Individual Differences in Human Path Integration Abilities Correlate with Gray Matter Volume in Retrosplenial Cortex, Hippocampus, and Medial Prefrontal Cortex

Abstract

Humans differ in their individual navigational abilities. These individual differences may exist in part because successful navigation relies on several disparate abilities, which rely on different brain structures. One such navigational capability is path integration, the updating of position and orientation, in which navigators track distances, directions, and locations in space during movement. Although structural differences related to landmark-based navigation have been examined, gray matter volume related to path integration ability has not yet been tested. Here, we examined individual differences in two path integration paradigms: (1) a location tracking task and (2) a task tracking translational and rotational self-motion. Using voxel-based morphometry, we related differences in performance in these path integration tasks to variation in brain morphology in 26 healthy young adults. Performance in the location tracking task positively correlated with individual differences in gray matter volume in three areas critical for path integration: the hippocampus, the retrosplenial cortex, and the medial prefrontal cortex. These regions are consistent with the path integration system known from computational and animal models and provide novel evidence that morphological variability in retrosplenial and medial prefrontal cortices underlies individual differences in human path integration ability. The results for tracking rotational self-motion—but not translation or location—demonstrated that cerebellum gray matter volume correlated with individual performance. Our findings also suggest that these three aspects of path integration are largely independent. Together, the results of this study provide a link between individual abilities and the functional correlates, computational models, and animal models of path integration.

Uniquely excitable neurons enable precise and persistent information transmission through the retrosplenial cortex

“…Subicular neurons, particularly those in the postsubiculum, display a strong preference for particular orientations and are thus called head direction (HD) cells (Taube et al, 1990). When an animal faces a particular direction for long durations, postsubiculum HD cells keep spiking persistently, likely contributing to the maintenance of the sense of orientation in the absence of ongoing vestibular changes (Taube et al, 1990;Chrastil et al, 2017). The unique properties of LR cells suggest they are ideally suited to respond to this persistent subicular input ( Figure 9I-J), enabling the RSC to utilize this valuable head-direction input to help generate a sense of orientation regardless of how long an animal has been facing the same direction.…”

“…It is not yet known whether distinct types of subicular cells (Simonnet and Brecht, 2019;Yamawaki et al, 2019a) differentially contact LR versus RS cells, nor do we yet know the short-term dynamics of subicular inputs to LR versus RS cells. Similarly, it remains to be determined whether LR and RS neurons can independently generate sustained firing in the absence of subicular input: do either LR or RS neurons express the same ion channels that allow postsubicular cells to spike persistently (Chrastil et al, 2017)? Perhaps the single most important gap in the field's knowledge regarding L2/3 RSC neurons is the lack of any information on their in vivo spike patterns and how their firing encodes navigation and memory related information.…”

Everyday taxi drivers: Do better navigators have larger hippocampi?

“…Expert taxi drivers show increased right posterior hippocampal volume but decreased anterior hippocampal volume (Maguire et al, 2000) although these analyses exclude the body of the hippocampus (which we included as part of posterior hippocampus). Yet, anterior hippocampal volume correlates with path integration (Brown, Whiteman, Aselcioglu, & Stern, 2014;Chrastil, Sherrill, Aselcioglu, Hasselmo, & Stern, 2017) and self-reported navigation ability (Wegman et al, 2014). And several studies show correlations between navigation and total hippocampal volume (Hartley & Harlow, 2012;Head & Isom, 2010).…”

Differentiation of mild cognitive impairment using an entorhinal cortex-based test of VR navigation

“…Accurate PI requires the continuous integration of multisensory cues (visual, proprioceptive and vestibular) representing current position and heading direction, in reference to a fixed location (Etienne and Jeffery, 2004;. While several other brain regions have been implicated in PI, including the hippocampus, prefrontal and retrosplenial cortices (Chrastil et al, 2015(Chrastil et al, , 2017, converging evidence from numerous sources indicates that the EC plays a critical role in PI. Human imaging studies demonstrate the EC's role in components of PI such as route planning !…”