Abnormal Regional Spontaneous Neural Activity and Functional Connectivity in Thyroid-associated Ophthalmopathy Patients with Different Activity: a Resting-state FMRI Study

Overview

Journal Front Neurol

Specialty Neurology

Date 2023 Jul 21

PMID 37475733

Authors

Mengda Jiang

Haiyang Zhang

Yuting Liu

Shuo Wu

Jialu Qu

Yan Tang

Yang Song

Yinwei Li

Jing Sun

Ling Zhu

Huifang Zhou

Xiaofeng Tao

Affiliations

Soon will be listed here.

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, = 0.0049) and the Hamilton Anxiety Rating Scale (HARS; r = 0.5377, = 0.0119). Furthermore, the ALFF value in the Calcarine_R of inactive TAO patients negatively correlated with visual functioning (r = -0.5449, = 0.0072), while the ALFF values in the Caudate_L of active TAO patients positively correlated with visual functioning (r = 0.6496, = 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.

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References

Bartley G, Gorman C . Diagnostic criteria for Graves' ophthalmopathy. Am J Ophthalmol. 1995; 119(6):792-5. DOI: 10.1016/s0002-9394(14)72787-4. View

Smith T, Janssen J . Insulin-like Growth Factor-I Receptor and Thyroid-Associated Ophthalmopathy. Endocr Rev. 2018; 40(1):236-267. PMC: 6338478. DOI: 10.1210/er.2018-00066. View

Gould D, Roth F, Soparkar C . The diagnosis and treatment of thyroid-associated ophthalmopathy. Aesthetic Plast Surg. 2011; 36(3):638-48. DOI: 10.1007/s00266-011-9843-4. View

Lin I, Lee C, Liao S . Assessing quality of life in Taiwanese patients with Graves' ophthalmopathy. J Formos Med Assoc. 2014; 114(11):1047-54. DOI: 10.1016/j.jfma.2013.12.002. View

Sujanthan S, Shmuel A, Mendola J . Resting-state functional MRI of the visual system for characterization of optic neuropathy. Front Hum Neurosci. 2022; 16:943618. PMC: 9622755. DOI: 10.3389/fnhum.2022.943618. View

Victores A, Takashima M . Thyroid Eye Disease: Optic Neuropathy and Orbital Decompression. Int Ophthalmol Clin. 2015; 56(1):69-79. DOI: 10.1097/IIO.0000000000000101. View

Bartalena L, Piantanida E, Gallo D, Lai A, Tanda M . Epidemiology, Natural History, Risk Factors, and Prevention of Graves' Orbitopathy. Front Endocrinol (Lausanne). 2020; 11:615993. PMC: 7734282. DOI: 10.3389/fendo.2020.615993. View

Kaas J . The functional organization of somatosensory cortex in primates. Ann Anat. 1993; 175(6):509-18. DOI: 10.1016/s0940-9602(11)80212-8. View

Thiebaut de Schotten M, Urbanski M, Valabregue R, Bayle D, Volle E . Subdivision of the occipital lobes: an anatomical and functional MRI connectivity study. Cortex. 2013; 56:121-37. DOI: 10.1016/j.cortex.2012.12.007. View

10.

Zou Q, Zhu C, Yang Y, Zuo X, Long X, Cao Q . An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods. 2008; 172(1):137-41. PMC: 3902859. DOI: 10.1016/j.jneumeth.2008.04.012. View

11.

Qi C, Huang X, Tong Y, Shen Y . Altered Functional Connectivity Strength of Primary Visual Cortex in Subjects with Diabetic Retinopathy. Diabetes Metab Syndr Obes. 2021; 14:3209-3219. PMC: 8286104. DOI: 10.2147/DMSO.S311009. View

12.

Haber S . Corticostriatal circuitry. Dialogues Clin Neurosci. 2016; 18(1):7-21. PMC: 4826773. View

13.

Dai P, Zhang J, Wu J, Chen Z, Zou B, Wu Y . Altered Spontaneous Brain Activity of Children with Unilateral Amblyopia: A Resting State fMRI Study. Neural Plast. 2019; 2019:3681430. PMC: 6683781. DOI: 10.1155/2019/3681430. View

14.

Liang M, Xie B, Yang H, Yu L, Yin X, Wei L . Distinct patterns of spontaneous brain activity between children and adults with anisometropic amblyopia: a resting-state fMRI study. Graefes Arch Clin Exp Ophthalmol. 2015; 254(3):569-76. DOI: 10.1007/s00417-015-3117-9. View

15.

Chen W, Wu Q, Chen L, Zhou J, Chen H, Xu X . Disrupted Spontaneous Neural Activity in Patients With Thyroid-Associated Ophthalmopathy: A Resting-State fMRI Study Using Amplitude of Low-Frequency Fluctuation. Front Hum Neurosci. 2021; 15:676967. PMC: 8226248. DOI: 10.3389/fnhum.2021.676967. View

16.

McAlinden C . An overview of thyroid eye disease. Eye Vis (Lond). 2015; 1:9. PMC: 4655452. DOI: 10.1186/s40662-014-0009-8. View

17.

Grahn J, Parkinson J, Owen A . The cognitive functions of the caudate nucleus. Prog Neurobiol. 2008; 86(3):141-55. DOI: 10.1016/j.pneurobio.2008.09.004. View

18.

Krauzlis R . The control of voluntary eye movements: new perspectives. Neuroscientist. 2005; 11(2):124-37. DOI: 10.1177/1073858404271196. View

19.

Zhu P, Liu Z, Lu Y, Wang Y, Zhang D, Zhao P . Alterations in Spontaneous Neuronal Activity and Microvascular Density of the Optic Nerve Head in Active Thyroid-Associated Ophthalmopathy. Front Endocrinol (Lausanne). 2022; 13:895186. PMC: 9354054. DOI: 10.3389/fendo.2022.895186. View

20.

Chen W, Wu Q, Chen L, Zhou J, Chen H, Xu X . Aberrant brain voxel-wise resting state fMRI in patients with thyroid-associated ophthalmopathy. J Neuroimaging. 2021; 31(4):773-783. DOI: 10.1111/jon.12858. View