To explore the surrounding environment our brain must be able to recognize, memorize and recall specific places in the world. More specifically, forming and memorizing a mental image (i.e., a cognitive map) of a specific place plays a crucial role in our ability to navigate the spatial world. For this reason, it is plausible that being a good imager might enhance the skills to navigate in the environment. Over the past two decades, some important issues have been clarified regarding the link between imagery and navigational performance. Recently, functional resonance imaging (fMRI) studies clarified that voluntary mental imagery activates several brain regions spanning from frontal areas, such as the dorsal and ventral prefrontal cortex, to medial and temporal areas such as the hippocampus and category-selective regions (Mechelli, 2004; Ranganath and D’Esposito, 2005; Pearson and Westbrook, 2015). A top-down model has been introduced and proposes that mental images are organized and controlled by frontal regions including the inferior frontal gyrus and anterior cingulate cortex (Fulford et al., 2018), information stored in memory is retrieved in medial temporal areas such as the hippocampus, and the content-specific representation of the mental images activates regions in the most posterior part of the brain (Dijkstra et al., 2017). Indeed, the specific content of a mental image activates different brain regions, similarly to what happens during visual perception (Ganis et al., 2004). For instance, imagining a face leads to activation of the fusiform face area (FFA), a brain area activated during face perception; similarly, imaging a scene leads to activation of ventromedial posterior cortical regions (scene-selective regions), which are known to be activated during scene and landscape perception (Epstein and Baker, 2019).
The scene-selective regions include at least three visual cortical areas responding selectively to scenes, compared to other category images such as faces and objects. Specifically, these regions are termed the Parahippocampal Place Area (PPA), the Retrosplenial Complex (RSC), and the Occipital Place Area (OPA), which are temporal, medial, and occipital areas respectively. These regions play different and complementary roles, and several neuroimaging studies demonstrated the contribution of each aforementioned brain region in scene processing. PPA, located at the boundary between the posterior parahippocampal cortex and the anterior lingual gyrus, is activated by passive viewing of real-world scenes or landmarks (Epstein and Kanwisher, 1998); The Retrosplenial complex extends from the retrosplenial cortex itself, located posteriorly to the corpus callosum, through the posterior cingulate cortex to the anterior bank of the parietal-occipital fissure (Burles et al., 2017). RSC is mostly active during both real and imagined navigation (Maguire, 2001; Ino et al., 2002; Wolbers, 2005), retrieval of environment-centered information (Committeri et al., 2004; Galati et al., 2010), and is selectively sensitive to a change in point of view (Sulpizio et al., 2016), mental imagery of familiar places (Boccia et al., 2015) and encoding of permanent items (Auger et al., 2012; Auger and Maguire, 2013). More recently, a growing number of studies have disclosed the role of OPA in scene perception. OPA, which is located around the transverse occipital sulcus is retinotopically organized (Nasr et al., 2011) and shows a preference for the lower visual field (Silson et al., 2015), encodes environmental boundaries (Julian et al., 2016) and local navigational affordances (Bonner and Epstein, 2017), and represents motion information in the immediately visible scene from a first-person perspective (Kamps et al., 2016). These results suggest that OPA is specialized in encoding both low and high-level characteristics such as environmental affordances of a scene (Epstein and Baker, 2019) and might be a primary site toward higher cortical regions.
Several neuroimaging human studies revealed that PPA, RSC, and OPA are strongly interconnected. Studying functional connectivity among scene-selective and hippocampal regions at rest, Boccia et al. (Boccia et al., 2017a) found that PPA is connected to occipito-temporal areas including RSC, lingual gyrus, the calcarine cortex, the parieto-occipital sulcus, and the posterior hippocampus. Similarly, Silson et al. (2015) found that OPA is significantly more connected to the posterior portion of the parahippocampal area (pPPA) than to the anterior portion of the parahippocampal area (aPPA) while the retrosplenial complex/medial parietal cortex (MPA) is more strongly connected with aPPA than pPPA. Similar results were obtained by Baldassano et al. (2013)
In summary, PPA, RSC, and OPA are key nodes of a network supporting both perception and imagery of environmental scenes. Although the functional coupling between these regions seems to be well established in humans based on previous resting-state functional imaging studies (Margulies et al., 2009; Nasr et al., 2013), information about the directed causal interactions among PPA, RSC, and OPA is still lacking. Here, we used spectral Dynamic Causal Modelling (DCM) (Friston et al., 2003, 2014) for resting-state fMRI to assess the strength of the influence that these regions exert on each other without any explicit task. After assessing the dynamic functional connectivity in terms of directed effective connectivity among scene-selective regions, we also tested whether individual differences in connectivity estimates could be related to individual differences in mental imagery ability.
By using resting-state functional connectivity, we previously found that the pattern of reciprocal connections between scene-selective regions reflects individual differences in spatial navigation (Sulpizio et al., 2016; Tullo et al., 2018). In particular, the vividness of visual imagery seems to have a key role in a wide range of cognitive abilities (Pearson, 2019), including successful performance on mental rotation (Pazzaglia and Moè, 2013), spatial tasks (Piccardi et al., 2017), and navigation (Marchette et al., 2011; Keogh and Pearson, 2011, 2014). “Seeing with the mind’s eye”, i.e., imaging something, assumes that visual information arises from memory or likewise can be combined and modified to make a strategy or to achieve a goal (Kosslyn et al., 2001). In this sense, having a good imagery ability plays a crucial role in constructing and recalling a schematic representation of the environment (e.g., a map), adapting own position to the surrounding place, and consequently getting the easiest way-finding. In this framework, several studies revealed that individual differences in cognitive style such as visual or verbal strategy (Blazhenkova and Kozhevnikov, 2009, 2010) affect the type of information individuals choose to guide navigation (Pazzaglia and Moè, 2013; Kraemer et al., 2017; Piccardi et al., 2017). Indeed, subjects who select and search for salient landmarks rely on a landmark strategy; subjects who learn the path using egocentric coordinates (for example where to turn, right or left) rely on a route strategy; subjects who use both egocentric and allocentric coordinates rely on a survey strategy and they have a clearer global map of the surrounding environment (Pazzaglia and De Beni, 2001). It has been found that survey individuals re-orient themselves faster than landmarks and route-individuals because they are more independent from the space around them. Mental imagery is at the base of this ability. It has been found that a preference for verbalizing descriptions is useful for retrieving position information but not for giving the relative spatial location, while a visual cognitive strategy is useful for judging relative direction among landmarks (Nori and Giusberti, 2006; Kraemer et al., 2017).
Here we used DCM applied to rs-fMRI and a self-report questionnaire on mental imagery skills, which assess the vividness of visual mental images (Vividness of Visual Imagery Questionnaire, VVIQ) (Marks, 1973), to test the hypothesis that individual differences in mental imagery abilities account for how scene-selective regions interact with each other. Results of this study point out that causal information flow among scene-selective regions is relevant to understand individual differences, in particular mental imagery ability that plays a crucial role in successful navigation in the surrounding environment.