Binocular summation of visual acuity and contrast sensitivity in children with intermittent exotropia

Intermittent exotropia (IXT) is a common type of strabismus in children, which manifests the different degrees of binocular vision function loss at distance and at near [1]. Some patients gradually lost binocular vision and developed constant exotropia. Examinations such as worth-4 dot (W-4-D) test, striated glass test, and stereopsis tests at distance and near are commonly applied to evaluate the changes in binocular vision, but these examinations cannot fully reflect the changes of visual function in the actual daily environment. Binocular summation (BiS) refers to the superiority of binocular over monocular viewing on visual tasks, such as visual acuity (VA) and contrast sensitivity (CS), which involves the interaction in layer VI of the visual cortex and is easily presented at the low contrast [2]. The threshold of monocular contrast sensitivity (MCS) at low contrast is 1.5 times that of binocular contrast sensitivity (BCS) in healthy individuals [3]. BiS can be influnced by multiple factors such as age, interocular difference of visual acuity, and eye position [4‐8]. Successful strabismus surgery can improve BiS in strabismus patients [9], which might be related to eye position control and stereopsis [10‐13]. BCS in strabismus patients was significantly lower than monocular contrast sensitivity, especially at 6 cpd spatial frequency, which was not correlated with the degree of strabismus, gender, age, refraction error, stereopsis, and duration of IXT [14]. The BiS phenomenon and relevant mechanisms in IXT patients are still undetermined. The correlationship between BiS of VA and BiS of CS is not well probed. This study sought to characterize the changes in BiS for spatial resolution and contrast sensitivity in IXT patients before and after surgery and to identify the relationship between the two phenomena and corresponding influencing factors in IXT children.

Strabismus affects binocular vision as well as perception, fusion, and stereopsis. People perceive objects in daily life using both eyes, and the BiS value of a healthy individual is close to 1.4 [15]. The decline in vision-specific quality of life is associated with decreased vision under low-contrast conditions [16, 17]. Binocular neurons were reduced in patients with strabismus, and the magnitude of the BiS was decreased and close to the VA of better eye in the presence of a large interocular VA difference [3]. A prior study demonstrated that patients with strabismus had a reduction in BiS at 2.5% contrast and 1.25% contrast or even binocular inhibition, indicating a more serious impact of strabismus on binocular vision than previously recognized [18]. Decreased CS in IXT patients may be related to poor control and stereopsis [11, 12], and may also be independent of angle of deviation, gender, age, stereoscopic acuity and duration of IXT [14]. And the significant reduction in BiS at low contrast was regarded to correlate with the poor control of IXT patients, rather than near and distant stereopsis [19].

Our previous study suggested that BVA at low contrast was significantly improved after strabismus surgery and the number of IXT patients with the BiS was increased and that of binocular inhibition was decreased, which was related to obtaining postoperative central fusion and better recovery of distance stereopsis in some extent [9]. The present study revealed successfully corrected eye position and improved postoperative high- and low-contrast BiS in IXT patients, particularly at 2.5% contrast. However, BiS and BVA values exhibited no linear correlation with fusion and stereopsis. The higher values reported in this study than previous report, that might be related to the enrollment of only IXT patients and the age of the patients. Additionally, our study found that preoperative BVA at 2.5% contrast was better than the VA of the dominant eye, and preoperative BiS at 2.5% contrast was higher than that at 100%. The postoperative BiS at 2.5% contrast was significantly improved as compared to the preoperative BiS at 2.5% contrast and postoperative BiS at 100% contrast. We considered that the visual pathways for low contrast may be influenced comparatively later in IXT.

In the previous studies, the BSR was usually adopted as the evaluation parameter for the BiS phenomenon of CS, but the calculation methods were different such as BSR = BCV/MCV [8, 10, 20], or BSR = BCV² /(RCV² + LCV²) [12]. There also existed differences in evaluation methods such as sinusoidal grating [12, 20], Mars contrast sensitivity test [8, 10], etc. The animal experiments demonstrated that neurons in the lateral geniculate nucleus of strabismic amblyopia were only damaged at high spatial frequencies [21]. An existing study revealed that the BSR of IXT patients was significantly lower than that of the healthy controls at low spatial frequencies (1.5 c/d and 3 c/d), but no significant difference was noted at other spatial frequencies 6 c/d, 12 c/d, and 18 c/d [12]. CS was improved in bright conditions following surgical treatment of IXT patients while CS was decreased significantly in response to postoperative overcorrection [22]. CSF of amblyopia patients with fusion function was impaired at intermediate and high frequencies, presenting a higher proportion of BiS than strabismus patients without fusion function [8]. BSR of IXT patients was temporarily decreased 1 month postoperatively, which might be due to postoperative foreign body sensation, lacrimation, and conjunctival edema, and then it returned to the preoperative level 3 months after surgery [10].

In our series, the preoperative CS value in IXT children was decreased mainly at medium and high spatial frequencies (6c/d, 12c/d, 18c/d), which was similar to the finding reported in the investigation of strabismus amblyopia [23‐25]. Those values were restored to normal levels postoperatively but CS of nondominant eye was still lower than the mean CS of 10-year-old healthy children reported previously [26]. BSR at 3 c/d persisted binocular inhibition at the low frequency even after surgery. The most significant improvement was achieved postoperatively in the BSR and BCS at 6 c/d in IXT children. Larsson found that the VA value was correlated with CS at medium and high spatial frequencies (6 c/d, 12 c/d, and 18 c/d) rather than CS at 3 c/d in 217 healthy children [26], which is consistent with our findings. In addition, postoperative BCS in our study shared no correlation with stereopsis and fusion function, which was similar to Chung’s report [14].

Human visual system exists the multiple pathways, each of which is only related to its specific narrow-band spatial frequency and directionality [27]. Cells in area 17 in the visual cortex are inclined to respond to higher spatial frequencies, while those in area 18 are likely to respond to lower spatial frequencies [27]. Low spatial frequency involved the macrocellular pathway [12]. Multiple visual mechanisms might be implicated in the tests for threshold level and super-threshold level [20]. We suggest that the low-contrast BVA method was superior in presenting the binocular summation, and CS tests showed the different sensitivity to binocular summation across different spatial frequencies. Both supplemented the clinical assessment methods for binocular visual performance.

However, the study had certain limitations, such as a small sample size, short duration of follow-up, and absence of a control group. Additionally, as all patients gained peripheral fusion after surgery, and there was only one patient without central fusion, so we failed to statistically analyze the correlations of postoperative BiS and BSR with fusion function. Thus, a large sample scale and long-term follow-up are needed to further study in IXT children.

In conclusions, binocular VA and CS reflect the details of BiS at different visual pathways and different aspects, which are not related to stereopsis and fusion function and could not be substituted. Although BiS at 2.5% contrast is associated with BCS at 6/12 /18 c/d, they cannot replace each other. In the future, more attention should be paid to multi-dimensional binocular visual performance.