Presbyopia / SPO - 3.2.5.4. Neuroadaptation and multifocal lenses

Presbyopia / SPO

3.2.5.4. Neuroadaptation and multifocal lenses

Andreia M Rosa 1,2, Mariana Oliveira 2, Amélia Martins 2, José Costa 1,2, Miguel Castelo-Branco 3,4 e Joaquim Murta 1,2

1. Faculdade de Medicina da Universidade de Coimbra, Portugal

2. iCBR - Instituto de Investigação Clínica e Biomédica de Coimbra, Portugal

3. CIBIT - Coimbra Institute for Biomedical Imaging and Translational Research, Portugal

4. BIN - Brain Imaging Network of Portugal, Aveiro, Portugal

DYSPHOTOPIC SYMPTOMS AND NEUROPLASTICITY

Multifocal intraocular lenses reduce the need for near, far and intermediate distance glasses and are increasingly used1. However, some patients are dissatisfied with the surgical outcome, although they may have excellent visual acuity. This has been described as the “20/20 unhappy patient”2.

The main causes of dissatisfaction after multifocal lens implantation are symptoms collectively referred to as dysphotopsies2-5. Positive dysphotopsies (glare or glow, halos and starburst risks) are more frequent, while negative dysphotopsies (shadows, penumbra) are more rare3,5-7. These symptoms reflect aspects of visual function that go beyond the amount of vision, expressed by visual acuity, and reflect the most encompassing notion of visual quality. There is no effective treatment for this type of complaint, which leads to lens explantation in 4-12% of cases internationally3,5,8. According to a report on complications of foldable intraocular lenses, the American Society of Cataract and Refractive Surgery and the European Society of Cataract Surgeons and Refractive Surgery, the most frequent cause for explant or subsequent intervention after placement of multifocal lenses was the presence of glare and optic aberrations (68%)9. In fact, these complications have remained an obstacle to the greater use of intraocular multifocal lenses8,10.

Dysphotopsies are not clearly associated with objective optical parameters4. There are no significant differences in terms of light scattering, high order aberrations, pupillary diameter and uncorrected visual acuity between patients with and without dysphotopic symptoms, which shows that optical parameters per se do not explain the differences found in patients' symptoms2,8. This lack of association suggests the involvement of other mechanisms underlying visual complaints, possibly at the neuronal level. Even after excluding other causes of decreased visual quality, such as dry eye, posterior capsule opacification and retinal disease, there is no correlation between glare symptoms and optical quality parameters4,5.

As the difficulties experienced by patients tend to improve over time, it is thought that the brain adapts to new images, a phenomenon known as neuroadaptation3,11-16. One way of expressing this concept is given by two patients with identical visual results in terms of objective function, but with very different perceptions of their quality of vision. In fact, personal vision is determined by the way the brain processes data from the retina, since vision involves a perceptual construct and not just the analysis of an optically perfect image17.

The complexity associated with adapting each individual to their visual input has already been demonstrated for other diseases of the anterior segment of the eye18. For example, using adaptive optics to achieve the same level of image quality in patients with keratoconus and in a control group, the visual performance of the keratoconus group is lower than in the control group, especially in the subgroup with more high-order aberrations18. This data is especially relevant for patients with keratoconus, a disease that affects the cornea of young adults, thus excluding amblyopia as a cause for the absence of visual acuity improvement. The lack of improvement is attributed to neural factors, i.e. neuronal insensitivity due to prolonged visual experience with poor quality retinal imaging18. In fact, visual performance is influenced by retinal and neuronal factors, in addition to optical aberrations19. Neural adaptation to blurring influences visual performance deeply, even in normal eyes20. Blurring caused by high-order aberrations themselves is preferable rather than a version in which rotation of these aberrations has been induced, indicating that the neuronal visual system is adapted to the optical properties of the eye21.

Neuroplasticity thus refers to the brain's ability to reorganize its structure and/or functional connections and local organization in response to the modification of information from the surrounding environment22. Behavioral manifestations of visual plasticity include perceptual learning and adaptation, under the top-down control of attention1,23-25. Perceptual learning is a process in which the practice of a challenging task leads to significant and persistent improvements in visual performance23-25. The term visual adaptation designates both changes in neuronal processing, due to brief and repeated exposures, and due to the persistence of the long-term stimulus24,25. In the latter case, the effect is permanent, and long-term structural plasticity is induced. Both short-term and long-term adaptations may be due to the presence of the eye's optic defocus25,26. In addition, adaptation tends to mask the loss of sensitivity that occurs with disease or aging, which implies that the adaptation process remains largely functional in the elderly visual system. In this way, adaptation may be an important way to reconcile vision with optical quality of the eye throughout life26-28. It is then natural, to study the phenomena of adaptation and plasticity, in patients with multifocal intraocular lenses.

FUNCTIONAL MAGNETIC RESONANCE AS AN INNOVATIVE WAY TO EVALUATE NEUROADAPTATION TO MULTIFOCAL LENSES

Principle of functional magnetic resonance imaging

Functional magnetic resonance imaging (FMRI) studies are based on the blood oxygenation level dependent (BOLD) contrast that results from neuronal activity. When neurons become active, the vascular system provides more oxygenated hemoglobin than necessary through compensatory increase in blood flow29. This leads to a decrease in the deoxygenated hemoglobin/oxygenated hemoglobin ratio. Due to the different magnetic properties of these two forms of hemoglobin, the decrease in this relationship leads to an increase in magnetic resonance imaging T2 signal images30. Thus, the BOLD signal obtained from FMRI is totally noninvasive29,31. When a stimulus is visible, it causes an increase in the BOLD signal at the level of the visual cortex, which is proportional to the stimulus contrast32.

FMRI has been used to demonstrate the presence of neuroplasticity in other ocular diseases, such as pigmentary retinopathy, macular degeneration and amblyopia22,33-35. In this way, FMRI was used to study the neuroadaptation in patients with multifocal lenses at 2 time points: early postoperative (3 weeks) and late (6 months).

To evaluate the neuroadaptation, two parameters of FMRI were selected: activation of the visual cortex and activation of the attention-effort network, in addition to clinical ophthalmologic parameters. The FMRI task involved performing retinotopy for visual cortex mapping and a functional task. The functional task consisted of a sinusoidal pattern projected on a monitor in the resonator to measure the corresponding BOLD signal. In half of the presentations there was a frame of LED lights around the sinusoidal pattern, in order to induce slight glare (disability glare).

The contrast of the sinusoidal pattern was threshold and quasi-threshold for each patient, which implied their evaluation in the psychophysical laboratory before being applied in the resonance, in both visits. However, at the second visit, the values obtained in the first visit were applied in order to find out if the same level of contrast had become more visible due to neuroadaptation. The evaluation of the impact of light on contrast sensitivity was selected because the ability to discriminate an object against a similar background is a fundamental part of visual quality and may be altered in patients with multifocal lenses. Contrast threshold values were selected to be able to discern improvements over time (since high contrasts are always clearly visible) and to simulate everyday situations, such as night driving, in which visual tasks involve very low contrasts36.

Patients were also evaluated from an ophthalmological point of view, including visual acuity for far, near and intermediate distances, with and without correction, mono and binocular, reading speed, topography, aberrometry and a visual quality questionnaire with images. The implanted multifocal lenses were AcrySof ReSTOR SN6AD1 IOL, an apodised hybrid lens that combines refractive and diffractive regions with a +3.00 D addition. It was selected because it is one of the most used lenses and thus provides a practical clinical perspective. To control aspects related to memorization or other, we also studied a healthy control group, matched for age and gender, with no ophthalmologic surgical history.

NEUROADAPTATION IN THE PRESENCE OF SHINE

Light sources have a greater impact on recently operated patients (3 weeks) than in a control group37. Light decreases the BOLD signal of the primary visual cortex obtained when patients try to detect low contrast visual stimuli, which means that, comparatively, patients are more affected by the presence of light around the visual target, which makes the stimulus difficult to discern and leads to a relatively low value of the maximum and medium BOLD signal (area under the curve).

However, at the 6th month, contrast sensitivity increases, especially when evaluated under the light source, and the BOLD signal also increases (Figure 1).

Figure 1. Average curves of hemodynamic functional response estimated for stimuli with threshold contrast (in the presence of light source) in the early (3 weeks, left) and late (6 months, right) postoperative period. The BOLD signal (beta values) is displayed as a function of time, each volume corresponding to 2 seconds. After the onset of the stimulus, the BOLD signal reaches a maximum value, due to the compensatory increase of the oxygenated hemoglobin (β max). It then reduces to the minimum value before returning to the baseline. Light decreases the BOLD signal obtained for the low contrast stimulus in the early postoperative period, but not at the second visit (p> 0.05 for all periods, Wilcoxon's test).

Thus, at the 6th month visit the light source no longer significantly reduces the primary visual cortex signal when patients see a low-contrast stimulus, which means that patients improved their ability to detect this type of stimulus. Consequently, this is an objective measurement of the improvement of disability glare, at the cortical level.

NEUROADAPTATION BY ACTIVATION OF EFFORT AND ATTENTION BRAIN ZONES

A fascinating question, regarding the symptoms reported by the patients, refers to the possibility of observing, in an objective and cortical way, the difficulty that the patients report when performing a certain task. To answer this question, a difficult stimulus (low contrast, with light around) and an easy stimulus were presented, both for patients with multifocal lenses and for the control group.

At the first visit (early postoperative) patients had significant activation of the neural network associated with attention (frontal, frontal-mid, parietal-frontal and post-central gyrus) when they observed the difficult stimulus, while the control group presented only a relative deactivation at occipital level, probably related to the lower level of visibility of the stimulus with less contrast, but without the effort presented by patients. However, during the second visit, there was less recruitment of areas of effort and attention (Figure 2).

Figure 1. Whole-brain analysis at the first visit (image above) showed that patients activated the parietal lobe (1), the medial frontal gyrus (2), and the cingulate (3) when they were asked to detect a difficult stimulus (threshold contrast under light) versus an easy stimulus (with 2.5 x more contrast). At the second visit, however, there is only a relative recruitment of the medial frontal gyrus (5).

On the other hand, even on the first visit, patients with more complaints (higher scores in the visual quality questionnaire) also had higher recruitment of the neural network of attention, cingulate cortex and caudate.

These cortical areas are dedicated to cognitive learning and control, task planning and resolution, and thus suggest the beginning of the neuroadaptation process^38-41.

When comparing the activation of stress zones between the subgroup of patients who had the most symptoms versus the one who had the least symptoms at 6 months, it was found that there were no significant differences, as opposed to the initial results (Figure 3).

Figure 3. Patients who were most disturbed by dysphotopic symptoms at the first visit were compared with those who felt less discomfort when both were asked to detect a low-contrast stimulus under light source. The group with higher quotation in the questionnaire (more discomfort) showed greater activity in several regions of the frontal lobe and parietal, as well as activations of cingulate and caudate gyri in the first visit, but not 6 months later (p (FDR) <0.05).

This evolution suggests that patients with more symptoms at the initial visit required greater activation of the attention network, which facilitated perceptual learning through the interaction of areas associated with attention and visual cortical regions, leading to normalization at the second visit³⁹.

In fact, other studies have already shown an increase in the BOLD signal in the visual cortex associated with the development of ease/experience in the performance of visual tasks, and a corresponding reduction in the level of effort required³⁸.

READING SPEED

Reading speed is one of the most important aspects of the quality of vision, since in modern societies reading is an essential faculty in everyday life^42,43. Therefore, it is also important to evaluate the improvement of this ability in patients undergoing ophthalmologic surgery, such as after cataract surgery and implantation of multifocal intraocular lenses. It is interesting to know the acuity of reading and its speed.

For this purpose, the aforementioned group of patients with multifocal lenses was evaluated using the Portuguese version of the Radner test, the Radner-Coimbra test⁴⁴. These reading tables are based on the concept of phrases-optotypes, that is, phrases highly similar in terms of number and position of words, structure, syllables, characters and average reading difficulty. Thus, the differences found between visits are actually due to the improvement or worsening of the clinical situation, not due to the randomness of the sentence or sentences that the patient read at each visit^44,45.

Patients with multifocal lenses showed improvement over the postoperative follow-up in terms of reading acuity, reading speed and maximal reading score, with stability in the control group⁴⁶.

QUESTIONNAIRE SCORE

The subjective visual quality was evaluated as reported by the patients, through the Quality of Vision questionnaire (QoV). This questionnaire is second-generation, which means that its results, after Rasch's analysis, can be used in statistical tests, since it does not assume that the space between categories of answers is equidistant and that all questions have the same value¹⁷.

The QoV evaluates 10 symptoms (brightness, halos, starry scratches, blur, defocus, distortion, double or multiple images, fluctuations, difficulties in focusing and depth perception) with images to elucidate each term. Each symptom has 3 associated questions about the frequency, severity, and discomfort caused by the respective symptom.

There was an improvement in the score of the questionnaires at the second visit (6^th month) in the group of patients, while the control group did not present significant differences.

FUNCTIONAL PLASTICITY AND LEARNING AFTER CATARACT SURGERY

In this study we sought to replicate everyday conditions that cause difficulties for patients with multifocal lenses, such as visual tasks under artificial and low light. Evaluating the detection of contrast under light source was thus a way of reproducing the circumstances of daily living inside the MRI apparatus. It was assumed that the translation of the neuroadaptation would be maximized by exposure to a source of brightness, which was confirmed by the results.

It was verified that there was initially activation of attention, effort and learning zones (effort pattern), but with normalization at the 6^th month. The results obtained are consistent with previous studies that demonstrated that the cortical regions associated with the effort network are less activated after learning a visual task and that the decrease in cortical activation is highly correlated with the magnitude of the capacity to correctly perform this task³⁹. Although there was no learning training in the study by the authors, as the visual task was only repeated at the 6^th postoperative month, it can be considered that vision in daily life after cataract surgery is a form of natural learning.

Patients are exposed to sources of brightness and to low contrast stimuli daily, and repeated exposure to a visual stimulus results in a better perception of this stimulus, that is, perceptual learning³⁹. With practice, they attune themselves to the relevant characteristics and are able to extract them from the environment with greater selectivity and fluency⁴⁷. Reducing the activation of attention-related areas during learning represents a lower need for attention as the task becomes easier due to improved procedural efficiency^38,39.

Cingulate gyrus plays an important role in attention, goal behavior and error monitoring, which explains its activation at the first visit, in the first stages of adaptation, but not at the second visit, when the performance of the visual task changed to be made more easily⁴⁰. The same line of reasoning applies to the absence of caudate activations during the second visit, since this region is involved in the planning and execution of strategies to achieve complex/difficult goals⁴¹.

As the improvements in terms of vision, symptoms, contrast detection and reading speed could be attributed to a favorable evolution of the optical properties, aberrometry was performed by ray tracing in both visits. Ray-traced aberrometers use thin, separate beams in concentric rings that are projected sequentially into the eye⁴⁸. This method avoids confusion in the evaluation of eyes with many aberrations or with multifocal lenses, since the evaluation is made point by point, avoiding the overlap that would occur in other aberrometers, due to the presence of the Fresnel rings in multifocal lenses⁴⁹. It is important to control the optical properties to ensure that the observed improvements are due to better cortical processing and not due to improved optical properties such as high order aberrations, modular transfer function (MTF), or the Strehl ratio. In both the patient and control groups there were no significant changes in the optical parameters, which reinforces the notion that the best results presented by the patients at the second visit are not due to the optical properties of the eye.

Thus, this study demonstrates, for the first time, the association between subjective difficulties reported by patients and the results of FMRI, regardless of optical properties and psychophysical performance. It provides objective data that neuroadaptation to multifocal lenses occurs through a process of recruiting visual areas of attention and learning in the initial postoperative period. A form of long-term adaptation/functional plasticity – probably perceptual learning – leads to the regularization of cortical activity towards a non-effort neuronal pattern. These modifications represent an improvement in neuronal efficiency, so that fewer brain regions are recruited to perform a given task, similarly to what has already been reported in terms of gaining expertise in tasks involving computer games⁵⁰.

The immediate clinical application of these results is based on patient reassurance. There is in fact a process of neuroadaptation, with recruitment of zones of effort and learning, with regularization in the first months towards a pattern of non-effort. Patients with more dysphotopic symptoms have no worse optical properties and resolve most of the symptoms within the first 6 months. In addition, patients should not avoid demanding visual tasks. Although these activities may lead to greater activation of zones of effort and attention initially, it has been shown that this activation is reduced over time and is accompanied by improvement in visual, psychophysical and reading performance. In fact, the recruitment of the attention network facilitates perceptual learning through the interaction between the attention areas and the visual cortical regions³⁹. Perceptual training by performing demanding visual tasks can help patients with more symptoms select relevant information, ignore irrelevant stimuli such as halos, and improve the detection of low contrasts under light.

In this way, understanding the relationship between optical properties and symptoms may still lead to a more effective treatment of dysphotopsies. Anxiety, for example, has a negative impact on perceptual learning⁵¹. Performance decreases when resources (such as spatial attention, executive functions) are consumed by anxiety^51,52. Anxiety has a negative impact on verbal and spatial processes and there is a correlation between it and performance failure⁵¹. In this way, it is necessary to manage the anxiety provoked by the presence of dysphotopic symptoms in the early postoperative period.

Although a group of patients with multifocal lenses have been studied, dysphotopsies also occur in patients with monofocal lenses. It will also be relevant to study the neuroadaptation to different lens designs, since some models may induce less dysphotopsies and allow a more physiological adaptation. It is further clear from the information now obtained that analysis of functional connectivity between visual and attention-related areas will be especially important in patients in whom neuroadaptation has not been well and effectively established. Specifically, cortico-striatal connections contribute to the interpretation of ambiguous visual scenes, such as halos, glares, and star streaks⁵³. It could thus be possible to identify preoperative markers associated with positive adaptation to multifocal lenses or other refractive procedures, establishing bridges between functional magnetic resonance imaging and psychophysical testing.

CONCLUSION

Neuroadaptation, in the context of cataract surgery and multifocal lenses, occurs early through the recruitment of attention, learning, and effort zones, becomes established over months, an leads to improved performance in terms of visual acuity, contrast sensitivity and speed of reading, with improvement of subjective complaints not dependent on the optical properties studied.

REFERENCES

1. Martins Rosa A, Silva MF, Ferreira S, Murta J, Castelo-Branco

M. Plasticity in the human visual cortex: an ophthalmology-based perspective. BioMed Res Int 2013; 2013: 568354.

2. Kinard K, Jarstad A, Olson RJ. Correlation of visual quality with satisfaction and function in a normal cohort of pseudophakic patients. J Cataract Refract Surg 2013; 39(4): 590-7.

3. de Vries NE, Webers CA, Touwslager WR, Bauer NJ, de Brabander J, Berendschot TT, Nuijts. Dissatisfaction after implantation of multifocal intraocular lenses. J Cataract Refract Surg 2011; 37(5): 859-65.

4. Wilkins MR, Allan BD, Rubin GS, Findl O, Hollick EJ, Bunce C, Xing W, Moorfields IOL Study Group. Randomized trial of multifocal intraocular lenses versus monovision after bilateral cataract surgery. Ophthalmology 2013; 120(12): 2449-55.

5. Woodward MA, Randleman JB, Stulting RD. Dissatisfaction after multifocal intraocular lens implantation. J Cataract Refract Surg 2009; 35(6): 992-7.

6. Welch NR, Gregori N, Zabriskie N, Olson RJ. Satisfaction and dysphotopsia in the pseudophakic patient. Can J Ophthalmol 2010; 45(2): 140-3.

7. Holladay JT, Zhao H, Reisin CR. Negative dysphotopsia: the enigmatic penumbra. J Cataract Refract Surg 2012; 38(7): 1251-65.

8. Calladine D, Evans JR, Shah S, Leyland M. Multifocal versus monofocal intraocular lenses after cataract extraction. Cochrane Database Syst Rev 2012; (9): CD003169.

9. Mamalis N. Complications of foldable intraocular lenses requiring explantation or secondary intervention--2001 survey update. J Cataract Refract Surg 2002; 28(12): 2193-201.

10. Dolders MG, Nijkamp MD, Nuijts RM, van den Borne B, Hendrikse F, Ament A, Groot W. Cost effectiveness of foldable multifocal intraocular lenses compared to foldable monofocal intraocular lenses for cataract surgery. Br J Ophthalmol 2004; 88(9): 1163-8.

11. Braga-Mele R, Chang D, Dewey S, Foster G, Henderson BA, Hill W, Hoffman R, Little B, Mamalis N, Oetting T, Serafano D, Talley- Rostov A , Vasavada A, Yoo S, ASCRS Cataract Clinical Committee. Multifocal intraocular lenses: relative indications and contraindications for implantation. J Cataract Refract Surg 2014; 40(2): 313-22.

12. Fernandez-Buenaga R, Alio JL, Munoz-Negrete FJ, Barraquer Compte RI, Alio-Del Barrio JL. Causes of IOL explantation in Spain. Eur J Ophthalmol 2012; 22(5): 762-8.

13. Palomino Bautista C, Carmona Gonzalez D, Castillo Gomez A, Bescos JA. Evolution of visual performance in 250 eyes implanted with the Tecnis ZM900 multifocal IOL. Eur J Ophthalmol 2009; 19(5): 762-8.

14. Pepin SM. Neuroadaptation of presbyopia-correcting intraocular lenses. Curr Opin Ophthalmol 2008; 19(1): 10-2.

15. Shimizu K, Ito M. Dissatisfaction after bilateral multifocal intraocular lens implantation: an electrophysiology study. J Refract Surg 2011; 27(4): 309-12.

16. Rabsilber TM, Rudalevicius P, Jasinskas V, Holzer MP, Auffart GU. Influence of +3.00 D and +4.00 D near addition on functional outcomes of a refractive multifocal intraocular lens model. J Cataract Refract Surg 2013; 39(3): 350-7.

17. McAlinden C, Pesudovs K, Moore JE. The development of an instrument to measure quality of vision: the Quality of Vision (QoV) questionnaire. Invest Ophthalmol Vis Sci 2010; 51(11): 5537-45.

18. Sabesan R, Yoon G. Visual performance after correcting higher order aberrations in keratoconic eyes. J Vis 2009; 9(5): 6 1-10.

19. Campbell FW, Green DG. Optical and retinal factors affecting visual resolution. J Physiol 1965; 181(3): 576-93.

20. Webster MA, Georgeson MA, Webster SM. Neural adjustments to image blur. Nat Neurosci 2002; 5(9): 839-40.

21. Artal P, Chen L, Fernandez EJ, Singer B, Manzanera S, Williams DR. Neural compensation for the eye’s optical aberrations. J Visi 2004; 4(4): 281-7.

22. Nelson CA. Neural plasticity and human development: the role of early experience in sculpting memory systems. Develop Sci 2000; 3(2): 115-36.

23. Karmarkar UR, Dan Y. Experience-dependent plasticity in adult visual cortex. Neuron 2006; 52(4): 577-85.

24. Thompson P, Burr D. Visual after effects. Curr Biol. 2009; 19(1): R11- 4.

25. Yehezkel O, Sagi D, Sterkin A, Belkin M, Polat U. Learning to adapt: Dynamics of readaptation to geometrical distortions. Vision Res 2010; 50(16): 1550-8.

26. Webster MA. Adaptation and visual coding. J Vis 2011; 11(5).

27. Werner A, Bayer A, Schwarz G, Zrenner E, Paulus W. Effects of ageing on postreceptoral short-wavelength gain control: transient tritanopia increases with age. Vision Res 2010; 50(17): 1641-8.

28. Rivest J, Kim JS, Intriligator J, Sharpe JA. Effect of aging on visual shape distortion. Gerontology 2004; 50(3): 142-51.

29. Huettel SA, Song AW, McCarthy G. Functional Magnetic Resonance Imaging: Sinauer Associates, Incorporated; 2009.

30. Pauling L, Coryell CD. The Magnetic Properties and Structure of Hemoglobin, Oxyhemoglobin and Carbonmonoxyhemoglobin. Proc Natl Sci USA 1936; 22(4): 210-6.

31. Miki A, Haselgrove JC, Liu GT. Functional magnetic resonance imaging and its clinical utility in patients with visual disturbances. Surv Ophthalmol 2002; 47(6): 562-79.

32. Goodyear BG, Nicolle DA, Humphrey GK, Menon RS. BOLD fMRI response of early visual areas to perceived contrast in human amblyopia. J Neurophysiol 2000; 84(4): 1907-13.

33. Kalia A, Lesmes LA, Dorr M, Gandhi T, Chatterjee G, Ganesh S, Bex PJ, Sinha P. Development of pattern vision following early and extended blindness. Proc Natl Sci USA 2014; 111(5): 2035-9.

34. Sabel BA, Gudlin J. Vision restoration training for glaucoma: a randomized clinical trial. JAMA Ophthalmol 2014; 132(4): 381-9.

35. Baker CI, Peli E, Knouf N, Kanwisher NG. Reorganization of visual processing in macular degeneration. J Neurosci 2005; 25(3): 614-8.

36. Montes-Mico R, Alio JL. Distance and near contrast sensitivity function after multifocal intraocular lens implantation. J Cataract Refract Surg 2003; 29(4): 703-11.

37. Rosa AM, Miranda AC, Patricio M, McAlinden C, Silva FL, Murta JN, Castelo-Branco M. Functional Magnetic Resonance Imaging to Assess the Neurobehavioral Impact of Dysphotopsia with Multifocal Intraocular Lenses. Ophthalmology 2017; 124(9): 1280-9.

38. Lewis CM, Baldassarre A, Committeri G, Romani GL, Corbetta M. Learning sculpts the spontaneous activity of the resting human brain. Proc Natl Acad Sci USA 2009; 106(41): 17558-63.

39. Mukai I, Kim D, Fukunaga M, Japee S, Marrett S, Ungerleider LG. Activations in visual and attention-related areas predict and correlate with the degree of perceptual learning. J Neurosci 2007; 27(42): 11401-11.

40. Choi MH, Kim HS, Yoon HJ, Lee JC, Baek JH, Choi JS, Tack GR, Min BC, Lim DW, Chung SC. Increase in brain activation due to sub-tasks during driving: fMRI study using new MR-compatible driving simulator. J Physiol Anthropol 2017; 36(1): 11.

41. Grahn JA, Parkinson JA, Owen AM. The cognitive functions of the caudate nucleus. Prog Neurobiol 2008; 86(3): 141-55.

42. Elliott DB, Hurst MA, Weatherill J. Comparing clinical tests of visual function in cataract with the patient’s perceived visual disability. Eye (Lond) 1990; 4 (Pt 5): 712-7.

43. Alio JL, Radner W, Plaza-Puche AB, Ortiz D, Neipp MC, Quiles MJ, Rodríguez-Marín J. Design of short Spanish sentences for measuring reading performance: Radner-Vissum test. J Cataract Refract Surg 2008; 34(4): 638-42.

44. Rosa AM, Farinha CL, Radner W, Diendorfer G, Loureiro MF, Murta JN. Development of the Portuguese version of a standardized reading test: the Radner-Coimbra Charts. Arq Bras Oftalmol 2016; 79(4): 238-42.

45. Radner W, Obermayer W, Richter-Mueksch S, Willinger U, Velikay- Parel M, Eisenwort B. The validity and reliability of short German sentences for measuring reading speed. Graefes Arch Clin Exp Ophthalmol 2002; 240(6): 461-7.

46. Rosa AM, Miranda ÂC, Patrício MM, McAlinden C, Silva FL, Castelo-Branco M, Murta JN. Functional magnetic resonance imaging to assess neuroadaptation to multifocal intraocular lenses. J Cataract Refract Surg 2017; 43(10): 1287-96.

47. Kellman PJ, Garrigan P. Perceptual learning and human expertise. Phys Life Rev 2009; 6(2): 53-84.

48. Molebny VV, Panagopoulou SI, Molebny SV, Wakil YS, Pallikaris IG. Principles of ray tracing aberrometry. J Refract Surg 2000; 16(5): S572-5.

49. Jun I, Choi YJ, Kim EK, Seo KY, Kim TI. Internal spherical aberration by ray tracing-type aberrometry in multifocal pseudophakic eyes. Eye (Lond) 2012; 26(9): 1243-8.

50. Sigman M, Pan H, Yang Y, Stern E, Silbersweig D, Gilbert CD. Top- down reorganization of activity in the visual pathway after learning a shape identification task. Neuron 2005; 46(5): 823-35.

51. Vytal KE, Cornwell BR, Letkiewicz AM, Arkin NE, Grillon C. The complex interaction between anxiety and cognition: insight from spatial and verbal working memory. Front Human Neurosci 2013; 7: 93.

52. Shackman AJ, Maxwell JS, McMenamin BW, Greischar LL, Davidson RJ. Stress potentiates early and attenuates late stages of visualprocessing. J Neuroci 2011; 31(3): 1156-61.

53. Lopez-Paniagua D, Seger CA. Interactions within and between corticostriatal loops during component processes of category learning. J Cogn Neuroci 2011; 23(10): 3068-83.

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