Altered functional activity of the precuneus and superior temporal gyrus in patients with residual dizziness caused by benign paroxysmal positional vertigo

Abstract

Objective: Benign paroxysmal positional vertigo (BPPV) is a common clinical vertigo disease, and the most effective treatment for this disease is canal repositioning procedures (CRP). Most patients return to normal after a single treatment. However, some patients still experience residual dizziness (RD) after treatment, and this disease's pathogenesis is currently unclear. The purpose of this study is to explore whether there are abnormal brain functional activities in patients with RD by using resting-state functional magnetic resonance imaging (rs-fMRI) and to provide imaging evidence for the study of the pathogenesis of RD.

Materials and methods: The BPPV patients in the Second Affiliated Hospital of Xuzhou Medical University had been included from December 2021 to November 2022. All patients had been received the collection of demographic and clinical characteristics (age, gender, involved semicircular canal, affected side, CRP times, BPPV course, duration of RD symptoms, and whether they had hypertension, diabetes, coronary heart disease.), scale assessment, including Dizziness Handicap Inventory (DHI), Hamilton Anxiety Inventory (HAMA), Hamilton Depression Inventory (HAMD), rs-fMRI data collection, CRP treatment, and then a one-month follow-up. According to the follow-up results, 18 patients with RD were included. At the same time, we selected 19 healthy individuals from our hospital's physical examination center who matched their age, gender as health controls (HC). First, the amplitude of low-frequency fluctuations (ALFF) analysis method was used to compare the local functional activities of the two groups of subjects. Then, the brain regions with different ALFF results were extracted as seed points. Functional connectivity (FC) analysis method based on seed points was used to explore the whole brain FC of patients with RD. Finally, a correlation analysis between clinical features and rs-fMRI data was performed.

Results: Compared to the HC, patients with RD showed lower ALFF value in the right precuneus and higher ALFF value in the right superior temporal gyrus (STG). When using the right STG as a seed point, it was found that the FC between the right STG, the right supramarginal gyrus (SMG), and the left precuneus was decreased in RD patients. However, no significant abnormalities in the FC were observed when using the right precuneus as a seed point.

Conclusion: In patients with RD, the local functional activity of the right precuneus is weakened, and the local functional activity of the right STG is enhanced. Furthermore, the FC between the right STG, the right SMG, and the left precuneus is weakened. These changes may explain the symptoms of dizziness, floating sensation, walking instability, neck tightness, and other symptoms in patients with RD to a certain extent.

Keywords: amplitude of low frequency fluctuation; benign paroxysmal positional vertigo; functional connectivity; residual dizziness; resting state function magnetic resonance imaging.

Figure 1

(A) Compared to HC, the ALFF value of the right precuneus is decreased in patients with RD (p < 0.05, TFCE permutation test corrected). Blue represents a significant decrease in ALFF value. (B) The z-ALFF value of the right precuneus between the RD group and HC group is statistically different (p < 0.001, uncorrected). The red scatter plot represents the z-ALFF value in the right precuneus of each participant in the RD group, and the blue scatter plot represents the z-ALFF value in the right precuneus of each participant in the HC group. (C) Compared to HC, the ALFF value of the right STG is increased in patients with RD (p < 0.05, TFCE permutation test corrected). Red represents a significant increase in ALFF value. (D) The z-ALFF value of the right STG between the RD and HC group is statistically different (p < 0.001, uncorrected). The red dot represents the z-ALFF value in the right STG of each participant in the RD group, and the blue dot represents the z-ALFF value in the right STG of each participant in the HC group.

Figure 2

(A) Compared to HC, the FC between the right STG and the left precuneus decreases in patients with RD (p < 0.05, TFCE permutation test corrected). Blue represents a significant decrease in functional connectivity. (B) There are statistical differences in FC values between the right STG and the left precuneus between the RD and HC groups (p < 0.001, uncorrected). The red box plot represents the z-FC value between the right STG and the left precuneus in the RD group, and the blue box plot represents the z-FC value between the right STG and the left precuneus in the RD group. (C) Compared to HC, the FC between the right STG and the right SMG decreases in patients with RD (p < 0.05, TFCE permutation test corrected). Blue represents a significant decrease in FC. (D) There are statistical differences in FC values between the right STG and the right SMG between the RD and HC groups (p < 0.001, uncorrected). The red box plot represents the z-FC value between the right STG and the right SMG in the RD group, and the blue box plot represents the z-FC value between the right STG and the right SMG in the RD group. (E) The right STG is used as the seed point. Green represents the right STG.

Figure 3

(A) The z-ALFF value of the right precuneus is negatively correlated with the HAMA anxiety scale in the RD group (r = −0.56, p = 0.01, uncorrected); (B) The z-ALFF value of the right STG is positively correlated with the duration of BPPV in the RD group (r = 0.49, p = 0.03, uncorrected).