Altered brain network functional connectivity patterns in patients with vestibular migraine diagnosed according to the diagnostic criteria of the Bárány Society and the International Headache Society

Abstract

Background: Vestibular migraine (VM) is considered one of the most common causes of episodic central vestibular disorders, the mechanism of VM is currently still unclear. The development of functional nuclear magnetic resonance (fMRI) in recent years offers the possibility to explore the altered functional connectivity patterns in patients with VM in depth. The study aimed to investigate altered patterns of brain network functional connectivity in patients with VM diagnosed based on the diagnostic criteria of the Bárány Society and the International Headache Society, and hope to provide a scientific theoretical basis for understanding whether VM is a no-structural central vestibular disease, i.e., functional central vestibular disease with altered brain function. Methods: Seventeen patients with VM who received treatment in our hospital from December 2018 to December 2020 were enrolled. Eight patients with migraine and 17 health controls (HCs) were also included. Clinical data of all patients were collected. Blood pressure, blood routine tests and electrocardiography were conducted to exclude other diseases associated with chronic dizziness. Videonystagmography, the vestibular caloric test, the video head impulse test and vestibular-evoked myogenic potentials were measured to exclude peripheral vestibular lesions. MRI was utilized to exclude focal lesions and other neurological diseases. All subjects underwent fMRI. The independent component analysis was performed to explore changes in intra- and inter-network functional connectivity in patients with VM. Results: Among 17 patients with VM, there were 7 males and 10 females with an average age of 39.47 ± 9.78 years old. All patients had a history of migraine. Twelve (70.6%) patients had recurrent spontaneous vertigo, 2 (11.7%) patients had visually induced vertigo, and 3 (17.6%) patients had head motion-induced vertigo. All 17 patients with VM reported worsening of dizziness vertigo during visual stimulation. The migraine-like symptoms were photophobia or phonophobia (n = 15, 88.2%), migraine-like headache (n = 8, 47.1%), visual aura during VM onset (n = 7, 41.2%). 5 (29.4%) patients with VM had hyperactive response during the caloric test, and 12 (70.6%) patients had caloric test intolerance. Eleven (64.7%) patients had a history of motion sickness. Totally 13 independent components were identified. Patients with VM showed decreased functional connectivity in the bilateral medial cingulate gyrus and paracingulate gyrus within sensorimotor network (SMN) compared with HCs. They also showed weakened functional connectivity between auditory network (AN) and anterior default mode network (aDMN) compared with HCs, and enhanced functional connectivity between AN and the salience network (SN) compared with patients with migraine. Conclusion: Patients with vestibular migraine showed obvious altered functional connectivity in the bilateral medial cingulate gyrus and paracingulate gyrus within the SMN. The median cingulate and paracingulate gyri may be impaired, the disinhibition of sensorimotor network and vestibular cortical network may result in a hypersensitivity state (photophobia/phonophobia). Altered functional connectivity between AN and DMN, SN may lead to increased sensitivity to vestibular sensory processing.