Vestibular Loss and Balance Training Cause Similar Changes in Human Cerebral White Matter Fractional Anisotropy

Abstract

Patients with bilateral vestibular loss suffer from severe balance deficits during normal everyday movements. Ballet dancers, figure skaters, or slackliners, in contrast, are extraordinarily well trained in maintaining balance for the extreme balance situations that they are exposed to. Both training and disease can lead to changes in the diffusion properties of white matter that are related to skill level or disease progression respectively. In this study, we used diffusion tensor imaging (DTI) to compare white matter diffusivity between these two study groups and their age- and sex-matched controls. We found that vestibular patients and balance-trained subjects show a reduction of fractional anisotropy in similar white matter tracts, due to a relative increase in radial diffusivity (perpendicular to the main diffusion direction). Reduced fractional anisotropy was not only found in sensory and motor areas, but in a widespread network including long-range connections, limbic and association pathways. The reduced fractional anisotropy did not correlate with any cognitive, disease-related or skill-related factors. The similarity in FA between the two study groups, together with the absence of a relationship between skill or disease factors and white matter changes, suggests a common mechanism for these white matter differences. We propose that both study groups must exert increased effort to meet their respective usual balance requirements. Since balance training has been shown to effectively reduce the symptoms of vestibular failure, the changes in white matter shown here may represent a neuronal mechanism for rehabilitation.

Balance training improves memory and spatial cognition in healthy adults

“…Connections between vestibular nuclei and the cerebellum, hippocampus, as well as prefrontal and parietal cortices provide information for cognitive functions such as spatial functions, navigation and memory 13 , 14 . For example, bilateral vestibular lesions were found to result in decreased performance in spatial memory tasks 15 , hippocampal atrophy 16 , and reduced fractional anisotropy in white matter tracts within the limbic system and the thalamus 17 . Caloric stimulation of the vestibular nuclei in healthy adults, on the other hand, improved verbal and spatial memory 18 and Galvanic vestibular stimulation modulated mental rotation and perspective taking abilities, depending on the threshold of the current 19 , 20 .…”

Hippocampal gray matter volume in bilateral vestibular failure

“…The disease duration in our BVF patients was shorter than in patients who had undergone surgical nerve section due to acoustic neuroma [Brandt et al, ]. However, disease duration is clearly long enough for changes in gray matter and even white matter fractional anisotropy to occur, which may develop even within months during exercise in healthy subjects [Draganski et al, ; zu Eulenburg et al, ; Hummel et al, ]. Conceivably, morphological GMV reduction could have been counterbalanced by compensatory mechanisms, that is, vestibular rehabilitation or altered visual sensitivity in hippocampus with GMV increase in posterior but GMV decrease in anterior hippocampus [Hufner et al, ].…”

Postural Instability in Subjects With Usher Syndrome

“…They also show that sporting activities could modify brain connectivity or plasticity in patients with brain injury or neurodegenerative disorders (39). Hummel et al (40) studied white matter diffusion ability in subjects with bilateral vestibular failure, balance-trained subjects, and controls using diffusion tensor imaging. They found that both groups of subjects showed similar reduction of white matter diffusion in comparison with control subjects.…”

“…These authors suggested that, in both subjects with bilateral vestibular failure and balance-trained subjects, brain connectivity changed as subjects exerted similar effort to reach their respective postural stability. Specific balance training can help improve imbalance in people with a lack of vestibular function by changing the brain connectivity, particularly by increasing the radial diffusivity component in the white matter (40). In the future, studies combining postural measures and specific vestibular and visual rehabilitative therapy for Usher patients will be necessary to assess the progress and improvement of these patients objectively.…”