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A New Counter-Intuitive Therapy for Adult Amblyopia

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A New Counter-Intuitive Therapy for Adult Amblyopia bioRxiv preprint doi: https://doi.org/10.1101/360420; this version posted July 2, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 A new counter-intuitive therapy for adult amblyopia 2 3 Lunghi Claudia, PhD 1,2, Sframeli Angela Tindara MD3, Lepri Antonio MD3, Lepri Martina MS3, Lisi 4 Domenico MS3, Sale Alessandro PhD4*+, Morrone Maria Concetta PhD1,5+ 5 6 Affiliations: 1Department of Translational Research on New Technologies in Medicine and 7 Surgery, University of Pisa, Italy; 2Laboratoire des systèmes perceptifs, Département d’études 8 cognitives, École normale supérieure, PSL University, CNRS, 75005 Paris, France; 3Ophthalmology 9 Unit, Deptartment of Surgical, Medical, Molecular and Critical Area Pathology, University of Pisa, 10 Italy; 4Neuroscience Institute, National Research Council (CNR), Pisa, Italy; 5IRCCS Stella Maris, 11 Calambrone, Pisa, Italy. 12 +Co-senior authors 13 14 *Corresponding Author: 15 Alessandro Sale 16 Neuroscience Institute, National Research Council (CNR), Via Moruzzi 1, 56124, Pisa, Italy; 17 Email: [email protected] 18 19 Manuscript information 20 # Characters: title = 51, running head = 33. 21 # Words: abstract = 156, introduction = 457, discussion = 705, body = 3247 22 # Figures: 5 23 # Color Figures: 0 24 1 bioRxiv preprint doi: https://doi.org/10.1101/360420; this version posted July 2, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 25 Abstract 26 Visual cortex plasticity is high during a critical period of early postnatal development, but 27 rapidly diminishes with the transition to adulthood. Accordingly, visual disorders such as 28 amblyopia (lazy eye), can be treated early in life by long-term occlusion of the non-amblyopic eye, 29 but may become irreversible in adults, because of the decline in brain plasticity. Here we show 30 that a novel counter-intuitive approach can promote the recovery of visual function in adult 31 amblyopic patients: short-term occlusion of the amblyopic (not the fellow) eye, combined with 32 physical exercise (cycling). After six brief (2h) training sessions, visual acuity improved in all ten 33 patients (0.15±0.02 LogMar), and six of them also recovered stereopsis. The improvement was 34 preserved for up to one year after training. A control experiment revealed that physical activity 35 was crucial for the recovery of visual acuity and stereopsis. Thus, we propose a non-invasive 36 therapeutic strategy for adult human amblyopia based an inverse-occlusion and physical exercise 37 procedure. 38 39 2 bioRxiv preprint doi: https://doi.org/10.1101/360420; this version posted July 2, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 40 Introduction 41 Amblyopia is a neurodevelopmental disorder of vision1,2 with a prevalence ranging from 1 42 to 5% depending on the population tested3. The most frequent causes of amblyopia are 43 strabismus, anisometropia and deprivation (for example due to cataracts) early in life1,2, within the 44 so-called critical period, defined as the temporal window during development where the plastic 45 potential of the visual cortex is maximal4,5. If the retinal image is degraded during development, 46 the visual cortex disregards the eye providing degraded input and responds primarily to the eye 47 providing the better signal. Amblyopia can be ameliorated in young children by the long-term 48 occlusion of the better (non-amblyopic) eye3. However, in humans, treatment after the closure of 49 the critical period dramatically decreases therapy efficacy requiring extensive occlusion of the 50 non-amblyopic eye to produce only a modest improve of visual acuity (234 hours of occlusion per 51 0.1 LogMar acuity improvement6). New therapeutic strategies recently proposed for adult 52 amblyopia involve either very prolonged visual training7–12, or invasive manipulations13,14, 53 rendering them almost ineffective for clinical purposes. 54 Recently, new hope has emerged from evidence that the early visual cortex retains some 55 degree of plasticity in adult humans15–23. Many studies have demonstrated a plastic response to 56 visual deprivation: a few hours15,16 or a few days17,18 of binocular deprivation modulate excitability 57 of the primary visual cortex. But also monocular occlusion of one eye for a few hours paradoxically 58 boosts the deprived eye signal, shifting ocular dominance in favor of the deprived eye19–22. This 59 counter-intuitive effect of monocular deprivation reflects a compensatory reaction of the visual 60 cortex to deprivation aimed at maintaining the average cortical activity constant, indicating that 61 some form of homeostatic plasticity24 is also present in adult humans. Importantly, this plasticity 62 is mediated by a decrease of GABA concentration in the primary visual cortex25 and is enhanced by 63 physical exercise26. 3 bioRxiv preprint doi: https://doi.org/10.1101/360420; this version posted July 2, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 64 The modulatory effect of physical activity on visual plasticity is corroborated by several 65 recent studies on animal models27–30: in adult rats and mice physical activity boosts visual cortical 66 plasticity by modulating the levels of GABAergic inhibition27–29 via a specific somatosensory- visual 67 circuitry27–30. Interestingly, visual cortical GABAergic interneurons are implicated in the 68 mechanisms controlling the onset and offset of the visual critical period in these animal models31. 69 While physical exercise appears as a potentially suitable and non-invasive therapeutic 70 strategy for adult amblyopia, no attempts have been made, to date, to investigate its effects on 71 amblyopic human subjects. Focusing on adult anisometropic patients, we performed a 72 counterintuitive experiment which combined short-term deprivation of the amblyopic eye with 73 physical exercise. We found that after six short training sessions (2h each), visual acuity and 74 stereopsis improved in adult patients, and that the improvement persisted for up to one year after 75 the end of the treatment. 76 77 78 79 Methods 80 Subjects 81 Adult anisometropic patients were enrolled for the study after an ophthalmic screening 82 examination in which detailed ocular and systemic anamnesis has been investigated (see 83 Procedures section). Patients with a history of chronic ocular diseases other than amblyopia have 84 been excluded from the study as long as patients presenting any chronic systemic disease. 85 Similarly, patients with neurological or psychiatric disorder or under medication of any sort were 86 excluded. 4 bioRxiv preprint doi: https://doi.org/10.1101/360420; this version posted July 2, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 87 Out of 40 patients screened, 10 met the inclusion criteria and were enrolled for the study 88 (four males, mean age 33±1.5, Clinical data reported in Table 1). 89 90 Ethical Statement 91 Experimental procedures are in line with the declaration of Helsinki and were approved by 92 the regional ethics committee [Comitato Etico Pediatrico Regionale—Azienda Ospedaliero- 93 Universitaria Meyer—Firenze (FI)], under the protocol “Plasticità del sistema visivo” (3/2011). 94 95 Apparatus and Stimuli 96 Binocular Rivalry 97 The experiment took place in a dark and quiet room. Visual stimuli were generated by the 98 ViSaGe stimulus generator (CRS, Cambridge Research Systems), housed in a PC (Dell) controlled by 99 Matlab programs. Visual stimuli were two Gaussian-vignetted sinusoidal gratings (Gabor Patches), 100 oriented either 45° clockwise or counterclockwise (size: 2σ = 2°, spatial frequency: 2 cpd), 101 presented on a uniform background (luminance: 37.4 cd/m2, C.I.E: 0.442 0.537) in central vision 102 with a central black fixation point and a common squared frame to facilitate dichoptic fusion. 103 Visual stimuli were displayed on a 20-inch Clinton Monoray (Richardson Electronics Ltd., LaFox, IL) 104 monochrome monitor, driven at a resolution of 1024x600 pixels, with a refresh rate of 120 Hz. 105 Observers viewed the display at a distance of 57 cm through CRS Ferro-Magnetic shutter goggles 106 that occluded alternately one of the two eyes each frame. Responses were recorded through the 107 computer keyboard. 108 Procedures 109 Screening Examination 5 bioRxiv preprint doi: https://doi.org/10.1101/360420; this version posted July 2, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.
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