Abnormal regional spontaneous neural activity and functional connectivity in thyroid-associated ophthalmopathy patients with different activity: a resting-state fMRI study

Mengda Jiang; Haiyang Zhang; Yuting Liu; Shuo Wu; Jialu Qu; Yan Tang; Yang Song; Yinwei Li; Jing Sun; Ling Zhu; Huifang Zhou; Xiaofeng Tao

doi:10.3389/fneur.2023.1199251

Abnormal regional spontaneous neural activity and functional connectivity in thyroid-associated ophthalmopathy patients with different activity: a resting-state fMRI study

Front Neurol. 2023 Jul 5:14:1199251. doi: 10.3389/fneur.2023.1199251. eCollection 2023.

Authors

Mengda Jiang¹, Haiyang Zhang^{2

3}, Yuting Liu^{2

4}, Shuo Wu^{2

4}, Jialu Qu^{2

4}, Yan Tang¹, Yang Song⁵, Yinwei Li^{2

3}, Jing Sun^{2

3}, Ling Zhu¹, Huifang Zhou^{2

3}, Xiaofeng Tao¹

Affiliations

¹ Department of Radiology, Shanghai Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
² Department of Ophthalmology, Shanghai Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
³ Shanghai Key Laboratory of Orbital Diseases and Ocular Oncology, Shanghai, China.
⁴ Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁵ Department of MR Scientific Marketing, Siemens Healthcare, Shanghai, China.

Abstract

Purpose: We aimed to evaluate the spontaneous neuronal activity and functional connectivity pattern variations using resting-state functional magnetic resonance imaging (rs-fMRI) measures, such as amplitude of low-frequency fluctuation (ALFF), fractional amplitude of low-frequency fluctuation (fALFF), and functional connectivity (FC), in patients with thyroid-associated ophthalmopathy (TAO).

Method: A total of 24 active TAO patients, 26 inactive TAO patients, and 27 matched healthy controls (HCs) were included. First, ALFF and fALFF were used to detect local neural activity changes, the MRI data were analyzed, and regions with group differences were taken as seeds. Second, FC analysis was performed to explore the altered connection between seeds and other brain regions. A correlation analysis was performed to assess the relationship between functional brain activity and clinical indices and neuropsychiatric behaviors.

Results: Compared to HCs, both active and inactive TAO patients exhibited significantly lower ALFF values in the right calcarine (Calcarine_R) and left postcentral gyrus (Postcentral_L). Active TAO patients also showed significantly higher ALFF values in the left caudate nucleus (Caudate_L) and increased fALFF values in the superior lobe of the right cerebellum (Cerebelum_Crus1_R). Moreover, both active and inactive TAO patients demonstrated decreased FC within the left postcentral gyrus (Postcentral_L) compared to HCs. Additionally, active TAO patients exhibited lower FC compared to inactive TAO patients. The ALFF values in the Calcarine_R of active TAO patients positively correlated with disease duration (r = 0.5892, p = 0.0049) and the Hamilton Anxiety Rating Scale (HARS; r = 0.5377, p = 0.0119). Furthermore, the ALFF value in the Calcarine_R of inactive TAO patients negatively correlated with visual functioning (r = -0.5449, p = 0.0072), while the ALFF values in the Caudate_L of active TAO patients positively correlated with visual functioning (r = 0.6496, p = 0.0014).

Conclusion: We found that the Caudate_L and Cerebelum_Crus1_R related to motor control and coordination in active TAO patients exhibit significant compensatory mechanisms; whereas, the Calcarine_R and Postcentral_L related to visual and somatosensory cortices show varying degrees of impairment. Our findings complement the functional neural mechanism of TAO.

Keywords: amplitude of low-frequency fluctuation; fractional amplitude of low-frequency fluctuation; functional connectivity; resting-state functional magnetic resonance; thyroid-associated ophthalmopathy.