Background
Amblyopia is characterized by reduced visual acuity [
1] associated with structural brain [
2,
3] and retinal [
4] changes that are usually not observed during the standard ophthalmological examination. It occurs due to asymmetric interocular suppression of visual inputs to the cortex, very often caused by the misalignment (strabismus) of the eyes [
5‐
7] and / or unequal and uncorrected refractive error (anisometropia) [
8], and stimulus deprivation due to an obstruction of visual pathway [
7,
9]. In amblyopic adult eyes, cosmetic results are believed to be the main benefit for patients with chronic strabismus undergoing surgical treatment. Nevertheless, several studies have proved that binocular summation can be modulated after the alignment of the eyes [
10,
11] and elimination of diplopia and/or a compensatory head posture [
12‐
14]. However, the surgical alignment of the strabismic eyes in adult with amblyopia is usually not followed by visual acuity improvements. Moreover, it has been associated with risk of squint relapse [
15].
Fixation stability is often affected in amblyopic patients [
16]. It has been recently reported that visual acuity improvements are accompanied by changes in fixation stability after amblyopic treatment [
17]. Therefore, fixational eye movements may be considered in amblyopic treatment. Microperimetry, or fundus-controlled visual field examination, is a relatively new method to measure monocular macular light sensitivity while recording eye movements to monitor visual fixation (for review see Rohrschneider et al., 2008) [
18]. In addition, the continuous recording of eye movements during the examination enables the establishment of the preferred retinal locus (PRLs), which is the preferential location on which the tested eye fixates a central target. This approach allows recording and quantifying fixation stability [
19].
The biofeedback fixation training (BFT), integrated in some microperimetric systems, allows selecting one retinal location to be stimulated for either providing a more stable fixation or to change PRL retinal location [
20,
21]. It has been earlier reported [
22,
23] and increasingly emphasized [
24‐
27] that BFT improves fixation stability in patients with low vision. The conditions causing low vision due to retinal alterations in macular diseases may stimulate the replacement of the fixation area to a less affected surrounding area (eccentric viewing). In contrast, amblyopic patients with strabismus may display eccentric fixation, in which the visual center (functional fovea) is shifted to a non-foveal area due to suppressive mechanisms during the critical period of development [
28]. It was long demonstrated that visual fixation can be improved with auditory feedback in amblyopia [
29]. More recently, functional gain was demonstrated in children and adults undergoing visual training using pattern stimulation associated with auditory feedback [
30,
31].
We hypothesize that BFT providing a better control of microsaccades could improve fixation stability in amblyopic adult eyes after surgical alignment of the strabismus. The purpose of the present study was to investigate the effects of surgical treatment and BFT on fixation stability.
Discussion
The results of our present study show that: i) fixation stability is impaired in strabismic amblyopic adult eyes and ii) biofeedback fixation training (BFT) after alignment of the strabismus may improve fixation stability. Normal vision and appropriate binocular function depend upon the integrity of the eye’s movements to efficiently guide both eyes so that visual target is brought and maintained at the fixational (foveal) area (for review see Collewijn & Kowler, 2008) [
37]. Accordingly, disturbed fixational eye movements may affect the quality of vision in subjects with strabismus and/or amblyopia [
16,
38‐
42].
Fixational eye movements are characterized by slow oscillations of the eyes controlled by subcortical and cortical areas of the brain (for review see Kowler, 2011) [
43]. The proper oculomotor control of the eyes ensures that the visual target is centrally placed on the fovea which is responsible for the best visual acuity that can be achieved by the visual system [
44]. The present data emphasized [
16,
38,
45,
46] that fixation in healthy eyes is quite stable while it is altered in patients with strabismus.
In subjects with normal vision, steady fixation allows keeping the visual target on the correct retinal position in both eyes so that visual attention is maintained until the object of interest can be detected or discriminated [
47]. In contrast, unstable fixational eye movements continuously move the visual target out from the fixational locus, disturbing the attentional dedication to the visual target [
39]. Here we show that fixation can be modulated in adult strabismic patients. We hypothesize that a more stable fixation could perhaps modulate monocular visual acuity and binocular vision in amblyopic eyes. Future investigations may address this question.
Amblyopia caused by strabismus, associated or not to anisometropia, may show eccentric and unstable fixation due to more severe extraocular motor alterations [
40]. Previous reports taken together with the present data allow speculating that efforts to improve visual acuity of strabismic adult eyes with amblyopia should consider improving fixation stability in addition to stimulating visual perception of the amblyopic eye.
Although surgical correction of eye’s position in infants may successfully result in normal visual development during the critical period, reestablishment of fixation stability is not always achieved [
16,
48]. In non-human adult primates, only a temporary improvement of fixation stability is observed after surgical treatment of strabismus [
49]. Strabismus surgery delivered to the adult amblyopic eye is usually indicated as cosmetic correction, since visual perception and binocular vision are not expected to be changed after the surgical alignment. Functional improvements associated with surgical alignment of strabismus in adults are not clearly established. Some authors found that strabismus surgery significantly improves the self-reported quality of life due to a positive effect in visual performance [
50,
51]. Pineles et al. found that binocular summation is improved after strabismus surgery [
11]. However other authors showed that binocular function are not significantly modulated by the surgical alignment of the eyes when the critical period of development is over [
52].
We hypothesize that improvements in fixation stability after correction of the eye position and BFT, may stimulate visual mechanisms responsible for the spatial vision in amblyopic eyes, increasing the possibility of visual acuity improvement. Among several types of behavioural rehabilitation for amblyopia [
53‐
55], improvement of visual function provided by a short-term biofeedback training delivered to anisometropic amblyopic eyes of teenagers has been reported [
30]. Here we reported that strabismic amblyopic eyes may benefit from BFT after surgical alignment of strabismus. Further studies with a large population may investigate the relations between clinical parameters, such as binocular balance [
56], and visual improvements provided by BFT. In addition, to establish the proper criteria for selecting those patients who would more likely benefit from BFT for enhancing visual performance in amblyopic eyes.
Limitations of our study are the small sample size of participants. Further investigation with a larger population is necessary to confirm the present results. Moreover, although our results showed that surgical correction alone was not capable to improve fixation stability, a case-control study, in which some subjects are not enrolled in the training program and some subjects performing sham training after the surgical correction, would allow us to evaluate if the fixational improvements demonstrated here would be expected after surgical correction of strabismus or if they are related to the microperimetric biofeedback fixation training. Finally, we spculate that a more stable fixation of an amblyopic eye would help maintaining the primary position of the eye which could, in turn, reduce the possibility of strabismus relapse after the surgical correction.
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