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Neuroscience Bulletin
Published in: Neuroscience Bulletin 7/2023

Open Access 01-07-2023 | Strabismus | Original Article

Cortical Deficits are Correlated with Impaired Stereopsis in Patients with Strabismus

Authors: Sida Xi, Yulian Zhou, Jing Yao, Xinpei Ye, Peng Zhang, Wen Wen, Chen Zhao

Published in: Neuroscience Bulletin | Issue 7/2023

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Abstract

In this study, we explored the neural mechanism underlying impaired stereopsis and possible functional plasticity after strabismus surgery. We enrolled 18 stereo-deficient patients with intermittent exotropia before and after surgery, along with 18 healthy controls. Functional magnetic resonance imaging data were collected when participants viewed three-dimensional stimuli. Compared with controls, preoperative patients showed hypoactivation in higher-level dorsal (visual and parietal) areas and ventral visual areas. Pre- and postoperative activation did not significantly differ in patients overall; patients with improved stereopsis showed stronger postoperative activation than preoperative activation in the right V3A and left intraparietal sulcus. Worse stereopsis and fusional control were correlated with preoperative hypoactivation, suggesting that cortical deficits along the two streams might reflect impaired stereopsis in intermittent exotropia. The correlation between improved stereopsis and activation in the right V3A after surgery indicates that functional plasticity may underlie the improvement of stereopsis. Thus, additional postoperative strategies are needed to promote functional plasticity and enhance the recovery of stereopsis.
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Literature
1.
Candy TR, Cormack LK. Recent understanding of binocular vision in the natural environment with clinical implications. Prog Retin Eye Res 2022, 88: 101014.PubMedCrossRef
2.
Welchman AE, Deubelius A, Conrad V, Bülthoff HH, Kourtzi Z. 3D shape perception from combined depth cues in human visual cortex. Nat Neurosci 2005, 8: 820–827.PubMedCrossRef
3.
4.
Ohzawa I, DeAngelis GC, Freeman RD. Stereoscopic depth discrimination in the visual cortex: Neurons ideally suited as disparity detectors. Science 1990, 249: 1037–1041.PubMedCrossRef
5.
Watanabe M, Tanaka H, Uka T, Fujita I. Disparity-selective neurons in area V4 of macaque monkeys. J Neurophysiol 2002, 87: 1960–1973.PubMedCrossRef
6.
Parker AJ. Binocular depth perception and the cerebral cortex. Nat Rev Neurosci 2007, 8: 379–391.PubMedCrossRef
7.
Alizadeh AM, Van Dromme I, Verhoef BE, Janssen P. Caudal Intraparietal Sulcus and three-dimensional vision: A combined functional magnetic resonance imaging and single-cell study. NeuroImage 2018, 166: 46–59.PubMedCrossRef
8.
9.
Preston TJ, Li S, Kourtzi Z, Welchman AE. Multivoxel pattern selectivity for perceptually relevant binocular disparities in the human brain. J Neurosci 2008, 28: 11315–11327.PubMedPubMedCentralCrossRef
10.
11.
12.
Wu Q, Guo W, Hu H, Li R, Zhu H, Chen XX. Altered spontaneous brain activity in patients with comitant exotropia before and after surgery: A resting-state fMRI study. Exp Eye Res 2022, 222: 109161.PubMedCrossRef
13.
Yan X, Wang Y, Xu L, Liu Y, Song S, Ding K, et al. Altered functional connectivity of the primary visual cortex in adult comitant strabismus: A resting-state functional MRI study. Curr Eye Res 2019, 44: 316–323.PubMedCrossRef
14.
Jin H, Chen RB, Zhong YL, Lai PH, Huang X. Effect of impaired stereoscopic vision on large-scale resting-state functional network connectivity in comitant exotropia patients. Front Neurosci 2022, 16: 833937.PubMedPubMedCentralCrossRef
15.
Liang M, Xie B, Yang H, Yin X, Wang H, Yu L, et al. Altered interhemispheric functional connectivity in patients with anisometropic and strabismic amblyopia: A resting-state fMRI study. Neuroradiology 2017, 59: 517–524.PubMedCrossRef
16.
Chen F, Hu Z, Liu H, Zhen F, Liu C, Li Q. Altered homotopic connectivity in the cerebellum predicts stereopsis dysfunction in patients with comitant exotropia. Front Hum Neurosci 2022, 16: 917769.PubMedPubMedCentralCrossRef
17.
Xi S, Yao J, Zhang S, Liu R, Wu L, Ye X, et al. Disrupted neural signals in patients with concomitant exotropia. Ophthalmic Physiol Opt 2020, 40: 650–659.PubMedCrossRef
18.
Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT, Van Essen DC, et al. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007, 447: 83–86.PubMedCrossRef
19.
Nasr S, Kennedy B, Nabasaliza A, Bex P, Hunter DG, Tootell RBH. Revealing differential mechanisms of absolute vs. relative disparity encoding in human extrastriate visual cortex and impacts of amblyopia on them. J Vis 2021, 21: 1986.
20.
Nasr S, Kennedy B, Nabasaliza A, Bex P, Tootell RB, Hunter DG. Impact of amblyopia on the function of stereo- and motion-selective clusters in human extrastriate cortex. Investig Ophthalmol Vis Sci 2021, 62: 154.
21.
Liu Y, Liu C, Zhang W, Chen X, Zhao K. Model of a support vector machine to assess the functional cure for surgery of intermittent exotropia. Sci Rep 2019, 9: 8321.PubMedPubMedCentralCrossRef
22.
Adams WE, Leske DA, Hatt SR, Mohney BG, Birch EE, Weakley DR Jr, et al. Improvement in distance stereoacuity following surgery for intermittent exotropia. J Am Assoc Pediatr Ophthalmol Strabismus 2008, 12: 141–144.CrossRef
23.
Dickmann A, Aliberti S, Rebecchi MT, Aprile I, Salerni A, Petroni S, et al. Improved sensory status and quality-of-life measures in adult patients after strabismus surgery. J Am Assoc Pediatr Ophthalmol Strabismus 2013, 17: 25–28.CrossRef
24.
Ding J, Levi DM. Recovery of stereopsis through perceptual learning in human adults with abnormal binocular vision. Proc Natl Acad Sci U S A 2011, 108: E733–E741.PubMedPubMedCentralCrossRef
25.
Wang Y, Wang X, Shi H, Xia L, Dong J, Nguchu BA, et al. Microstructural properties of major white matter tracts in constant exotropia before and after strabismus surgery. Br J Ophthalmol 2022, 106: 870–877.PubMedCrossRef
26.
Buck D, Clarke MP, Haggerty H, Hrisos S, Powell C, Sloper J, et al. Grading the severity of intermittent distance exotropia: The revised Newcastle Control Score. Br J Ophthalmol 2008, 92: 577.PubMedCrossRef
27.
Webber AL, Wood JM, Thompson B, Birch EE. From suppression to stereoacuity: A composite binocular function score for clinical research. Ophthalmic Physiol Opt 2019, 39: 53–62.PubMedPubMedCentralCrossRef
28.
29.
Hess RF, Mansouri B, Thompson B, Gheorghiu E. Latent stereopsis for motion in depth in strabismic amblyopia. Invest Ophthalmol Vis Sci 2009, 50: 5006–5016.PubMedCrossRef
30.
Li X, Zhu Q, Janssens T, Arsenault JT, Vanduffel W. In vivo identification of thick, thin, and pale stripes of macaque area V2 using submillimeter resolution (f)MRI at 3 T. Cereb Cortex 2019, 29: 544–560.PubMedCrossRef
31.
Greve DN, Fischl B. Accurate and robust brain image alignment using boundary-based registration. NeuroImage 2009, 48: 63–72.PubMedCrossRef
32.
33.
Greve DN, Fischl B. False positive rates in surface-based anatomical analysis. Neuroimage 2018, 171: 6–14.PubMedCrossRef
34.
Eklund A, Nichols TE, Knutsson H. Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci U S A 2016, 113: 7900–7905.PubMedPubMedCentralCrossRef
35.
Wang L, Mruczek REB, Arcaro MJ, Kastner S. Probabilistic maps of visual topography in human cortex. Cereb Cortex 2015, 25: 3911–3931.PubMedCrossRef
36.
Georgieva SS, Todd JT, Peeters R, Orban GA. The extraction of 3D shape from texture and shading in the human brain. Cereb Cortex 2008, 18: 2416–2438.PubMedPubMedCentralCrossRef
37.
38.
Hubel DH, Wiesel TN, Yeagle EM, Lafer-Sousa R, Conway BR. Binocular stereoscopy in visual areas V-2, V-3, and V-3A of the macaque monkey. Cereb Cortex 2015, 25: 959–971.PubMedCrossRef
39.
Tsao DY, Vanduffel W, Sasaki Y, Fize D, Knutsen TA, Mandeville JB, et al. Stereopsis activates V3A and caudal intraparietal areas in macaques and humans. Neuron 2003, 39: 555–568.PubMedCrossRef
40.
Ng AKT, Jia K, Goncalves NR, Zamboni E, Kemper VG, Goebel R, et al. Ultra-high-field neuroimaging reveals fine-scale processing for 3D perception. J Neurosci 2021, 41: 8362–8374.PubMedPubMedCentralCrossRef
41.
Hou C, Tyson TL, Uner IJ, Nicholas SC, Verghese P. Excitatory contribution to binocular interactions in human visual cortex is reduced in strabismic amblyopia. J Neurosci 2021, 41: 8632–8643.PubMedPubMedCentralCrossRef
42.
Durand JB, Peeters R, Norman JF, Todd JT, Orban GA. Parietal regions processing visual 3D shape extracted from disparity. Neuroimage 2009, 46: 1114–1126.PubMedCrossRef
43.
44.
45.
Yin X, Chen L, Ma M, Zhang H, Gao M, Wu X, et al. Altered brain structure and spontaneous functional activity in children with concomitant strabismus. Front Hum Neurosci 2021, 15: 777762.PubMedPubMedCentralCrossRef
46.
Wang H, Crewther SG, Liang M, Laycock R, Yu T, Alexander B, et al. 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 2017, 11: 195.PubMedPubMedCentralCrossRef
47.
Grant S, Suttle C, Melmoth DR, Conway ML, Sloper JJ. Age- and stereovision-dependent eye-hand coordination deficits in children with amblyopia and abnormal binocularity. Invest Ophthalmol Vis Sci 2014, 55: 5687–5701.PubMedPubMedCentralCrossRef
48.
Yang X, Zhang J, Lang L, Gong Q, Liu L. Assessment of cortical dysfunction in infantile esotropia using fMRI. Eur J Ophthalmol 2014, 24: 409–416.PubMedCrossRef
49.
Li Q, Bai J, Zhang J, Gong Q, Liu L. Assessment of cortical dysfunction in patients with intermittent exotropia: An fMRI study. PLoS One 2016, 11: e0160806.PubMedPubMedCentralCrossRef
50.
Upadhyaya S, Meng H, Das VE. Electrical stimulation of superior colliculus affects strabismus angle in monkey models for strabismus. J Neurophysiol 2017, 117: 1281–1292.PubMedCrossRef
51.
Linton P. Stereopsis in the absence of binocular disparity. In: The Perception and Cognition of Visual Space. 1st ed. Cham: Springer International Publishing, 2017: 73–116.
52.
53.
Fawcett SL, Wang YZ, Birch EE. The critical period for susceptibility of human stereopsis. Invest Ophthalmol Vis Sci 2005, 46: 521–525.PubMedCrossRef
54.
Decramer T, Premereur E, Uytterhoeven M, van Paesschen W, van Loon J, Janssen P, et al. Single-cell selectivity and functional architecture of human lateral occipital complex. PLoS Biol 2019, 17: e3000280.PubMedPubMedCentralCrossRef
55.
Chandrasekaran C, Canon V, Dahmen JC, Kourtzi Z, Welchman AE. Neural correlates of disparity-defined shape discrimination in the human brain. J Neurophysiol 2007, 97: 1553–1565.PubMedCrossRef
56.
Kourtzi Z, Kanwisher N. Representation of perceived object shape by the human lateral occipital complex. Science 2001, 293: 1506–1509.PubMedCrossRef
57.
Carpenter RHS. Supplementary eye field: Keeping an eye on eye movement. Curr Biol 2004, 14: R416–R418.PubMedCrossRef
58.
Martinez-Trujillo JC, Medendorp WP, Wang H, Crawford JD. Frames of reference for eye-head gaze commands in primate supplementary eye fields. Neuron 2004, 44: 1057–1066.PubMedCrossRef
59.
Schall JD. Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys. J Neurophysiol 1991, 66: 530–558.PubMedCrossRef
60.
Missal M, Heinen SJ. Facilitation of smooth pursuit initiation by electrical stimulation in the supplementary eye fields. J Neurophysiol 2001, 86: 2413–2425.PubMedCrossRef
61.
Stuphorn V, Taylor TL, Schall JD. Performance monitoring by the supplementary eye field. Nature 2000, 408: 857–860.PubMedCrossRef
62.
Mushiake H, Fujii N, Tanji J. Visually guided saccade versus eye-hand reach: Contrasting neuronal activity in the cortical supplementary and frontal eye fields. J Neurophysiol 1996, 75: 2187–2191.PubMedCrossRef
63.
Chan ST, Tang KW, Lam KC, Chan LK, Mendola JD, Kwong KK. Neuroanatomy of adult strabismus: A voxel-based morphometric analysis of magnetic resonance structural scans. Neuroimage 2004, 22: 986–994.PubMedCrossRef
64.
Maneschg OA, Barboni MTS, Nagy ZZ, Németh J. Fixation stability after surgical treatment of strabismus and biofeedback fixation training in amblyopic eyes. BMC Ophthalmol 2021, 21: 264.PubMedPubMedCentralCrossRef
65.
Qiu H, Li XY, Li HY, Wang XL, Zhang JS. Binocular vision training after intermittent exotropia surgery. Int J Ophthalmol 2010, 10: 1522–1523.
66.
Yang X, Fan Y, Chu H, Yan L, Wiederhold BK, Wiederhold M, et al. Preliminary study of short-term visual perceptual training based on virtual reality and augmented reality in postoperative strabismic patients. Cyberpsychol Behav Soc Netw 2022, 25: 465–470.PubMedCrossRef
67.
68.
Backus BT, Fleet DJ, Parker AJ, Heeger DJ. Human cortical activity correlates with stereoscopic depth perception. J Neurophysiol 2001, 86: 2054–2068.PubMedCrossRef
69.
Goncalves NR, Ban H, Sanchez-Panchuelo RM, Francis ST, Schluppeck D, Welchman AE. 7 tesla fMRI reveals systematic functional organization for binocular disparity in dorsal visual cortex. J Neurosci 2015, 35: 3056–3072.PubMedPubMedCentralCrossRef
70.
Chen N, Chen Z, Fang F. Functional specialization in human dorsal pathway for stereoscopic depth processing. Exp Brain Res 2020, 238: 2581–2588.PubMedCrossRef
Metadata
Title
Cortical Deficits are Correlated with Impaired Stereopsis in Patients with Strabismus
Authors
Sida Xi
Yulian Zhou
Jing Yao
Xinpei Ye
Peng Zhang
Wen Wen
Chen Zhao
Publication date
01-07-2023
Publisher
Springer Nature Singapore
Published in
Neuroscience Bulletin / Issue 7/2023
Print ISSN: 1673-7067
Electronic ISSN: 1995-8218
DOI
https://doi.org/10.1007/s12264-022-00987-7

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