Beyond Dizziness: Virtual Navigation, Spatial Anxiety and Hippocampal Volume in Bilateral Vestibulopathy

Abstract

Bilateral vestibulopathy (BVP) is defined as the impairment or loss of function of either the labyrinths or the eighth nerves. Patients with total BVP due to bilateral vestibular nerve section exhibit difficulties in spatial memory and navigation and show a loss of hippocampal volume. In clinical practice, most patients do not have a complete loss of function but rather an asymmetrical residual functioning of the vestibular system. The purpose of the current study was to investigate navigational ability and hippocampal atrophy in BVP patients with residual vestibular function. Fifteen patients with BVP and a group of age- and gender- matched healthy controls were examined. Self-reported questionnaires on spatial anxiety and wayfinding were used to assess the applied strategy of wayfinding and quality of life. Spatial memory and navigation were tested directly using a virtual Morris Water Maze Task. The hippocampal volume of these two groups was evaluated by voxel-based morphometry. In the patients, the questionnaire showed a higher spatial anxiety and the Morris Water Maze Task a delayed spatial learning performance. MRI revealed a significant decrease in the gray matter mid-hippocampal volume (Left: p = 0.006, Z = 4.58, Right: p < 0.001, Z = 3.63) and posterior parahippocampal volume (Right: p = 0.005, Z = 4.65, Left: p < 0.001, Z = 3.87) compared to those of healthy controls. In addition, a decrease in hippocampal formation volume correlated with a more dominant route-finding strategy. Our current findings demonstrate that even partial bilateral vestibular loss leads to anatomical and functional changes in the hippocampal formation and objective and subjective behavioral deficits.

Keywords: hippocampal atrophy; loss of vestibular function; navigation strategies; spatial anxiety; spatial orientation.

Figure 1

(A) Example of a visual cue as seen from the subject's perspective, while navigating in the platform. (B) Floor plan of the virtual room, indicating the position of the cues and the platform (black square).

Figure 2

Mean (+SEM) measures during the hidden platform training (Phase II) for the control (CON) and bilateral vestibulopathy (BVP) groups; (A) Latency to navigate to the platform, (B) Path length to the platform, expressed as Path Length/Pool Diameter, (C) Heading error. (D–F)represent the same measures averaged over the first 5 and last 5 training blocks. ^*significant group effect at p < 0.05.

Figure 3

Mean (+SEM) measures during the no-platform probe trial (Phase III) for the control (CON) and bilateral vestibulopathy (BVP) groups; (A) Latency to enter the platform quadrant, (B) Path length to the platform quadrant, expressed as Path Length/Pool Diameter, (C) Percent time spent in the platform quadrant, and (D) Percent path length spent in the platform quadrant.

Figure 4

Areas of higher GM volume in healthy controls compared to BVP patients. (A) Clusters of GM differences between the two groups are shown on sagittal and coronal planes through the maximum cluster in the right hemisphere at 28 −22 −9 at p < 0.001 uncorr. and (B) left hemisphere at −28 −25 −17 p < 0.05 FWE corr. Clusters and significance values are from an ROI analysis of the HC and PHC bilaterally and are projected onto a mean image of the included subjects. Color bars indicate the range of t-values. The threshold for statistical significance was 3.69.

Figure 5

The Wayfinding Scale route strategy scores correlate negatively with GM hippocampal volume bilaterally. Results are shown in a sagittal and coronal plane through the peak voxel at −28 −25 −17 and with the PHC GM volume on the right (not visible here). (p < 0.001 uncorr., ROI analysis of the HC and PHC bilaterally). Color bars indicate the range of t-values. The threshold for statistical significance was 3.69. PHC, Parahippocampus; GM, Gray Matter; ROI, Region of Interest; HC, Hippocampus.