Aberrant cerebral blood flow and functional connectivity in patients with vestibular migraine: a resting-state ASL and fMRI study

Abstract

Background: Prior neuroimaging studies on vestibular migraine (VM) have extensively certified the functional and structural alterations in multiple brain regions and networks. However, few studies have assessed the cerebral blood flow (CBF) in VM patients using arterial spin labeling (ASL). The present study aimed to investigate CBF and functional connectivity (FC) alterations in VM patients during interictal periods.

Methods: We evaluated 52 VM patients and 46 healthy controls (HC) who received resting-state pseudo-continuous ASL and functional magnetic resonance imaging (fMRI) scanning. Comparisons of voxel-based CBF and seed-based FC were performed between the two groups. Brain regions showed significant group differences in CBF analyses were chosen as seeds in FC analyses. Additionally, the associations between abnormal imaging results and clinical features were explored.

Results: Compared with HC, VM patients showed higher normalized CBF in the right precentral gyrus (PreCG), left postcentral gyrus (PostCG), left superior frontal gyrus and bilateral insular (p < 0.05, FDR corrected). Furthermore, VM patients exhibited increased FC between the right PreCG and areas of the left PostCG, left cuneus and right lingual gyrus (p < 0.05, FDR corrected). In addition, we observed decreased FC between the left insular and regions of the left thalamus and right anterior cingulate cortex, as well as increased FC between the left insular and right fusiform gyrus in VM patients (p < 0.05, FDR corrected). Moreover, these variations in brain perfusion and FC were significantly correlated with multiple clinical features including frequency of migraine symptoms, frequency of vestibular symptoms and disease duration of VM (all p < 0.05).

Conclusions: Patients with VM during interictal period showed hyperperfusion and abnormal resting-state FC in brain regions potentially contributed to disrupted multi-sensory and autonomic processing, as well as impaired ocular motor control, pain modulation and emotional regulation. Our study provided novel insights into the complex neuropathology of VM from a CBF perspective.

Keywords: Arterial spin labeling; Cerebral blood flow; Functional connectivity; Functional magnetic resonance imaging; Migraine; Vestibular migraine.

Fig. 1

Brain regions with significant differences in normalized cerebral blood flow between patients with vestibular migraine and healthy controls (p < 0.05, FDR corrected). FDR, False discovery rate; L, Left; R, Right

Fig. 2

The normalized CBF values of patients with vestibular migraine and healthy controls (all p < 0.0001). IQR, Interquartile range; R-PreCG, Right precentral gyrus; L-PostCG, Left postcentral gyrus; L-SFG, Left superior frontal gyrus

Fig. 3

Brain regions showing significant differences in FC between VM patients and HC when the right precentral gyrus was chosen as a seed (p < 0.05, FDR corrected). Red areas indicate increased FC. FC, Functional connectivity; VM, Vestibular migraine; HC, healthy controls; FDR, False discovery rate; L, Left; R, Right. L-PostCG, Left postcentral gyrus; R-LG, Right lingual gyrus

Fig. 4

Brain regions showing significant differences in FC between VM patients and HC when the left insular was selected as a seed (p < 0.05, FDR corrected). Blue regions denote decreased FC, red areas indicate increased FC. FC, Functional connectivity; VM, Vestibular migraine; HC, healthy controls; FDR, False discovery rate; L, Left; R, Right. L-THA, Left thalamus; R-ACC, Right anterior cingulate cortex; R-FG, Right fusiform gyrus

Fig. 5

The FC values (z-values) of patients with vestibular migraine (VM) and healthy controls (HC) (all p < 0.0001). FC, Functional connectivity; FG, Fusiform gyrus; ACC, Anterior cingulate cortex; PostCG, Postcentral gyrus; LG, Lingual gyrus

Fig. 6

The significant correlations between neuroimaging changes and clinical data in patients with vestibular migraine. (A) Normalized cerebral blood flow (CBF) in left postcentral gyrus was positively correlated with the frequency of migraine symptoms (p = 0.001, r = 0.475); (B) Normalized CBF in left insular was positively correlated with the frequency of vestibular symptoms (p = 0.006, r = 0.407); (C) Functional connectivity (FC) between left insular and left thalamus was negatively correlated with the duration of vestibular migraine (p = 0.011, r= -0.352); (D) FC between right precentral gyrus (PreCG) and right lingual gyrus was positively correlated with the frequency of vestibular symptoms (p = 0.012, r = 0.377)