Abnormal spontaneous brain functional activity in adult patients with amblyopia: a resting-state functional magnetic resonance imaging study_Journal of Biomedical Engineering

Authors：

CHEN Xia ^1,2 , LIAO Meng ^1,2 ,  JIANG Ping ^3,4 ,  LIU Longqian ^1,2 , GONG Qiyong ³

1. Department of Ophthalmology, West China Hospital of Sichuan University, Chengdu 610041, P. R. China;
2. Department of Optometry and Visual Science, West China School of Medicine, Sichuan University, Chengdu 610041, P. R. China;
3. Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu 610041, P. R. China;
4. West China Medical Publishers, West China Hospital of Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

JIANG Ping, Email: jiangping@wchscu.cn; LIU Longqian, Email: b.q15651@hotmail.com

Keywords：

Amblyopia; Resting-state functional magnetic resonance imaging; Amplitude of low-frequency fluctuation; Fractional amplitude of low-frequency fluctuation; Percent amplitude of fluctuation

DOI：

10.7507/1001-5515.202203072

Video：

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Amblyopia is a visual development deficit caused by abnormal visual experience in early life, mainly manifesting as defected visual acuity and binocular visual impairment, which is considered to reflect abnormal development of the brain rather than organic lesions of the eye. Previous studies have reported abnormal spontaneous brain activity in patients with amblyopia. However, the location of abnormal spontaneous activity in patients with amblyopia and the association between abnormal brain function activity and clinical deficits remain unclear. The purpose of this study is to analyze spontaneous brain functional activity abnormalities in patients with amblyopia and their associations with clinical defects using resting-state functional magnetic resonance imaging (fMRI) data. In this study, 31 patients with amblyopia and 31 healthy controls were enrolled for resting-state fMRI scanning. The results showed that spontaneous activity in the right angular gyrus, left posterior cerebellum, and left cingulate gyrus were significantly lower in patients with amblyopia than in controls, and spontaneous activity in the right middle temporal gyrus was significantly higher in patients with amblyopia. In addition, the spontaneous activity of the left cerebellum in patients with amblyopia was negatively associated with the best-corrected visual acuity of the amblyopic eye, and the spontaneous activity of the right middle temporal gyrus was positively associated with the stereoacuity. This study found that adult patients with amblyopia showed abnormal spontaneous activity in the angular gyrus, cerebellum, middle temporal gyrus, and cingulate gyrus. Furthermore, the functional abnormalities in the cerebellum and middle temporal gyrus may be associated with visual acuity defects and stereopsis deficiency in patients with amblyopia. These findings help explain the neural mechanism of amblyopia, thus promoting the improvement of the treatment strategy for amblyopia.

Citation： CHEN Xia, LIAO Meng, JIANG Ping, LIU Longqian, GONG Qiyong. Abnormal spontaneous brain functional activity in adult patients with amblyopia: a resting-state functional magnetic resonance imaging study. Journal of Biomedical Engineering, 2022, 39(4): 759-766. doi: 10.7507/1001-5515.202203072 Copy

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3.	Kumaran S E, Khadka J, Baker R, et al. Functional limitations recognised by adults with amblyopia and strabismus in daily life: a qualitative exploration. Ophthal and Physl Opt, 2019, 39(3): 131-140.
4.	Fu Zhujun, Hong Hao, Su Zhicai, et al. Global prevalence of amblyopia and disease burden projections through 2040: a systematic review and meta-analysis. Br J Ophthalmol, 2020, 104(8): 1164-1170.
5.	Huang Dan, Chen Xuejuan, Zhu Hui, et al. Prevalence of amblyopia and its association with refraction in Chinese preschool children aged 36-48 months. Br J Ophthalmol, 2018, 102(6): 767-771.
6.	Conner I P, Odom J V, Schwartz T L, et al. Monocular activation of V1 and V2 in amblyopic adults measured with functional magnetic resonance imaging. J AAPOS, 2007, 11(4): 341-350.
7.	Tavor I, Parker J O, Mars R B, et al. Task-free MRI predicts individual differences in brain activity during task performance. Science, 2016, 352(6282): 216-220.
8.	Yang Xubo, Lu Lu, Li Qian, et al. Altered spontaneous brain activity in patients with strabismic amblyopia: A resting-state fMRI study using regional homogeneity analysis. Exp Ther Med, 2019, 18(5): 3877-3884.
9.	Zang Yufeng, He Yong, Zhu Chaozhe, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev, 2007, 29(2): 83-91.
10.	Zhang Jianfeng, Liu Dongqiang, Qian Shufang, et al. The neural correlates of amplitude of low-frequency fluctuation: a multimodal resting-state MEG and fMRI-EEG study. Cereb Cortex, 2022. DOI: 10.1093/cercor/bhac124.
11.	Dai Peishan, Zhang Jinlong, Wu Jing, et al. Altered spontaneous brain activity of children with unilateral amblyopia: A resting state fMRI study. Neural Plast, 2019, 2019: 1-10.
12.	Tang Angcang, Chen Taolin, Zhang Junran, et al. Abnormal spontaneous brain activity in patients with anisometropic amblyopia using resting-state functional magnetic resonance imaging. J Pediat Ophth Strab, 2017, 54(5): 303-310.
13.	Zou Qihong, Zhu Chaozhe, Yang Yihong, et al. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: Fractional ALFF. J Neurosci Meth, 2008, 172(1): 137-141.
14.	Jia Xize, Sun Jiawei, Ji Gongjun, et al. Percent amplitude of fluctuation: A simple measure for resting-state fMRI signal at single voxel level. Plos One, 2020, 15(1): e227021.
15.	Esteban O, Birman D, Schaer M, et al. MRIQC: Advancing the automatic prediction of image quality in MRI from unseen sites. Plos One, 2017, 12(9): e184661.
16.	Gorgolewski K, Burns C D, Madison C, et al. Nipype: a flexible, lightweight and extensible neuroimaging data processing framework in python. Front Neuroinform, 2011, 5: 13.
17.	Esteban O, Markiewicz C J, Blair R W, et al. fMRIPrep: a robust preprocessing pipeline for functional MRI. Nat Methods, 2019, 16(1): 111-116.
18.	Jenkinson M, Beckmann C F, Behrens T E J, et al. FSL. NeuroImage, 2012, 62(2): 782-790.
19.	Jia Xize, Wang Jue, Sun Haiyang, et al. RESTplus: an improved toolkit for resting-state functional magnetic resonance imaging data processing. Sci Bull, 2019, 64(14): 953-954.
20.	Choi S, Jeong G, Kim Y, et al. Proposal for human visual pathway in the extrastriate cortex by fiber tracking method using diffusion-weighted MRI. NeuroImage, 2020, 220: 117145.
21.	Rolls E T. The cingulate cortex and limbic systems for action, emotion, and memory. Handb Clin Neurol, 2019, 166: 23-37.
22.	Ito S, Stuphorn V, Brown J W, et al. Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science, 2003, 302(5642): 120-122.
23.	Wu Kangrui, Yu Yajie, Tang Liying, et al. Altered brain network centrality in patients with adult strabismus with amblyopia: A resting-state functional magnetic resonance imaging (fMRI) study. Med Sci Monitor, 2020, 26: e925856.
24.	Dai Peishan, Zhou Xiaoyan, Ou Yilin, et al. Altered effective connectivity of children and young adults with unilateral amblyopia: A resting-state functional magnetic resonance imaging study. Front Neurosci, 2021, 15: 657576.
25.	Voogd J, Schraa-Tam C K L, van der Geest J N, et al. Visuomotor cerebellum in human and nonhuman primates. Cerebellum, 2012, 11(2): 392-410.
26.	Alvarez T L, Scheiman M, Morales C, et al. Underlying neurological mechanisms associated with symptomatic convergence insufficiency. Sci Rep, 2021, 11(1): 6545.
27.	James K H, Kersey A J. Dorsal stream function in the young child: an fMRI investigation of visually guided action. Dev Sci, 2018, 21(2): e12546.
28.	Min Youlan, Su Ting, Shu Yongqiang, et al. Altered spontaneous brain activity patterns in strabismus with amblyopia patients using amplitude of low-frequency fluctuation: a resting-state fMRI study. Neuropsych Dis and Treat, 2018, 14: 2351-2359.
29.	Lin Xiaoming, Ding Kun, Liu Yong, et al. Altered spontaneous activity in anisometropic amblyopia subjects: revealed by resting-state fMRI. Plos One, 2012, 8(7): e433738.
30.	Ding Kun, Liu Yong, Yan Xiaohe, et al. Altered functional connectivity of the primary visual cortex in subjects with amblyopia. Neural Plast, 2013, 2013: 1-8.
31.	Niechwiej-Szwedo E, Colpa L, Wong A M F. Visuomotor behaviour in amblyopia: Deficits and compensatory adaptations. Neural Plast, 2019, 2019: 1-18.
32.	Gonzalez E G, Wong A M, Niechwiej-Szwedo E, et al. Eye position stability in amblyopia and in normal binocular vision. Vis Sci, 2012, 53(9): 5386-5394.
33.	Niechwiej-Szwedo E, Goltz H C, Colpa L, et al. Effects of reduced acuity and stereo acuity on saccades and reaching movements in adults with amblyopia and strabismus. Invest Ophth Vis Sci, 2017, 58(2): 914-921.
34.	Vedamurthy I, Knill D C, Huang S J, et al. Recovering stereo vision by squashing virtual bugs in a virtual reality environment. Philos T R Soc B, 2016, 371(1697): 20150264.
35.	Kim H R, Angelaki D E, DeAngelis G C. Gain modulation as a mechanism for coding depth from motion parallax in macaque area MT. J Neurosci, 2017, 37(34): 8180-8197.
36.	Treue S, Maunsell J H R. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature, 1996, 382(6591): 539-541.
37.	Uka T, DeAngelis G C. Linking neural representation to function in stereoscopic depth perception: Roles of the middle temporal area in coarse versus fine disparity discrimination. J Neurosci, 2006, 26(25): 6791-6802.
38.	周朋. 基于静息态功能磁共振成像的弱视患者脑功能研究. 北京: 中国科学院大学, 2016.
39.	Parker A J, Smith J E, Krug K. Neural architectures for stereo vision. Philos Trans R Soc Lond B Biol Sci, 2016, 371(1697): 20150261.
40.	Welchman A E, Deubelius A, Conrad V, et al. 3D shape perception from combined depth cues in human visual cortex. Nat Neurosci, 2005, 8(6): 820-827.
41.	Cottereau B R, Ales J M, Norcia A M. The evolution of a disparity decision in human visual cortex. NeuroImage, 2014, 92: 193-206.
42.	Uji M, Lingnau A, Cavin I, et al. Identifying cortical substrates underlying the phenomenology of stereopsis and realness: A pilot fMRI study. Front Neurosci, 2019, 13: 646.
43.	Kim H R, Angelaki D E, DeAngelis G C. The neural basis of depth perception from motion parallax. Philos Trans R Soc Lond B Biol Sci, 2016, 371(1697): 20150256.
44.	Newsome W T, DeAngelis G C, Cumming B G. Cortical area MT and the perception of stereoscopic depth. Nature, 1998, 394(6694): 677-680.
45.	Wang F, Yang W, Zhang L, et al. Brain activation difference evoked by different binocular disparities of stereograms: An fMRI study. Phys Medica, 2016, 32(10): 1308-1313.
46.	Chen Nihong, Chen Zhimin, Fang Fang. Functional specialization in human dorsal pathway for stereoscopic depth processing. Exp Brain Res, 2020, 238(11): 2581-2588.
47.	Tailor V K, Schwarzkopf D S, Dahlmann-Noor A H. Neuroplasticity and amblyopia: vision at the balance point. Curr Opin Neurol, 2017, 30(1): 74-83.
48.	Ferreri F, Rossini P M. TMS and TMS-EEG techniques in the study of the excitability, connectivity, and plasticity of the human motor cortex. Rev Neurosci, 2013, 24(4): 431-442.
49.	Lou A R, Madsen K H, Paulson O B, et al. Monocular visual deprivation suppresses excitability in adult human visual cortex. Cereb Cortex, 2011, 21(12): 2876-2882.
50.	Tuna A R, Pinto N, Brardo F M, et al. Transcranial magnetic stimulation in adults with amblyopia. J Neuroophthalmol, 2020, 40(2): 185-192.
51.	Donkor R, Silva A E, Teske C, et al. Repetitive visual cortex transcranial random noise stimulation in adults with amblyopia. Sci Rep, 2021, 11(1): 3029.
52.	Erkelens I M, Bobier W R, Macmillan A C, et al. A differential role for the posterior cerebellum in the adaptive control of convergence eye movements. Brain Stimul, 2020, 13(1): 215-228.
53.	Colnaghi S, Colagiorgio P, Ramat S, et al. After effects of cerebellar continuous theta burst stimulation on reflexive saccades and smooth pursuit in humans. Cerebellum, 2017, 16(4): 764-771.

1. Kiorpes L, Daw N. Cortical correlates of amblyopia. Visual Neurosci, 2018, 35: e016.
2. Wallace D K, Repka M X, Lee K A, et al. Amblyopia Preferred Practice Pattern^®. Ophthalmology, 2018, 125(1): 105-142.
3. Kumaran S E, Khadka J, Baker R, et al. Functional limitations recognised by adults with amblyopia and strabismus in daily life: a qualitative exploration. Ophthal and Physl Opt, 2019, 39(3): 131-140.
4. Fu Zhujun, Hong Hao, Su Zhicai, et al. Global prevalence of amblyopia and disease burden projections through 2040: a systematic review and meta-analysis. Br J Ophthalmol, 2020, 104(8): 1164-1170.
5. Huang Dan, Chen Xuejuan, Zhu Hui, et al. Prevalence of amblyopia and its association with refraction in Chinese preschool children aged 36-48 months. Br J Ophthalmol, 2018, 102(6): 767-771.
6. Conner I P, Odom J V, Schwartz T L, et al. Monocular activation of V1 and V2 in amblyopic adults measured with functional magnetic resonance imaging. J AAPOS, 2007, 11(4): 341-350.
7. Tavor I, Parker J O, Mars R B, et al. Task-free MRI predicts individual differences in brain activity during task performance. Science, 2016, 352(6282): 216-220.
8. Yang Xubo, Lu Lu, Li Qian, et al. Altered spontaneous brain activity in patients with strabismic amblyopia: A resting-state fMRI study using regional homogeneity analysis. Exp Ther Med, 2019, 18(5): 3877-3884.
9. Zang Yufeng, He Yong, Zhu Chaozhe, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev, 2007, 29(2): 83-91.
10. Zhang Jianfeng, Liu Dongqiang, Qian Shufang, et al. The neural correlates of amplitude of low-frequency fluctuation: a multimodal resting-state MEG and fMRI-EEG study. Cereb Cortex, 2022. DOI: 10.1093/cercor/bhac124.
11. Dai Peishan, Zhang Jinlong, Wu Jing, et al. Altered spontaneous brain activity of children with unilateral amblyopia: A resting state fMRI study. Neural Plast, 2019, 2019: 1-10.
12. Tang Angcang, Chen Taolin, Zhang Junran, et al. Abnormal spontaneous brain activity in patients with anisometropic amblyopia using resting-state functional magnetic resonance imaging. J Pediat Ophth Strab, 2017, 54(5): 303-310.
13. Zou Qihong, Zhu Chaozhe, Yang Yihong, et al. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: Fractional ALFF. J Neurosci Meth, 2008, 172(1): 137-141.
14. Jia Xize, Sun Jiawei, Ji Gongjun, et al. Percent amplitude of fluctuation: A simple measure for resting-state fMRI signal at single voxel level. Plos One, 2020, 15(1): e227021.
15. Esteban O, Birman D, Schaer M, et al. MRIQC: Advancing the automatic prediction of image quality in MRI from unseen sites. Plos One, 2017, 12(9): e184661.
16. Gorgolewski K, Burns C D, Madison C, et al. Nipype: a flexible, lightweight and extensible neuroimaging data processing framework in python. Front Neuroinform, 2011, 5: 13.
17. Esteban O, Markiewicz C J, Blair R W, et al. fMRIPrep: a robust preprocessing pipeline for functional MRI. Nat Methods, 2019, 16(1): 111-116.
18. Jenkinson M, Beckmann C F, Behrens T E J, et al. FSL. NeuroImage, 2012, 62(2): 782-790.
19. Jia Xize, Wang Jue, Sun Haiyang, et al. RESTplus: an improved toolkit for resting-state functional magnetic resonance imaging data processing. Sci Bull, 2019, 64(14): 953-954.
20. Choi S, Jeong G, Kim Y, et al. Proposal for human visual pathway in the extrastriate cortex by fiber tracking method using diffusion-weighted MRI. NeuroImage, 2020, 220: 117145.
21. Rolls E T. The cingulate cortex and limbic systems for action, emotion, and memory. Handb Clin Neurol, 2019, 166: 23-37.
22. Ito S, Stuphorn V, Brown J W, et al. Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science, 2003, 302(5642): 120-122.
23. Wu Kangrui, Yu Yajie, Tang Liying, et al. Altered brain network centrality in patients with adult strabismus with amblyopia: A resting-state functional magnetic resonance imaging (fMRI) study. Med Sci Monitor, 2020, 26: e925856.
24. Dai Peishan, Zhou Xiaoyan, Ou Yilin, et al. Altered effective connectivity of children and young adults with unilateral amblyopia: A resting-state functional magnetic resonance imaging study. Front Neurosci, 2021, 15: 657576.
25. Voogd J, Schraa-Tam C K L, van der Geest J N, et al. Visuomotor cerebellum in human and nonhuman primates. Cerebellum, 2012, 11(2): 392-410.
26. Alvarez T L, Scheiman M, Morales C, et al. Underlying neurological mechanisms associated with symptomatic convergence insufficiency. Sci Rep, 2021, 11(1): 6545.
27. James K H, Kersey A J. Dorsal stream function in the young child: an fMRI investigation of visually guided action. Dev Sci, 2018, 21(2): e12546.
28. Min Youlan, Su Ting, Shu Yongqiang, et al. Altered spontaneous brain activity patterns in strabismus with amblyopia patients using amplitude of low-frequency fluctuation: a resting-state fMRI study. Neuropsych Dis and Treat, 2018, 14: 2351-2359.
29. Lin Xiaoming, Ding Kun, Liu Yong, et al. Altered spontaneous activity in anisometropic amblyopia subjects: revealed by resting-state fMRI. Plos One, 2012, 8(7): e433738.
30. Ding Kun, Liu Yong, Yan Xiaohe, et al. Altered functional connectivity of the primary visual cortex in subjects with amblyopia. Neural Plast, 2013, 2013: 1-8.
31. Niechwiej-Szwedo E, Colpa L, Wong A M F. Visuomotor behaviour in amblyopia: Deficits and compensatory adaptations. Neural Plast, 2019, 2019: 1-18.
32. Gonzalez E G, Wong A M, Niechwiej-Szwedo E, et al. Eye position stability in amblyopia and in normal binocular vision. Vis Sci, 2012, 53(9): 5386-5394.
33. Niechwiej-Szwedo E, Goltz H C, Colpa L, et al. Effects of reduced acuity and stereo acuity on saccades and reaching movements in adults with amblyopia and strabismus. Invest Ophth Vis Sci, 2017, 58(2): 914-921.
34. Vedamurthy I, Knill D C, Huang S J, et al. Recovering stereo vision by squashing virtual bugs in a virtual reality environment. Philos T R Soc B, 2016, 371(1697): 20150264.
35. Kim H R, Angelaki D E, DeAngelis G C. Gain modulation as a mechanism for coding depth from motion parallax in macaque area MT. J Neurosci, 2017, 37(34): 8180-8197.
36. Treue S, Maunsell J H R. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature, 1996, 382(6591): 539-541.
37. Uka T, DeAngelis G C. Linking neural representation to function in stereoscopic depth perception: Roles of the middle temporal area in coarse versus fine disparity discrimination. J Neurosci, 2006, 26(25): 6791-6802.
38. 周朋. 基于静息态功能磁共振成像的弱视患者脑功能研究. 北京: 中国科学院大学, 2016.
39. Parker A J, Smith J E, Krug K. Neural architectures for stereo vision. Philos Trans R Soc Lond B Biol Sci, 2016, 371(1697): 20150261.
40. Welchman A E, Deubelius A, Conrad V, et al. 3D shape perception from combined depth cues in human visual cortex. Nat Neurosci, 2005, 8(6): 820-827.
41. Cottereau B R, Ales J M, Norcia A M. The evolution of a disparity decision in human visual cortex. NeuroImage, 2014, 92: 193-206.
42. Uji M, Lingnau A, Cavin I, et al. Identifying cortical substrates underlying the phenomenology of stereopsis and realness: A pilot fMRI study. Front Neurosci, 2019, 13: 646.
43. Kim H R, Angelaki D E, DeAngelis G C. The neural basis of depth perception from motion parallax. Philos Trans R Soc Lond B Biol Sci, 2016, 371(1697): 20150256.
44. Newsome W T, DeAngelis G C, Cumming B G. Cortical area MT and the perception of stereoscopic depth. Nature, 1998, 394(6694): 677-680.
45. Wang F, Yang W, Zhang L, et al. Brain activation difference evoked by different binocular disparities of stereograms: An fMRI study. Phys Medica, 2016, 32(10): 1308-1313.
46. Chen Nihong, Chen Zhimin, Fang Fang. Functional specialization in human dorsal pathway for stereoscopic depth processing. Exp Brain Res, 2020, 238(11): 2581-2588.
47. Tailor V K, Schwarzkopf D S, Dahlmann-Noor A H. Neuroplasticity and amblyopia: vision at the balance point. Curr Opin Neurol, 2017, 30(1): 74-83.
48. Ferreri F, Rossini P M. TMS and TMS-EEG techniques in the study of the excitability, connectivity, and plasticity of the human motor cortex. Rev Neurosci, 2013, 24(4): 431-442.
49. Lou A R, Madsen K H, Paulson O B, et al. Monocular visual deprivation suppresses excitability in adult human visual cortex. Cereb Cortex, 2011, 21(12): 2876-2882.
50. Tuna A R, Pinto N, Brardo F M, et al. Transcranial magnetic stimulation in adults with amblyopia. J Neuroophthalmol, 2020, 40(2): 185-192.
51. Donkor R, Silva A E, Teske C, et al. Repetitive visual cortex transcranial random noise stimulation in adults with amblyopia. Sci Rep, 2021, 11(1): 3029.
52. Erkelens I M, Bobier W R, Macmillan A C, et al. A differential role for the posterior cerebellum in the adaptive control of convergence eye movements. Brain Stimul, 2020, 13(1): 215-228.
53. Colnaghi S, Colagiorgio P, Ramat S, et al. After effects of cerebellar continuous theta burst stimulation on reflexive saccades and smooth pursuit in humans. Cerebellum, 2017, 16(4): 764-771.

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