Navigation strategies in patients with vestibular loss tested in a virtual reality T-maze

Abstract

During navigation, humans mainly rely on egocentric and allocentric spatial strategies, two different frames 37 of reference working together to build a coherent representation of the environment. Spatial memory deficits 38 during navigation have been repeatedly reported in patients with vestibular disorders. However, little is known 39 about how vestibular disorders can change the use of spatial navigation strategies. Here, we used a new reverse 40 T-maze paradigm in virtual reality to explore whether vestibular loss specifically modifies the use of egocentric 41 or allocentric spatial strategies in patients with unilateral (n = 23) and bilateral (n = 23) vestibular loss 42 compared to healthy volunteers matched for age, sex and education level (n = 23). Results showed that the 43 odds of selecting and using a specific strategy in the T-maze was significantly reduced in both unilateral and 44 bilateral vestibular loss. An exploratory analysis suggests that only right vestibular loss decreased the odds of 45 adopting a spatial strategy, indicating a functional asymmetry of vestibular functions. When considering 46patients who used strategies to navigate, we observed that a bilateral vestibular loss reduced the odds to use of 47 an allocentric strategy, whereas a unilateral vestibular loss decreased the odds to use of an egocentric strategy. 48Age was significantly associated with an overall lower chance to adopt a navigation strategy and, more 49 specifically, with a decrease in the odds of using an allocentric strategy. We did not observe any sex difference 50 in the ability to select and use a specific navigation strategy. Findings are discussed in light of previous studies 51 on visuo-spatial abilities and studies of vestibulo-hippocampal interactions in peripheral vestibular disorders. 52We discuss the potential impact of the history of the disease (chronic stage in patients with a bilateral 53 vestibulopathy vs. subacute stage in patients with a unilateral vestibular loss), of hearing impairment and non-54 specific attentional deficits in patients with vestibular disorders.

Vestibular contribution to spatial orientation and navigation

“…Overall, this pattern reflected a selective deficit in allocentric navigation strategies, which rely on a mental representation of a cognitive map, while visual landmark-based and stimulus-response strategies were used more abundantly, likely in an attempt of functional compensation. Similar results were reported in a recent study, which applied a virtual reversed T-maze paradigm to document a preference for egocentric or allocentric navigation strategies in patients with bilateral or unilateral vestibular loss [35 ▪▪ ]. It was observed that patients with bilateral vestibulopathy had a generally reduced ability to select a specific navigation strategy and specifically had some reduced odds to use an allocentric strategy.…”

Central vestibular networking for sensorimotor control, cognition, and emotion

“…Over the last decades, especially in the last 3 years, there has been increasing evidence from studies in animals [50][51][52] and humans [53][54][55][56] that the central vestibular system has numerous connections with brain areas related to memory, such as thalamic head direction cells, hippocampal place cells, and entorhinal grid cells [57 & ]. Disorders of 'higher' vestibular functions involve more than one sensory modality and cognitive domain and include, for example, hemispatial neglect and room-tilt illusion with a less favourable course if elicited by lesions in the vestibular-dominant right hemisphere [58].…”

Recent developments in the understanding of the interactions between the vestibular system, memory, the hippocampus, and the striatum

“…Gammeri et al (7) studied the navigation strategies of patients with vestibular loss using a virtual reality reverse T-maze to distinguish "allocentric" (a spatial strategy based on external landmarks) and "egocentric" (response, e.g., left vs. right turn) strategies. They compared 23 patients with unilateral vestibular loss (UVL) to 23 with bilateral vestibular loss (BVL) and 23 healthy controls matched for age, sex and education.…”