Metabolic and Functional Connectivity Changes in Mal de Debarquement Syndrome

PLOS ONE, Dec 2019

Background Individuals with mal de debarquement syndrome (MdDS) experience a chronic illusion of self-motion triggered by prolonged exposure to passive motion, such as from sea or air travel. The experience is one of rocking dizziness similar to when the individual was originally on the motion trigger such as a boat or airplane. MdDS represents a prolonged version of a normal phenomenon familiar to most individuals but which persists for months or years in others. It represents a natural example of the neuroplasticity of motion adaptation. However, the localization of where that motion adaptation occurs is unknown. Our goal was to localize metabolic and functional connectivity changes associated with persistent MdDS. Methods Twenty subjects with MdDS lasting a median duration of 17.5 months were compared to 20 normal controls with 18F FDG PET and resting state fMRI. Resting state metabolism and functional connectivity were calculated using age, grey matter volume, and mood and anxiety scores as nuisance covariates. Results MdDS subjects showed increased metabolism in the left entorhinal cortex and amygdala (z>3.3). Areas of relative hypometabolism included the left superior medial gyrus, left middle frontal gyrus, right amygdala, right insula, and clusters in the left superior, middle, and inferior temporal gyri. MdDS subjects showed increased connectivity between the entorhinal cortex/amygdala cluster and posterior visual and vestibular processing areas including middle temporal gyrus, motion sensitive area MT/V5, superior parietal lobule, and primary visual cortex, while showing decreased connectivity to multiple prefrontal areas. Conclusion These data show an association between resting state metabolic activity and functional connectivity between the entorhinal cortex and amygdala in a human disorder of abnormal motion perception. We propose a model for how these biological substrates can allow a limited period of motion exposure to lead to chronic perceptions of self-motion.

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Metabolic and Functional Connectivity Changes in Mal de Debarquement Syndrome

Citation: Cha Y-H, Chakrapani S, Craig A, Baloh RW ( Metabolic and Functional Connectivity Changes in Mal de Debarquement Syndrome Yoon-Hee Cha 0 Shruthi Chakrapani 0 Alexis Craig 0 Robert W. Baloh 0 Matthew Thurtell, University of Iowa, United States of America 0 1 Department of Neurology, University of California Los Angeles , Los Angeles , California, United States of America, 2 Semel/Resnick Institute, University of California Los Angeles , Los Angeles , California, United States of America, 3 Cognitive Sciences, University of California Irvine , Irvine, California , United States of America Background: Individuals with mal de debarquement syndrome (MdDS) experience a chronic illusion of self-motion triggered by prolonged exposure to passive motion, such as from sea or air travel. The experience is one of rocking dizziness similar to when the individual was originally on the motion trigger such as a boat or airplane. MdDS represents a prolonged version of a normal phenomenon familiar to most individuals but which persists for months or years in others. It represents a natural example of the neuroplasticity of motion adaptation. However, the localization of where that motion adaptation occurs is unknown. Our goal was to localize metabolic and functional connectivity changes associated with persistent MdDS. Methods: Twenty subjects with MdDS lasting a median duration of 17.5 months were compared to 20 normal controls with 18F FDG PET and resting state fMRI. Resting state metabolism and functional connectivity were calculated using age, grey matter volume, and mood and anxiety scores as nuisance covariates. Results: MdDS subjects showed increased metabolism in the left entorhinal cortex and amygdala (z.3.3). Areas of relative hypometabolism included the left superior medial gyrus, left middle frontal gyrus, right amygdala, right insula, and clusters in the left superior, middle, and inferior temporal gyri. MdDS subjects showed increased connectivity between the entorhinal cortex/amygdala cluster and posterior visual and vestibular processing areas including middle temporal gyrus, motion sensitive area MT/V5, superior parietal lobule, and primary visual cortex, while showing decreased connectivity to multiple prefrontal areas. Conclusion: These data show an association between resting state metabolic activity and functional connectivity between the entorhinal cortex and amygdala in a human disorder of abnormal motion perception. We propose a model for how these biological substrates can allow a limited period of motion exposure to lead to chronic perceptions of self-motion. - Funding: This work was funded by the National Institutes of Health/National Institute on Deafness and Other Communication Disorders, NIH/NIDCD R03 DC010451, University of California, Los Angeles UCLA GCRC M01-RR000865, and the Mal de Debarquement Syndrome (MdDS) Balance Foundation Early Career Award. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. In an 1881 article in the Lancet, J.A. Irwin wrote about a common phenomenon that occurs after sea travel: This leads to the question of how all the phenomena of seasickness have usually a rapid tendency to pass away the new habit may become so strong that a disturbance of it, by a return to the land, will be marked by similar phenomena; hence the unsteady gait sometimes observableafter a long and stormy voyage [1]. The unsteadiness that occurs after one disembarks from a boat or plane is a common phenomenon that normally ceases within two days of returning to land [2,3]. However, in some individuals, a sensation that they are still rocking on the boat persists for months or years leading to imbalance, visuospatial problems, and cognitive dysfunction [4]. When this phenomenon becomes persistent, it is formally known as mal de debarquement syndrome, literally meaning the sickness of disembarkment (MdDS) [5]. Very little is known about the underlying neurobiology that leads to persistent MdDS as there are no scientific studies that have established the underlying anatomical cause of this perceptual disorder. Case series have shown that there are no inner ear or structural brain abnormalities associated with MdDS, which is not unexpected since the triggers that lead to persistent MdDS such as going on a cruise, flying in an airplane, or driving for long distances are unlikely to cause structural brain or inner ear damage [4]. However, MdDS may be a disorder of neuroplasticity in which entrainment to a periodically moving environment changes the functional state of the brain making it difficult to readapt to stable land conditions. Individuals with MdDS feel much better when back in motion again, such as getting back on the boat or driving in a car [4,6]. The inability to shut off the mechanisms that become activated during motion (...truncated)


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Yoon-Hee Cha, Shruthi Chakrapani, Alexis Craig, Robert W. Baloh. Metabolic and Functional Connectivity Changes in Mal de Debarquement Syndrome, PLOS ONE, 2012, Volume 7, Issue 11, DOI: 10.1371/journal.pone.0049560