Efficacy of navigation may be influenced by retrosplenial cortex-mediated learning of landmark stability.

Stephen D Auger,Eleanor A Maguire,Peter Zeidman

doi:10.1016/j.neuropsychologia.2017.08.012

Abstract

Human beings differ considerably in their ability to orient and navigate within the environment, but it has been difficult to determine specific causes of these individual differences. Permanent, stable landmarks are thought to be crucial for building a mental representation of an environment. Poor, compared to good, navigators have been shown to have difficulty identifying permanent landmarks, with a concomitant reduction in functional MRI (fMRI) activity in the retrosplenial cortex. However, a clear association between navigation ability and the learning of permanent landmarks has not been established. Here we tested for such a link. We had participants learn a virtual reality environment by repeatedly moving through it during fMRI scanning. The environment contained landmarks of which participants had no prior experience, some of which remained fixed in their locations while others changed position each time they were seen. After the fMRI learning phase, we divided participants into good and poor navigators based on their ability to find their way in the environment. The groups were closely matched on a range of cognitive and structural brain measures. Examination of the learning phase during scanning revealed that, while good and poor navigators learned to recognise the environment's landmarks at a similar rate, poor navigators were impaired at registering whether landmarks were stable or transient, and this was associated with reduced engagement of the retrosplenial cortex. Moreover, a mediation analysis showed that there was a significant effect of landmark permanence learning on navigation performance mediated through retrosplenial cortex activity. We conclude that a diminished ability to process landmark permanence may be a contributory factor to sub-optimal navigation, and could be related to the level of retrosplenial cortex engagement.

Highlights

MRI regions of interest (ROIs) We focused on three regions of interest (ROI): retrosplenial cortex (RSC) and posterior parahippocampal cortex (PHC), due to their previously demonstrated roles in processing features of real-world landmarks in association with navigation ability (Auger et al, 2012; Auger and Maguire, 2013; Janzen et al, 2008; Mullally and Maguire, 2011; Troiani et al, 2014), and the hippocampus (HC), which has been associated with navigation expertise (Bohbot et al, 2007; Hartley et al, 2003; Iaria et al, 2008; Janzen et al, 2008; Maguire et al, 2000; Schinazi et al, 2013; Woollett and Maguire, 2011)
While the groups were defined based upon performance in the navigation task, similar significant differences between the two groups were apparent in the sketch map test of the paths and the landmark placement test
Our interest was in good and poor navigators – those who were successful or not at finding their way within this environment after the learning phase. We found that those who were poor at wayfinding were impaired, compared to good navigators, at registering whether landmarks were permanent or transient during learning, and this was associated with reduced activity in RSC

Summary

Introduction

Behavioural and brain differences between good and poor navigators have been widely reported (Auger et al, 2012; Auger and Maguire, 2013; Baumann et al, 2010; Epstein et al, 2005; Hartley et al, 2003; Janzen et al, 2008; Maguire et al, 2000; Ohnishi et al, 2006; Sulpizio et al, 2016; Wegman and Janzen, 2011; Woollett and Maguire, 2011), but the specific causes of navigation variability have been more difficult to determine (Wolbers and Hegarty, 2010). Effective navigation relies upon the formation and utilisation of accurate environmental representations, the bedrock of which are stable landmarks (Burnett et al, 2001; Lynch, 1960; Siegel and White, 1975) These landmarks can be distal, global cues (Doeller et al, 2008) or more proximal objects (Committeri et al, 2004; Galati et al, 2010; Lew, 2011; Marchette et al, 2015, 2014; Yoder et al, 2011), but whatever the size or salience of these permanent, non-moving environmental features, how they are processed by the brain may be related to a person's general navigation ability (Auger et al, 2012; Auger and Maguire, 2013). Other work has revealed that representations of permanence in RSC developed rapidly for completely novel items, and RSC responses directly tracked the emerging knowledge of landmark permanence (Auger et al, 2015)

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Conclusion