showed activation in the right precuneus and angular gyrus. This finding confirms the existence of a dedicated network for the egocentric representation of space in the right hemisphere, including areas in the parietal cortex (probably related to spatial representation) and the retrosplenial cortex (possibly coding heading vectors by means of head direction cells).

Interestingly, patients with right brain damage often have a deficit in spatial navigation and wayfinding (Aguirre and D’Esposito 1999) and lesions of the right precuneus and angular gyrus lead to egocentric disorientation (Aguirre and D’Esposito 1999). Several studies also suggest that the retrosplenial cortex is involved in egocentric spatial navigation and that its lesioning may lead to a condition called Heading Disorientation (Aguirre and D’Esposito 1999; Takahashi et al. 1997) or Retrosplenial Amnesia (Rudge and Warrington 1991). This network is probably also involved in translating allocentric representations of space into egocentric ones and vice versa (Byrne and Becker 2007).

Some caution is required in interpreting the results of comparison between egocentric and allocentric strategies. First of all, in discussing the differences between allocentric and egocentric strategies, it has to be taken into account that fMRI studies of egocentric navigation are intrinsically limited by the nature of the neuroimaging technique. Indeed, ecological egocentric navigation, especially in animal models, is supposed to heavily depend on internally generated cues, such as idiothetic cues (for example, proprioceptive, vestibular, optic flow inputs). In this light, the mandatory absence of actual motion in fMRI, excluding the presence of any idiothetic cue, affects the egocentric-based processing. This pervasive limitation across fMRI studies of egocentric navigation could account at least in part of the similarity between allocentric and egocentric strategies that resulted from our meta-analysis. Secondly, the a posteriori assignment of the studies to the egocentric and the allocentric navigational strategies could have weakened the differences in the meta-analysis results due to a mis-classification of studies or the overlapping in the strategies that may be used in performing some tasks. Indeed, the authors did not always explicitly report the kind of strategy their study aimed to analyze. However, in all of the studies the type of strategy the authors had sought for their tasks can be easily detected, even when it is not explicitly described in introduction, by the description of tasks themselves and by the discussion, where authors tried to link their functional findings to specific cognitive processes. Moreover, in most of the studies included in the meta-analysis, authors elicited a specific strategy by adopting paradigmatic tasks specifically developed to tap just a definite strategy rather than explicitly instructing subjects to follow that definite strategy. Thus it is possible that, despite the author’s intention to evaluate the neural bases of a navigational strategy (for example egocentric strategy) by means of a paradigmatic task (for example, a route-following task), actually some subjects perform the task by relying on the other strategy (for example, by relying on an allocentric strategy). It should, however, be consider that this is a common problem in cognitive neuroscience, since we can never be completely sure that subjects perform any experimental task by relying on the strategy authors meant to test. In any case, even being cautious, we retain that present results offer import suggestions for understanding the complex human navigational system and also suggest directions for future studies, which should pay attention in the more clearly defining the strategy analyzed and also in contrasting different strategies in the same study.