A total of 10 unilateral AMD patients between 62.8 and 76.7 years old (mean age: 71.1 ± 4.6 years) and 10 bilateral AMD patients between 57.1 and 78.5 years old (mean age: 70.8 ± 6.1 years) participated in the study. We also tested 10 age-matched healthy controls (mean age: 69.8 ± 6.3 years). All participants were recruited from the Department of Ophthalmology, Hôtel-Dieu Hospital in Paris and from the Centre Ophtalmologique du Val-d'Oise (France). Their participation was voluntary.

All participants had to fulfill criteria: ametropia inferior to five dioptries (spherical equivalent), no ocular surgery background, no retina laser treatment, no other ophthalmology pathologies, no diabetes, no known cognitive loss, no known vestibular abnormality, and no known orthopedic surgeries and abnormalities.

The investigation adhered to the principles of the Declaration of Helsinki and was approved by our Institutional Human Experimentation Committee (Comité de Protection des Personnes CPP, Ile de France V). Written informed consent was obtained from each participant after an explanation of the experimental procedure.

All AMD subjects underwent ophthalmologic and orthoptic examination to evaluate their visual function. Clinical data of each AMD patients are shown in Tables 1, 2. Clinical data of healthy elderly subjects are shown in Table 3.

Visual acuity was measured separately for each eye at far distance (5 m) with the Monoyer chart. Next we have translated to ETDRS with an adapted scale. Stereoscopic acuity was measured by TNO test (Test of Netherlands Organization for Applied Scientific Research; Walraven, 1975). Unilateral AMD patients have a corrected monocular visual acuity between 20/125 and 20/20, and bilateral AMD patients a corrected monocular acuity between 20/800 and 20/25. Only eight of the ten AMD participants have a stereoscopic acuity <480 s of arc. Visual functions are also evaluated for control subjects. They have a monocular corrected visual acuity of 20/20 and stereoscopic acuity for 120 s of arc.

Age-related macular degeneration severity scale of AREDS was used for each eye (AREDS, 2001). SD-OCT (Spectralis®, Heidelberg Engineering) for each eye allows identifying AMD level by locating geographic atrophies (deterioration of the photoreceptors) and choroidal neovascularization (growth of pathologic blood vessels from the choroid into the subretinal space).

Among participants, 60% of bilateral AMD and 80% of unilateral AMD are choroidal neovascularization. Other studies have reported that there is two AMD with choroidal neovascularization for one AMD with geographic atrophy (Chakravarthy et al., 2007).

The eye with the better corrected visual acuity is considered as the dominant eye.

A force platform (AFP40/16 Stabilotest, principle of strain gauge) consisting of two dynamometric clogs was used to measure and quantify postural stability (Standards by Association Française de Posturologie, produced by TechnoConcept®, Céreste, France; Figure 1). Foot position is standardized with footprints. This platform included a 16-bit analog-digital and acquisition frequency was 40 Hz. The excursion of center of pressure was measured during 25.6 s. Postural parameters were calculated following Gagey's standards (Gagey et al., 1993; Gagey and Weber, 1999).

In a dark room, participants stood on the platform and fixed a target (3 × 3 cm; identically for all subjects) in front of their eye level (150 cm). Four visual conditions were tested: binocular eye viewing (BEV), dominant eye viewing (DEV), non-dominant eye viewing (NDEV), and eyes closed (EC). We choose to test postural control separately for each eye in order to compare the impact of level of AMD on postural stability in order to develop training techniques for these subjects, even if these conditions are not physiological. Subjects were instructed to stay as still as possible with their arms along their body, to fix the target and stand quietly on the platform. Three randomized trials were performed for each visual condition successively. A short break was done between each condition. The total duration of the trial was 10 min.

To quantify the effect of AMD and visual conditions on postural control we analyzed the surface area (mm²), the length (mm), the mean speed (mm/s), and the anteroposterior (AP) and mediolateral (ML) displacements (mm) of the CoP that are the standard deviation of the displacement. Surface area is an effective measurement of CoP variability and corresponds to an ellipse with 90% of CoP (Chiari et al., 2002; Gagey and Weber, 2004; Vuillerme et al., 2008). Length is a path of CoP. Mean speed is an efficient indicator to quantity the neuro-muscular activity required to regulate postural control (Geurts et al., 1993).

Data were analyzed with ANOVA/MANOVA using the three groups of subjects (unilateral, bilateral AMD subjects, and control subjects) as inter- subject factor, and the four visual conditions (both eyes opens, dominant and non-dominant eye open, and both eyes closed) as within-subject factor.

In the case of significant effects post-hoc Bonferroni test was performed. The effect of a factor was considered as significant when the p-value was below 0.05.

In this study we found that AMD subjects had poor postural stability with respect to controls. This finding is in agreement with others studies (Elliott et al., 1995; Kotecha et al., 2013). Moreover, two postural parameters (surface area and AP displacement of CoP) were significantly different in bilateral AMD subjects compared with healthy elderly, and the AP displacement of CoP was significantly affected in unilateral AMD only.

Based on this finding we could assume that a postural evaluation, particularly of the surface area of the CoP, at the beginning of the AMD diagnosis may be predictive of future postural difficulties in these patients. An early postural rehabilitation care would prevent the risk of falling and in the future, studies leading with postural, and/or visual training will be necessary to improve the everyday life.

Postural balance changes throughout life. Qiu et al. (2012) studied the somatosensory system during aging and the impact of age on postural stability. Elderly patients (mean age: 72 years) have an augmentation of surface area and length of the CoP, and an augmentation of AP and ML sways, in comparison with young adults (mean age: 27 years). These authors suggested that mechanoreceptors sensibility decreases with aging as well as the capacity of treatment of sensorial information by the central nervous system. According to Faraldo-García et al. (2016), older subjects could have poor ability of adapt their body to disturbed sensory situations. Note that in younger subjects with loss of central vision (Stargardt disease) Agostini et al. (2016) found that compensatory strategies are used to control their postural stability. Such adaptive mechanisms are working well also in children with strabismus (see works of our groups, i.e., Lions et al., 2014; Bucci et al., 2016); we could make the hypothesis that in older subjects with AMD pathologies such compensations are not well developed, most likely because at this age plasticity occurs less frequently.

Our results proved that AP displacements of CoP was higher in AMD subjects than controls in closed eyes condition, most likely because AMD subjects have low mobility and degraded physical performance. Such hypothesis is confirmed by previous studies (Rovner et al., 2009; Chomistek et al., 2013; Loprinzi et al., 2015). These authors suggested that physical inactivity facilitated the progression of vision loss (Chomistek et al., 2013) and cognitive loss like depressive disorders (Rovner et al., 2009). Moreover, (Loprinzi et al., 2015) showed that AMD subjects, and more generally subjects with low visual acuity increased sedentary behavior, leading to increase of risk of developing metabolic, cardiovascular, and cerebrovascular diseases.

Few studies examined postural stability under monocular viewing. (Moraes et al., 2009), studied the impact of binocular vs. monocular viewing in controlling posture in quiet stance in young adults without visual abnormalities (mean age: 22.7 years). They suggested that binocular viewing allowed a greater postural control.

Note that even if our results failed to show any interaction effect between subjects and visual condition data on monocular viewing, they suggested that AMD subjects are more stable under dominant eye viewing than under both eyes viewing condition. Studies with more patients are needed to confirm this result. We made the hypothesis that monocular visual field of the dominant eye is less disturbed than binocular visual field in AMD subjects. The confirmation of this result would open perspectives of developing of training techniques without replacing the standard follow-up of the AMD subjects by clinical ophthalmological examination. In fact, in theory, neutralization process is expected to erase some of the scotoma (no view area) in the binocular visual field. But this process is difficult for elderly people due to the age-related decrease of brain plasticity.

The role of central vs. peripheral vision information in control balance was examined in several studies. Marigold and Patla (2007) examined the role of central or peripheral vision to avoid an obstacle. These authors reported that peripheral vision was sufficient for successful obstacle avoidance during locomotion. Moreover, more recently, Timmis et al. (2016) proved, in young adults, the impact of visual field loss (to 10° compared 20°) on risk of falls. They showed that only visual field loss to 20° increased risk of falls. We could hypothesis that the size of scotoma in AMD subjects may be predictive of postural instability. According to Berencsi et al. (2005), in young adults, central, and peripheral vision contributes to maintaining a stable standing posture. They suggested that peripheral vision control more the AP than ML displacements of CoP. Actually our result contrast this one, AP displacement of CoP is larger in AMD subjects with central field loss could be due to the different age of subjects tested in the two studies. Indeed, it is well-known that older subjects used more hip strategies to maintain postural control whereas young adults used ankle strategies (Daubney and Culham, 1999). Further studies comparing young and old subjects with poor vision are needed to explore postural strategies.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.