Altered spontaneous brain activity patterns in patients with corneal ulcer using amplitude of low‑frequency fluctuation: An fMRI study

Shi,Wen‑Qing; Wu,Wei; Ye,Lei; Jiang,Nan; Liu,Wen‑Feng; Shu,Yong‑Qiang; Su,Ting; Lin,Qi; Min,You‑Lan; Li,Biao; Zhu,Pei‑Wen; Shao,Yi

doi:10.3892/etm.2019.7550

Altered spontaneous brain activity patterns in patients with corneal ulcer using amplitude of low‑frequency fluctuation: An fMRI study

Authors:
- Wen‑Qing Shi
- Wei Wu
- Lei Ye
- Nan Jiang
- Wen‑Feng Liu
- Yong‑Qiang Shu
- Ting Su
- Qi Lin
- You‑Lan Min
- Biao Li
- Pei‑Wen Zhu
- Yi Shao
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, Fujian Provincial Key Laboratory of Ophthalmology and Visual Science, Eye Institute of Xiamen University, Xiamen, Fujian 361102, 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: May 7, 2019 https://doi.org/10.3892/etm.2019.7550
Pages: 125-132
Copyright: © Shi 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

The aim of the present study was to investigate the altered spontaneous brain activity in patients with corneal ulcer (CU) through the amplitude of low‑frequency fluctuation (ALFF) technique and the association with their visual performance. A total of 40 patients with CU and 40 healthy controls (HCs) matched for sex, age and educational level were enrolled. Resting‑state functional magnetic resonance imaging (rs‑fMRI) was performed to examine the probands. Spontaneous cerebral activity variations were investigated using the ALFF technique. The average ALFF values of the CU patients and the HCs were classified by utilizing receiver operating characteristic (ROC) curves. Contrary to HCs, the CU patients had significantly lower ALFF values in the left cerebellar anterior lobe, right middle frontal gyrus and left middle frontal gyrus, but higher ALFF values in the right cerebellar inferior lobe, left cerebellar inferior lobe, left inferior temporal gyrus, right fusiform gyrus, left superior frontal gyrus, right angular gyrus and bilateral superior frontal gyrus. ROC curve analysis of each brain region indicated that the accuracy of ALFF value specificity between the CU and HCs of the area under the curve was perfect. In conclusion, abnormal spontaneous activities were detected in numerous brain regions of CU patients, which may provide useful information for understanding the dysfunction of CU. These activity changes in brain regions may be used as effective clinical indicators for CU.

View Figures

View References

1	Wu J, Zhang WS, Zhao J and Zhou HY: Review of clinical and basic approaches of fungal keratitis. Int J Ophthalmol. 9:1676–1683. 2016.PubMed/NCBI
2	World Health Organization, . Causes of blindness and visual impairment. 2016.
3	Ngoie Maloba V, Ngayuna Nkiene J, Tunku Kabamba G and Chenge Borasisi G: Frequency of corneal ulcer: Retrospective study of 380 cases carried out in two centers in the DR Congo. J Fr Ophtalmol. 41:57–51. 2018.(In French). View Article : Google Scholar : PubMed/NCBI
4	El Sheha H: Self-retained amniotic membrane for dendritic keratitis. Ascrs. 2015.
5	Mascarenhas J, Lalitha P, Prajna NV, Srinivasan M, Das M, D'Silva SS, Oldenburg CE, Borkar DS, Esterberg EJ, Lietman TM and Keenan JD: Acanthamoeba, fungal, and bacterial keratitis: A comparison of risk factors and clinical features. Am J Ophthalmol. 157:56–62. 2014. View Article : Google Scholar : PubMed/NCBI
6	Thomas PA and Kaliamurthy J: Mycotic keratitis: Epidemiology, diagnosis and management. Clin Microbiol Infect. 19:210–220. 2013. View Article : Google Scholar : PubMed/NCBI
7	Bekiesińskafigatowska M, Helwich E, Rutkowska M, Stankiewicz J and Terczyńska I: Magnetic resonance imaging of neonates in the magnetic resonance compatible incubator. Arch Med Sci. 12:1064–1070. 2016. View Article : Google Scholar : PubMed/NCBI
8	Liu H and Wang X: Correlation of iron deposition and change of gliocyte metabolism in the basal ganglia region evaluated using magnetic resonance imaging techniques: An in vivo study. Arch Med Sci. 12:163–171. 2016. View Article : Google Scholar : PubMed/NCBI
9	Dai XJ, Liu CL, Zhou RL, Gong HH, Wu B, Gao L and Wang YX: Long-term sleep deprivation decreases the default spontaneous activity and connectivity pattern in healthy male subjects: A resting-state fMRI study. Neuropsychiatr Dis Treat. 11:761–772. 2015. View Article : Google Scholar : PubMed/NCBI
10	Biswal BB: Resting state fMRI: A personal history. Neuroimage. 62:938–944. 2012. View Article : Google Scholar : PubMed/NCBI
11	Zhang Y, Zhu C, Chen H, Duan X, Lu F, Li M, Liu F, Ma X, Wang Y, Zeng L, et al: Frequency-dependent alterations in the amplitude of low-frequency fluctuations in social anxiety disorder. J Affect Disord. 174:329–335. 2015. View Article : Google Scholar : PubMed/NCBI
12	Zuo XN, Di Martino A, Kelly C, Shehzad ZE, Gee DG, Klein DF, Castellanos FX, Biswal BB and Milham MP: The oscillating brain: Complex and reliable. Neuroimage. 49:1432–1445. 2010. View Article : Google Scholar : PubMed/NCBI
13	Huang X, Cai FQ, Hu PH, Zhong YL, Zhang Y, Wei R, Pei CG, Zhou FQ and Shao Y: Disturbed spontaneous brain-activity pattern in patients with optic neuritis using amplitude of low-frequency fluctuation: A functional magnetic resonance imaging study. Neuropsychiatr Dis Treat. 11:3075–3083. 2015.PubMed/NCBI
14	Huang X, Zhong YL, Zeng XJ, Zhou F, Liu XH, Hu PH, Pei CG, Shao Y and Dai XJ: Disturbed spontaneous brain activity pattern in patients with primary angle-closure glaucoma using amplitude of low-frequency fluctuation: A fMRI study. Neuropsychiatr Dis Treat. 11:1877–1883. 2015.PubMed/NCBI
15	Tan G, Huang X, Zhang Y, Wu AH, Zhong YL, Wu K, Zhou FQ and Shao Y: A functional MRI study of altered spontaneous brain activity pattern in patients with congenital comitant strabismus using amplitude of low-frequency fluctuation. Neuropsychiatr Dis Treat. 12:1243–1250. 2016.PubMed/NCBI
16	Satterthwaite TD, Elliott MA, Gerraty RT, Gerraty RT, Ruparel K, Loughead J, Calkins ME, Eickhoff SB, Hakonarson H, Gur RC, Gur RE and Wolf DH: An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage. 64:240–256. 2013. View Article : Google Scholar : PubMed/NCBI
17	Yan CG, Cheung B, Kelly C, Colcombe S, Craddock RC, Di Martino A, Li Q, Zuo XN, Castellanos FX and Milham MP: A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage. 76:183–201. 2013. View Article : Google Scholar : PubMed/NCBI
18	Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC and Raichle ME: The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA. 102:9673–9678. 2005. View Article : Google Scholar : PubMed/NCBI
19	Li HJ, Dai XJ, Gong HH, Nie X, Zhang W and Peng DC: Aberrant spontaneous low-frequency brain activity in male patients with severe obstructive sleep apnea revealed by resting-state functional MRI. Neuropsychiatr Dis Treat. 11:207–214. 2015.PubMed/NCBI
20	Dai XJ, Peng DC, Gong HH, Wan AL, Nie X, Li HJ and Wang YX: Altered intrinsic regional brain spontaneous activity and subjective sleep quality in patients with chronic primary insomnia: A resting--state fMRI study. Neuropsychiatr Dis Treat. 10:2163–2175. 2014. View Article : Google Scholar : PubMed/NCBI
21	Saad ZS, Gotts SJ, Murphy K, Chen G, Jo HJ, Martin A and Cox RW: Trouble at rest: How correlation patterns and group differences become distorted after global signal regression. Brain Connect. 2:25–32. 2012. View Article : Google Scholar : PubMed/NCBI
22	Zang YF, He Y, Zhu CZ, Cao QJ, Sui MQ, Liang M, Tian LX, Jiang TZ and Wang YF: Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 29:83–91. 2007. View Article : Google Scholar : PubMed/NCBI
23	Siddharth K, Michael AM, Cahill ND, Kiehl KA, Pearlson G, Baum SA and Calhoun VD: ICA-fNORM: Spatial normalization of fMRI data using intrinsic group-ICA networks. Front Syst Neurosci. 5:932011.PubMed/NCBI
24	Japee S, Holiday K, Satyshur MD, Mukai I and Ungerleider LG: A role of right middle frontal gyrus in reorienting of attention: A case study. Front Syst Neurosci. 9:232015. View Article : Google Scholar : PubMed/NCBI
25	Morgan HM, Jackson MC, van Koningsbruggen MG, Shapiro KL and Linden DE: Frontal and parietal theta burst TMS impairs working memory for visual-spatial conjunctions. Brain Stimul. 6:122–129. 2013. View Article : Google Scholar : PubMed/NCBI
26	Chang CC, Yu SC, Mcquoid DR, Messer DF, Taylor WD, Singh K, Boyd BD, Krishnan KR, MacFall JR, Steffens DC and Payne ME: Reduction of dorsolateral prefrontal cortex gray matter in late-life depression. Psychiatry Res. 193:1–6. 2011. View Article : Google Scholar : PubMed/NCBI
27	Nelson JD, Craig JP, Akpek EK, Azar DT, Belmonte C, Bron AJ, Clayton JA, Dogru M, Dua HS, Foulks GN, et al: TFOS DEWS II introduction. Ocul Surf. 15:269–275. 2017. View Article : Google Scholar : PubMed/NCBI
28	Leat SJ: A proposed model for integrated low-vision rehabilitation services in Canada. Optom Vis Sci. 93:77–84. 2016.PubMed/NCBI
29	Bruce ML and Hoff RA: Social and physical health risk factors for first-onset major depressive disorder in a community sample. Soc Psychiatry Psychiatr Epidemiol. 29:165–171. 1994.PubMed/NCBI
30	Ferrari C, Oldrati V, Gallucci M, Vecchi T and Cattaneo Z: The role of the cerebellum in explicit and incidental processing of facial emotional expressions: A study with transcranial magnetic stimulation. Neuroimage. 169:256–264. 2018. View Article : Google Scholar : PubMed/NCBI
31	Adamaszek M, D'Agata F, Ferrucci R, Habas C, Keulen S, Kirkby KC, Leggio M, Mariën P, Molinari M, Moulton E, et al: Consensus paper: Cerebellum and emotion. Cerebellum. 16:552–576. 2017. View Article : Google Scholar : PubMed/NCBI
32	Kilts CD, Kelsey JE, Knight B, Ely TD, Bowman FD, Gross RE, Selvig A, Gordon A, Newport DJ and Nemeroff CB: The neural correlates of social anxiety disorder and response to pharmacotherapy. Neuropsychopharmacology. 31:2243–2253. 2006. View Article : Google Scholar : PubMed/NCBI
33	Dien J, Brian ES, Molfese DL and Gold BT: Combined ERP/fMRI evidence for early word recognition effects in the posterior inferior temporal gyrus. Cortex. 49:2307–2321. 2013. View Article : Google Scholar : PubMed/NCBI
34	Stoeter P, Bauermann T, Nickel R, Corluka L, Gawehn J, Vucurevic G, Vossel G and Egle UT: Cerebral activation in patients with somatoform pain disorder exposed to pain and stress: An fMRI study. Neuroimage. 36:418–430. 2007. View Article : Google Scholar : PubMed/NCBI
35	James CE, Oechslin MS, Van De Ville D, Hauert CA, Descloux C and Lazeyras F: Musical training yields opposite effects on grey matter density in cognitive versus sensorimotor networks. Brain Struct Funct. 219:353–366. 2014. View Article : Google Scholar : PubMed/NCBI
36	Weiner KS: On (ab)normality: Einstein's fusiform gyrus. Brain Cogn. 94:1–3. 2015. View Article : Google Scholar : PubMed/NCBI
37	Caspers J, Palomero-Gallagher N, Caspers S, Schleicher A, Amunts K and Zilles K: Receptor architecture of visual areas in the face and word-form recognition region of the posterior fusiform gyrus. Brain Struct Funct. 220:205–219. 2015. View Article : Google Scholar : PubMed/NCBI
38	Jiang F, Dricot L, Weber J, Righi G, Tarr MJ, Goebel R and Rossion B: Face categorization in visual scenes may start in a higher order area of the right fusiform gyrus: Evidence from dynamic visual stimulation in neuroimaging. J Neurophysiol. 106:2720–36. 2011. View Article : Google Scholar : PubMed/NCBI
39	Yazar Y, Bergström ZM and Simons JS: Continuous theta burst stimulation of angular gyrus reduces subjective recollection. PLoS One. 9:e1104142014. View Article : Google Scholar : PubMed/NCBI
40	Makris N, Preti MG, Wassermann D, Rathi Y, Papadimitriou GM, Yergatian C, Dickerson BC, Shenton ME and Kubicki M: Human middle longitudinal fascicle: Segregation and behavioral-clinical implications of two distinct fiber connections linking temporal pole and superior temporal gyrus with the angular gyrus or superior parietal lobule using multi-tensor tractography. Brain Imaging Behav. 7:335–352. 2013. View Article : Google Scholar : PubMed/NCBI
41	Bocca F, Töllner T, Müller HJ and Taylor PC: The right angular gyrus combines perceptual and response-related expectancies in visual search: TMS-EEG evidence. Brain Stimul. 8:816–822. 2015. View Article : Google Scholar : PubMed/NCBI
42	Goldberg I, Harel M and Malach R: When the brain loses its self: Prefrontal inactivation during sensorimotor processing. Neuron. 50:329–339. 2006. View Article : Google Scholar : PubMed/NCBI
43	Fried I, Wilson C, MacDonald K and Behnke EJ: Electric current stimulates laughter. Nature. 391:6501998. View Article : Google Scholar : PubMed/NCBI
44	Guo MX, Dong HH, Zhang YT, Zhang Q and Yin XH: ALFF changes in brain areas of human with high myopia revealed by resting-state functional MRI. International Conference on Biomedical Engineering and Informatics. IEEE. 91–94. 2010.
45	Li Q, Xin H, Lei Y, Wei R, Zhang Y, Zhong YL, Jiang N and Shao Y: Altered spontaneous brain activity pattern in patients with late monocular blindness in middle-age using amplitude of low-frequency fluctuation: A resting-state functional MRI study. Clin Interv Aging. 11:1773–1780. 2016. View Article : Google Scholar : PubMed/NCBI
46	Tan G, Huang X, Ye L, Wu AH, He LX, Zhong YL, Jiang N, Zhou FQ and Shao Y: Altered spontaneous brain activity patterns in patients with unilateral acute open globe injury using amplitude of low-frequency fluctuation: A functional magnetic resonance imaging study. Neuropsychiatr Dis Treat. 12:2015–2020. 2016. View Article : Google Scholar : PubMed/NCBI
47	Wang ZL, Zou L, Lu ZW, Xie XQ, Jia ZZ, Pan CJ, Zhang GX and Ge XM: Abnormal spontaneous brain activity in type 2 diabetic retinopathy revealed by amplitude of low-frequency fluctuations: A resting-state fMRI study. Clin Radiol. 72:340.e1–340.e7. 2017. View Article : Google Scholar
48	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
49	Pan ZM, Li HJ, Bao J, Jiang N, Yuan Q, Freeberg S, Zhu PW, Ye L, Ma MY, Huang X and Shao Y: Altered intrinsic brain activities in patients with acute eye pain using amplitude of low-frequency fluctuation: A resting-state fMRI study. Neuropsychiatr Dis Treat. 14:251–257. 2018. View Article : Google Scholar : PubMed/NCBI