Age- and stereovision-dependent eye-hand coordination deficits in children with amblyopia and abnormal binocularity

Abstract

Purpose: To examine factors contributing to eye-hand coordination deficits in children with amblyopia and impaired stereovision.

Methods: Participants were 55 anisometropic or strabismic children aged 5.0 to 9.25 years with different degrees of amblyopia and abnormal binocularity, along with 28 age-matched visually-normal controls. Pilot data were obtained from four additional patients studied longitudinally at different treatment stages. Movements of the preferred hand were recorded using a 3D motion-capture system while subjects reached-to-precision grasp objects (two sizes, three locations) under binocular, dominant eye, and amblyopic/nonsighting eye conditions. Kinematic and "error" performance measures were quantified and compared by viewing condition and subject group using ANOVA, stepwise regression, and correlation analyses.

Results: Movements of the younger amblyopes (age 5-6 years; n = 30) were much slower, particularly in the final approach to the objects, and contained more spatial errors in reaching (∼×1.25-1.75) and grasping (∼×1.75-2.25) under all three views (P < 0.05) than their age-matched controls (n = 13). Amblyopia severity was the main contributor to their slower movements with absent stereovision a secondary factor and the unique determinant of their increased error-rates. Older amblyopes (age 7-9 years; n = 25) spent longer contacting the objects before lifting them (P = 0.015) compared with their matched controls (n = 15), with absence of stereovision still solely related to increases in reach and grasp errors, although these occurred less frequently than in younger patients. Pilot prospective data supported these findings by showing positive treatment-related associations between improved stereovision and reach-to-grasp performance.

Conclusions: Strategies that children with amblyopia and abnormal binocularity use for reach-to-precision grasping change with age, from emphasis on visual feedback during the "in-flight" approach at ages 5 to 6 years to more reliance on tactile/kinesthetic feedback from object contact at ages 7 to 9 years. However, recovery of binocularity confers increasing benefits for eye-hand coordination speed and accuracy with age, and is a better predictor of these fundamental performance measures than the degree of visual acuity loss.

Keywords: grasping; reaching; visuomotor control.

Copyright 2014 The Association for Research in Vision and Ophthalmology, Inc.

Figures

Figure 1

The experimental setup showing (top) the 3-wall mounted infrared motion capture cameras (Qualisys) triangulating the (bottom) black workspace table from above. On this, the start button is in the foreground, with the “large” object shown at a “near, midline” location; the “small” object at an “ipsi, far” location (for a right-handed subject); and the neutral object used only for practice at a “contra, far” location. The locations shown were used for children with arm lengths ≥35 cm; blue stickers indicate those used for subjects with shorter arms.

Figure 2

Average movement durations by age (A) 5 to 6 years, (B) 7 to 9 years, viewing condition and stereovision. Movement times increased successively between control, stereo+ and stereo nil subjects at ages 5 and 6 years, but were similar in the control and stereo+ participants at ages 7 to 9 years, including faster performance with binocular compared with monocular vision, whereas there were no differences across views in the older stereo nil subjects. Errors bars: SEMs.

Figure 3

Average total reach error-rates per trial by age (A) 5 to 6 years, (B) 7 to 9 years, viewing condition and stereovision. Stereo nil subjects made the most reaching errors at both ages with no differences across the three views, whereas performance was similar in the control and stereo+ participants, particularly at ages 7 to 9 years with fewest errors occurring in the binocular condition. Errors bars: SEMs.

Figure 4

Profiles of (A) a normal and (B) a corrected spatial reach path during binocular movements toward the same “near, midline” target (filled circle) in (A) a left-handed control subject aged 7.25 years and (B) a right-handed stereo nil patient aged 7.33 years. The origin (0) of both movements on the x-axis corresponds to the starting hand positions; solid traces show the reach paths collapsed into lateral and forward directions and terminating just short of the target (as they were recorded from the marker on the wrist). In (A) the movement of the left hand follows a typical, slightly curved trajectory in a leftward (x-axis, -ve) lateral direction, but in (B) the trajectory is not a rightward mirror-image. Instead, the patient initially moved slightly rightward (open arrow), but misdirected his reach toward the midline well short of the target's location, necessitating a subsequent trajectory correction (filled arrow)—defined as a spatial path error—in order to acquire it.

Figure 5

Average peak grip apertures produced by 5- to 6-year-old participants prior to grasping the (A) “small” and (B) “large” objects, by viewing condition and stereovision. Only the control subjects selectively opened their grip much wider when preparing to grasp the smaller object when using monocular vision, this being classically designed to increase the “safety margin” for error under conditions of perceptual uncertainty. Error bars: SEM.

Figure 6

Average total grasp error rates per trial by age (A) 5 to 6 years, (B) 7 to 9 years, viewing condition and stereovision. Grasp error rates increased successively between control, stereo+ and stereo nil subjects at ages 5 to 6 years, but were similar in the control and stereo+ participants at ages 7 to 9 years, including generally better performance with binocular compared with monocular vision, whereas there were no differences across views in the older stereo nil subjects. Errors bars: SEMs.

Figure 7

Recovery of stereovision and eye–hand coordination deficits in a child with anisometropic amblyopia (case A1). Patient data are median movement durations (12 trials per view) compared with 12 control subjects of equivalent ages (range, 7.0–8.75 years) over which the patient was tested between initial presentation (untreated) and the end of his spectacle adaptation (refracted) and occlusion therapy (occluded). For further patient details, see text. NonDom, the amblyopic eye in the patient; the nonsighting eye in the controls. Error bars are upper bound 95% confidence limits.

Figure 8

Persistent eye–hand coordination deficits with absent stereovision in a child with mixed (anisometropic and strabismic) amblyopia (case M1) at the end of her spectacle adaptation (refracted) and at follow-up, after occlusion therapy (occluded) compared with control subjects. Other conventions are as in Figure 7.