Altered brain activity in patients with strabismus and amblyopia detected by analysis of regional homogeneity: A resting‑state functional magnetic resonance imaging study

Shao,Yi; Li,Qing‑Hai; Li,Biao; Lin,Qi; Su,Ting; Shi,Wen‑Qing; Zhu,Pei‑Wen; Yuan,Qing; Shu,Yong‑Qiang; He,Ying; Liu,Wen‑Feng; Ye,Lei

doi:10.3892/mmr.2019.10147

Altered brain activity in patients with strabismus and amblyopia detected by analysis of regional homogeneity: A resting‑state functional magnetic resonance imaging study

Authors:
- Yi Shao
- Qing‑Hai Li
- Biao Li
- Qi Lin
- Ting Su
- Wen‑Qing Shi
- Pei‑Wen Zhu
- Qing Yuan
- Yong‑Qiang Shu
- Ying He
- Wen‑Feng Liu
- Lei Ye
View Affiliations

Affiliations: Department of Ophthalmology, The First Affiliated Hospital of Nanchang University, Jiangxi Province Ocular Disease Clinical Research Center, Nanchang, Jiangxi 330006, P.R. China, Eye Institute of Xiamen University, Fujian Provincial Key Laboratory of Ophthalmology and Visual Science, Xiamen, Fujian 361000, P.R. China, Department of Radiology, The First Affiliated Hospital of Nanchang University, Jiangxi Province Medical Imaging Research Institute, Nanchang, Jiangxi 330006, P.R. China
Published online on: April 10, 2019 https://doi.org/10.3892/mmr.2019.10147
Pages: 4832-4840
Copyright: © Shao et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Previous studies have demonstrated that strabismus or amblyopia can result in marked brain function and anatomical alterations. However, differences in spontaneous brain activity in strabismus and amblyopia (SA) patients as compared with control individuals remain unclear. The present study aimed to analyze the potential brain activity changes in SA patients and their association with behavioral performance. In total, 16 patients with SA (10 women and 6 men) and 16 healthy controls (HCs; 6 men and 10 women) with matched age and sex were recruited. All subjects were examined with resting‑state functional magnetic resonance imaging (rs‑fMRI), and changes in the spontaneous brain activity of SA patients were evaluated by the regional homogeneity (ReHo) method. The diagnostic ability of the ReHo method was assessed using receiver operating characteristic (ROC) curve analysis. In addition, the association between the mean ReHo value in different brain regions and the behavioral performance was explored by correlation analysis. It was observed that the ReHo value was significantly increased in SA patients compared with HCs in the following brain regions: left lingual gyrus, right middle occipital gyrus/precuneus, bilateral anterior cingulate, left middle occipital gyrus and bilateral precentral gyrus. By contrast, the ReHo value of the left inferior frontal gyrus was significantly lower than that in HCs. ROC curve analysis indicated that the ReHo method has certain credibility for the diagnosis of SA patients. In addition, no similar changes were detected in other brain regions. These results revealed abnormal spontaneous brain activity in certain parts of the brain in adult patients with SA, which suggests the involvement of the neuropathological or compensatory mechanism in these patients, and may be beneficial for clinical treatment.

View Figures

View References

1	Chen X, Fu Z, Yu J, Ding H, Bai J, Chen J, Gong Y, Zhu H, Yu R and Liu H: Prevalence of amblyopia and strabismus in Eastern China: results from screening of preschool children aged 36–72 months. Br J Ophthalmol. 100:515–519. 2016. View Article : Google Scholar : PubMed/NCBI
2	Lewandowski KB: Strabismus as a possible sign of subclinical muscular dystrophy predisposing to rhabdomyolysis and myoglobinuria: a study of an affected family. Can Anaesth Soc J. 29:372–376. 1982. View Article : Google Scholar : PubMed/NCBI
3	Dickmann A, Petroni S, Salerni A, Parrilla R, Savino G, Battendieri R, Perrotta V, Radini C and Balestrazzi E: Effect of vertical transposition of the medial rectus muscle on primary position alignment in infantile esotropia with A- or V-pattern strabismus. J AAPOS. 15:14–16. 2011. View Article : Google Scholar : PubMed/NCBI
4	Clark RA: The role of extraocular muscle pulleys in incomitant nonparalytic strabismus. Middle East Afr J Ophthalmol. 22:279–285. 2015. View Article : Google Scholar : PubMed/NCBI
5	Oh SY, Clark RA, Velez F, Rosenbaum AL and Demer JL: Incomitant strabismus associated with instability of rectus pulleys. Invest Ophthalmol Vis Sci. 43:2169–2178. 2002.PubMed/NCBI
6	Kekunnaya R and Negalur M: Duane retraction syndrome: causes, effects and management strategies. Clin Ophthal (Auckland, NZ);. 11:19172017. View Article : Google Scholar
7	Breinin GM: In discussion of: De Gindersen T, Zeavin B. Observations on the retraction syndrome of Duane. Arch Ophthalmol. 55:5761956.
8	Parsa CF, Grant PE, Dillon WP Jr, du Lac S and Hoyt WF: Absence of the abducens nerve in Duane syndrome verified by magnetic resonance imaging. Am J Ophthalmol. 125:399–401. 1998. View Article : Google Scholar : PubMed/NCBI
9	Lueder GT, Dunbar JA, Soltau JB, Lee BC and McDermott M: Vertical strabismus resulting from an anomalous extraocular muscle. J AAPOS. 2:126–128. 1998. View Article : Google Scholar : PubMed/NCBI
10	Zhao K and Shi X: Learn new version of Preferred Practice Pattern to further standardize the diagnosis and treatment of amblyopia. Zhonghua Yan Ke Za Zhi. 50:481–484. 2014.(In Chinese). PubMed/NCBI
11	Jin H, Yi JL, Xie H, Xiao F, Wang WJ, Shu XM, Xu YL, Chen SL and Ye WX: A study on visual development among preschool children. Zhonghua yan ke za Zhi. 47:1102–1106. 2011.PubMed/NCBI
12	Avram E and Stănilă A: Functional amblyopia. Oftalmologia. 57:3–8. 2013.(In Romanian). PubMed/NCBI
13	von Noorden GK: Abnormal Binocular Interaction: Evidence in Humans. Strabismus and Amblyopia. Lennerstrand G, von Noorden GK and Campos EC: Wenner-Gren Center International Symposium Series, Palgrave Macmillan; London: pp. 275–284. 1988, View Article : Google Scholar
14	Sjöstrand JB: Form deprivation amblyopia-a treatable cause of blindness. Acta Ophthalmol. 86:s2432010.
15	Wang H, Crewther SG, Liang M, Laycock R, Yu T, Alexander B, Crewther DP, Wang J and Yin Z: Impaired activation of visual attention network for motion salience is accompanied by reduced functional connectivity between frontal eye fields and visual cortex in Strabismic Amblyopia. Front Hum Neurosci. 11:1952017. View Article : Google Scholar : PubMed/NCBI
16	Turner R: Functional Magnetic Resonance Imaging (fMRI). Runehov A.L.C..Oviedo L: Encyclopedia of Sciences and Religions. 2013. pp. 352013
17	Chan ST, Tang KW, Lam KC, Chan LK, Mendola JD and Kwong KK: Neuroanatomy of adult strabismus: A voxel-based morphometric analysis of magnetic resonance structural scans. Neuroimage. 22:986–994. 2004. View Article : Google Scholar : PubMed/NCBI
18	Bi H, Zhang B, Tao X, Harwerth RS, Smith EL III and Chino YM: Neuronal responses in visual area V2 (V2) of macaque monkeys with strabismic amblyopia. Cereb Cortex. 21:2033–2045. 2011. View Article : Google Scholar : PubMed/NCBI
19	Huang X, Li SH, Zhou FQ, Zhang Y, Zhong YL, Cai FQ, Shao Y and Zeng XJ: Altered intrinsic regional brain spontaneous activity in patients with comitant strabismus: a resting-state functional MRI study. Neuropsychiatr Dis Treat. 12:1303–1308. 2016. View Article : Google Scholar : PubMed/NCBI
20	Zang Y, Jiang T, Lu Y, He Y and Tian L: Regional homogeneity approach to fMRI data analysis. Neuroimage. 22:394–400. 2004. View Article : Google Scholar : PubMed/NCBI
21	Tononi G, McIntosh AR, Russell DP and Edelman GM: Functional clustering: Identifying strongly interactive brain regions in neuroimaging data. Neuroimage. 7:133–149. 1998. View Article : Google Scholar : PubMed/NCBI
22	Shao Y, Cai FQ, Zhong YL, Huang X, Zhang Y, Hu PH, Pei CG, Zhou FQ and Zeng XJ: Altered intrinsic regional spontaneous brain activity in patients with optic neuritis: a resting-state functional magnetic resonance imaging study. Neuropsychiatr Dis Treat. 11:3065–3073. 2015. View Article : Google Scholar : PubMed/NCBI
23	Cui Y, Jiao Y, Chen YC, Wang K, Gao B, Wen S, Ju S and Teng GJ: Altered spontaneous brain activity in type 2 diabetes: a resting-state functional MRI study. Diabetes. 63:749–760. 2014. View Article : Google Scholar : PubMed/NCBI
24	Song Y, Mu K, Wang J, Lin F, Chen Z, Yan X, Hao Y, Zhu W and Zhang H: Altered spontaneous brain activity in primary open angle glaucoma: a resting-state functional magnetic resonance imaging study. PLoS One. 9:e894932014. View Article : Google Scholar : PubMed/NCBI
25	Huang X, Li HJ, Ye L, Zhang Y, Wei R, Zhong YL, Peng DC and Shao Y: Altered regional homogeneity in patients with unilateral acute open-globe injury: a resting-state functional MRI study. Neuropsychiatr Dis Treat. 12:1901–1906. 2016. View Article : Google Scholar : PubMed/NCBI
26	Huang X, Ye CL, Zhong YL, Ye L, Yang QC, Li HJ, Jiang N, Peng DC and Shao Y: Altered regional homogeneity in patients with late monocular blindness: a resting-state functional MRI study. Neuroreport. 28:1085–1091. 2017. View Article : Google Scholar : PubMed/NCBI
27	Huang X, Li D, Li HJ, Zhong YL, Freeberg S, Bao J, Zeng XJ and Shao Y: Abnormal regional spontaneous neural activity in visual pathway in retinal detachment patients: a resting-state functional MRI study. Neuropsychiatr Dis Treat. 13:2849–2854. 2017. View Article : Google Scholar : PubMed/NCBI
28	Dai XJ, Gong HH, Wang YX, Zhou FQ, Min YJ, Zhao F, Wang SY, Liu BX and Xiao XZ: Gender differences in brain regional homogeneity of healthy subjects after normal sleep and after sleep deprivation: a resting-state fMRI study. Sleep Med. 13:720–727. 2012. View Article : Google Scholar : PubMed/NCBI
29	Li Y, Liang P, Jia X and Li K: Abnormal regional homogeneity in Parkinson's disease: a resting state fMRI study. Clin Radiol. 71:e28–e34. 2016. View Article : Google Scholar : PubMed/NCBI
30	Holmes D, Rettmann M and Robb R: Visualization in Image-Guided Interventions. Image-Guided Interventions. Peters T and Cleary K: Springer; Boston, MA: 2008, View Article : Google Scholar
31	Harrison BJ and Pantelis C: Gradient-Echo Images. Encyclopedia of Psychopharmacology. Stolerman IP: Springer; Berlin, Heidelberg: 2010
32	Lee HW, Hong SB, Seo DW, Tae WS and Hong SC: Mapping of functional organization in human visual cortex: electrical cortical stimulation. Neurology. 54:849–854. 2000. View Article : Google Scholar : PubMed/NCBI
33	Liang M, Xie B, Yang H, Yin X, Wang H, Yu L, He S and Wang J: Altered interhemispheric functional connectivity in patients with anisometropic and strabismic amblyopia: a resting-state fMRI study. Neuroradiology. 59:517–524. 2017. View Article : Google Scholar : PubMed/NCBI
34	Qi S, Mu YF, Cui LB, Li R, Shi M, Liu Y, Xu JQ, Zhang J, Yang J and Yin H: Association of optic radiation integrity with cortical thickness in children with Anisometropic Amblyopia. Neurosci Bull. 32:51–60. 2016. View Article : Google Scholar : PubMed/NCBI
35	Yang X, Zhang J, Lang L, Gong Q and Liu L: Assessment of cortical dysfunction in infantile esotropia using fMRI. Eur J Ophthalmol. 24:409–416. 2014. View Article : Google Scholar : PubMed/NCBI
36	Schraa-Tam CK, van der Lugt A, Smits M, Frens MA, van Broekhoven PC and van der Geest JN: Differences between smooth pursuit and optokinetic eye movements using limited lifetime dot stimulation: a functional magnetic resonance imaging study. Clin Physiol Funct Imaging. 29:245–254. 2009. View Article : Google Scholar : PubMed/NCBI
37	Uddin LQ: Salience processing and insular cortical function and dysfunction. Nat Rev Neurosci. 16:55–61. 2015. View Article : Google Scholar : PubMed/NCBI
38	Weissman-Fogel I, Moayedi M, Taylor KS, Pope G and Davis KD: Cognitive and default-mode resting state networks: Do male and female brains “rest” differently? Hum Brain Mapp. 31:1713–1726. 2010.PubMed/NCBI
39	Liang M, Xie B, Yang H, Yu L, Yin X, Wei L and Wang J: Distinct patterns of spontaneous brain activity between children and adults with anisometropic amblyopia: a resting-state fMRI study. Graefes Arch Clin Exp Ophthalmol. 254:569–576. 2016. View Article : Google Scholar : PubMed/NCBI
40	Huang X, Li H-J, Zhang Y, Peng DC, Hu PH, Zhong YL, Zhou FQ and Shao Y: Microstructural changes of the whole brain in patients with comitant strabismus: evidence from a diffusion tensor imaging study. Neuropsychiatr Dis Treat. 12:2007–2014. 2016. View Article : Google Scholar : PubMed/NCBI
41	Wandell BA, Dumoulin SO and Brewer AA: Visual field maps in human cortex. Neuron. 56:366–383. 2007. View Article : Google Scholar : PubMed/NCBI
42	Yan X, Lin X, Wang Q, Zhang Y, Chen Y, Song S and Jiang T: Doral visual pathway changes in patients with comitant extropia. PLoS ONE 5 (6). e109312010. View Article : Google Scholar
43	Jia CH, Lu GM, Zhang ZQ, Wang Z, Huang W, Ma F, Yin J, Huang ZP and Shao Q: Comparison of deficits in visual cortex between anisometropic and strabismic amblyopia by fMRI retinotopic mapping. Zhonghua Yi Xue Za Zhi. 90:1446–1452. 2010.(In Chinese). PubMed/NCBI
44	San Pedro EC, Mountz JM, Ojha B, Khan AA, Liu HG and Kuzniecky RI: Anterior cingulate gyrus epilepsy: the role of ictal rCBF SPECT in seizure localization. Epilepsia. 41:594–600. 2000. View Article : Google Scholar : PubMed/NCBI
45	Devinsky O, Morrell M and Vogt BA: Contribution of anterior cingulate cortex to behavior. Brain 118 (Pt 1). 279–306. 1995.
46	Braga AMDS, Fujisao EK, Verdade RC, Paschoalato RP, Paschoalato RP, Yamashita S and Betting LE: Investigation of the cingulate cortex in idiopathic generalized epilepsy. Epilepsia. 56:1803–1811. 2015. View Article : Google Scholar : PubMed/NCBI
47	Alkawadri R, So NK, Van Ness PC and Alexopoulos AV: Cingulate epilepsy: report of 3 electroclinical subtypes with surgical outcomes. JAMA Neurol. 70:995–1002. 2013. View Article : Google Scholar : PubMed/NCBI
48	Unnwongse K, Wehner T and Foldvary-Schaefer N: Mesial frontal lobe epilepsy. J Clin Neurophysiol. 29:371–378. 2012. View Article : Google Scholar : PubMed/NCBI
49	Zhai J, Chen M, Liu L, Zhao X, Zhang H, Luo X and Gao J: Perceptual learning treatment in patients with anisometropic amblyopia: a neuroimaging study. Br J Ophthalmol. 97:1420–1424. 2013. View Article : Google Scholar : PubMed/NCBI
50	Xiao JX, Xie S, Ye JT, Liu HH, Gan XL, Gong GL and Jiang XX: Detection of abnormal visual cortex in children with amblyopia by voxel-based morphometry. Am J Ophthalmol. 143:489–493. 2007. View Article : Google Scholar : PubMed/NCBI
51	Ouyang J, Yang L, Huang X, Zhong YL, Hu PH, Zhang Y, Pei CG and Shao Y: The atrophy of white and gray matter volume in patients with comitant strabismus: evidence from a voxel-based morphometry study. Mol Med Rep. 16:3276–3282. 2017. View Article : Google Scholar : PubMed/NCBI