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.
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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)