Visual Restoration after Cataract Surgery Promotes Functional and Structural Brain Recovery

Abstract

Background: Visual function and brain function decline concurrently with aging. Notably, cataract patients often present with accelerated age-related decreases in brain function, but the underlying mechanisms are still unclear. Optical structures of the anterior segment of the eyes, such as the lens and cornea, can be readily reconstructed to improve refraction and vision quality. However, the effects of visual restoration on human brain function and structure remain largely unexplored.

Methods: A prospective, controlled clinical trial was conducted. Twenty-six patients with bilateral age-related cataracts (ARCs) who underwent phacoemulsification and intraocular lens implantation and 26 healthy controls without ARC, matched for age, sex, and education, were recruited. Visual functions (including visual acuity, visual evoke potential, and contrast sensitivity), the Mini-Mental State Examination and functional magnetic resonance imaging (including the fractional amplitude of low-frequency fluctuations and grey matter volume variation) were assessed for all the participants and reexamined for ARC patients after cataract surgery. This trial was registered with ClinicalTrials.gov (NCT02644720).

Findings: Compared with the healthy controls, the ARC patients presented decreased brain functionality as well as structural alterations in visual and cognitive-related brain areas preoperatively. Three months postoperatively, significant functional improvements were observed in the visual and cognitive-related brain areas of the patients. Six months postoperatively, the patients' grey matter volumes in these areas were significantly increased. Notably, both the function and structure in the visual and cognitive-related brain areas of the patients improved significantly and became comparable to those of the healthy controls 6months postoperatively.

Interpretation: We demonstrated that ocular reconstruction can functionally and structurally reverse cataract-induced brain changes. The integrity of the eye is essential for maintaining the structure and function of the brain within and beyond the primary visual pathway.

Keywords: Age-related cataract; Brain plasticity; Vision restoration; Visual impairment.

Copyright © 2018 German Center for Neurodegenerative Diseases (DZNE). Published by Elsevier B.V. All rights reserved.

Figures

Fig. 1

Flowchart of recruitment and follow-up evaluations from 1 week after the second eye surgery. Notes: fMRI, functional magnetic resonance imaging; MMSE, Mini-Mental State Examination; UCDVA, uncorrected distance visual acuity; BCDVA, best-corrected distance visual acuity; CS, contrast sensitivity; SVs, straylight values; VEP, visual evoked potential; IOL, intraocular lens; SIOL, single-focus intraocular lens; MIOL, multifocal intraocular lens.

Fig. 2

Comparison of brain function and structure between the control and cataract groups before surgery. a, MMSE scores of the control and cataract groups were recorded (P < 0·001, independent sample t-test). b, Surface maps show the changes in the fALFF values between the controls and patients with cataract (at a whole-brain threshold of P < 0·05, AlphaSim corrected, voxels > 228, two-sample t-test). c, d, Slice overlays and plots represent the mean signal from the smoothed difference images for each cluster. Significant differences in signals between the control group and the cataract group are highlighted within the red circle. Blue and cyan reflect decreases in the superior parietal lobule, superior occipital lobule, and precuneus with peak voxels observed in the inferior parietal lobule. Red and yellow reflect increases in the brainstem, and t indicates the peak t-score value for the t-test. e, Surface maps show the changes in GM volume between the controls and the patients with cataract. f, Slice overlays and plots represent the mean signals from the smoothed difference images for each cluster. Significant differences in signals between the control group and the cataract group are highlighted within the red circle. Blue and cyan reflect decreases in the anterior cingulate gyrus, and t indicates the peak t-score value for the t-test. Notes: Dotted lines indicate the mean value; MMSE, Mini-Mental State Examination; fALFF, fractional amplitudes of low-frequency fluctuation; L, left; Inf, inferior; GM, grey matter; Ant. anterior.

Fig. 3

Comparison of brain function in cataract patients before and after surgery. Surface maps show the fALFF value changes between preoperative and postoperative time points (at a whole-brain threshold of P  228, repeated measures analysis of variance). Slice overlays and plots represent the mean signals from the smoothed difference images for each cluster. Significant differences in signals are highlighted in the red circles. Blue and cyan reflect decreases. Red and yellow reflect increases, and t indicates the peak t-score value for the t-test. a, No significant difference in fALFF signals was detected between the preoperative and 1 week postoperative time points. b, The fALFF values were significantly decreased in the brainstem and cerebellum at 3 months postoperatively. c, The fALFF values were significantly decreased in the brainstem but increased in the superior parietal lobule 6 months postoperatively. Notes: L, left; Sup., superior.

Fig. 4

Comparison of brain GM volume in cataract patients before and after surgery. Surface maps show the changes in GM volume between preoperative and postoperative time points (at a whole-brain threshold of P  200, repeated measures analysis of variance). Slice overlays and plots represent the mean signals from the smoothed difference images for each cluster. Significant differences in the signals are highlighted in the red circles. Blue and cyan reflect decreases. Red and yellow reflect increases, and t indicates the peak t-score value for the t-test. a, b, No significant difference in the GM volume signal was detected between the preoperative time point and the 1-week (a) or 3-month (b) postoperative time points. c, Compared with the preoperative values, the GM volumes observed at 6 months after surgery were significantly increased in the calcarine, fusiform, anterior/middle cingulate gyrus, inferior/middle frontal gyrus, inferior/medial orbitofrontal cortex, and precentral/postcentral gyrus. Notes: Mid, middle; Sup, superior; R, right; Frontal. Inf. Orb, inferior orbitofrontal cortex; Frontal. Med. Orb., medial orbitofrontal cortex.

Fig. 5

Improvements in brain structure and function in cataract patients after visual restoration. Six months after cataract surgery, the GM volumes of the following regions were increased to various extents: 1-fusiform (L) (BA20/36, t = 4·928), 2-frontal. Inf. Orb (R) (BA38/47, t = 6·433), 3-frontal. Inf. Orb (L) (BA47, t = 6·062), 4-frontal. Med. Orb (L) (BA10, t = 5·317), 5-anterior cingulate gyrus (R) (BA9/32, t = 6·395), 6-middle frontal gyrus (L) (BA6/8/9, t = 6·395), 7-middle frontal gyrus (R) (BA6/8/9, t = 5·393), 8-middle cingulate gyrus (R) (BA31, t = 5·020), 9-precentral gyrus (L) (BA6, t = 5·429), 10-precentral gyrus (R) (BA4, t = 4·960), 11-postcentral gyrus (L) (BA4, t = 4·600), 13-calcarine (R) (BA18/30, t = 5·055), 14-calcarine (L) (BA18/19/30, t = 5·052) and 15-superior temporal gyrus (L) (BA21/22, t = 6·159). The fALFF of the 12-superior parietal lobule (L) (BA17/19, t = 4·566) was increased after surgery, whereas the fALFF of the 16-brainstem (t = −3·923) was decreased. Notes: The sizes of the spots represent the degree of quantitative changes; GM, grey matter; fALFF, the fractional amplitude of low-frequency fluctuations; frontal. Inf. Orb, inferior orbitofrontal cortex; frontal. Med. Orb, medial orbitofrontal cortex; R, right; L, left.