Amblyopia is a neurodevelopmental visual disorder arising from decorrelated binocular experience during the critical periods of development. The hallmark of amblyopia is reduced visual acuity and impairment in binocular vision. The consequences of amblyopia on various sensory and perceptual functions have been studied extensively over the past 50 years. Historically, relatively fewer studies examined the impact of amblyopia on visuomotor behaviours; however, research in this area has flourished over the past 10 years. Therefore, the aim of this review paper is to provide a comprehensive review of current knowledge about the effects of amblyopia on eye movements, upper limb reaching and grasping movements, as well as balance and gait. Accumulating evidence indicates that amblyopia is associated with considerable deficits in visuomotor behaviour during amblyopic eye viewing, as well as adaptations in behaviour during binocular and fellow eye viewing in adults and children. Importantly, due to amblyopia heterogeneity, visuomotor development in children and motor skill performance in adults may be significantly influenced by the etiology and clinical features, such as visual acuity and stereoacuity. Studies with larger cohorts of children and adults are needed to disentangle the unique contribution of these clinical characteristics to the development and performance of visuomotor behaviours.
Amblyopia is a common neurodevelopmental disorder clinically defined as reduced visual acuity that cannot be immediately corrected using optical refraction [
The widespread effects of amblyopia on perceptual and sensorimotor functions are not surprising given that vision provides a key sensory input necessary for the optimal development of neural circuits and behavioural functions [
Visual perceptual changes in amblyopia have been studied extensively (for recent reviews, see [
The only way to interact with our environment is through action: making eye movements while reading or looking for relevant objects, performing goal-directed reaching and grasping movements with our hands, or navigating to a target destination while avoiding obstacles. The intricate link between vision and movement was first revealed by Held and Hein [
Reaching and grasping is a complex behaviour, which requires spatial and temporal coordination among multiple sensory and motor systems. For example, following the decision to drink a cup of coffee, the action sequence requires coordinated movements of the eyes to fixate the cup, and then the arm to reach and grasp the cup without knocking it over or spilling its contents. This seemingly simple action requires extensive processing of the visual input along the dorsal cortical stream where neurons are preferentially activated by binocular inputs [
As discussed above, vision thus provides important sensory input for optimal performance of goal-directed behaviours. When visual feedback is restricted or eliminated, movements become slower, less accurate, and more variable. For example, visuomotor performance is significantly diminished when adults with normal vision are forced to perform a task under monocular compared to binocular viewing [
Population studies in children estimate the prevalence of amblyopia to be between 1.3% and 3.6% [
Periods of attempted fixation consist of fixational eye movements that include (
The effects of amblyopia on fixational eye movements have been studied for over 40 years, and several abnormalities have been documented in both adults and children with different amblyopia etiologies. The early studies included relatively small sample sizes, and they quantified fixation instability by reporting the frequency and amplitude of microsaccades, as well as amplitude and rate of ocular drift [
Advancements in eye-tracking technology have led to larger studies in children and adults, providing insight into the association between fixation instability and visual acuity deficits. Recent studies quantified fixation instability using a variable called bivariate contour ellipse area (BCEA), which provides a measure of dispersion of the eyes during a fixation interval. Therefore, BCEA is a global measure of fixation instability influenced by the presence of microsaccades and ocular drift, so a larger BCEA could be due to an increased drift or more frequent and/or larger microsaccades. Results from two recent studies with adults are in agreement with the earlier reports. First, Gonzalez et al. [
Several recent studies examined fixation instability in children with amblyopia. Subramanian et al. [
Two additional studies provide further insight into the contribution of microsaccades and drift to fixation instability in the pediatric population. First, Shi et al. [
The increased drift variance in both eyes of children with amblyopia might have implications for binocular oculomotor control, which was investigated by Kelly et al. [
To summarize, amblyopic eye fixation instability has been found in adults and children. Notably, most studies found no significant difference in BCEA between the control eyes and patients viewing with the fellow eye [
Fixation instability has been associated with poorer visual acuity [
Voluntary saccades are quick, conjugate eye movements performed to explore the environment in a task-dependent manner [
The effects of amblyopia on saccadic eye movements were first characterized by Schor [
Building on these pioneering studies, research into saccadic eye movements has flourished over the past 10 years. Recent studies assessed larger cohorts of patients, and showed that clinical characteristics, such as amblyopia etiology, acuity, and stereoacuity have a significant influence on saccade latency and kinematics. The effects of etiology were clearly demonstrated in a large cohort (
A detailed regression analysis of patient characteristics, including acuity, stereoacuity, and ocular deviation, on saccade latency was performed in a cohort of 55 adults with various amblyopia etiology (22 anisometropic, 18 strabismic, and 15 mixed mechanism) [
It is important to mention that subtle, but significant saccade latency deficits may also be present when viewing binocularly or monocularly with the fellow eye. For example, binocular compared to monocular viewing is associated with superior performance on various perceptual and motor tasks in visually normal participants (i.e., binocular summation) [
It is well known that saccade latency is task dependent; for example, latency is shorter when the fixation target disappears 50-200 ms prior to the presentation of a peripheral target, which is referred to as the gap effect [
The accuracy and precision of saccade amplitude are important measures of performance; however, only one study to date assessed these outcomes in a cohort of 55 adults with amblyopia [
Reduced saccade precision and an increased number of secondary saccades could impact reading, which is an important daily activity that requires accurate and precise control of eye movements. Several studies that examined reading in amblyopia reported significantly lower reading speeds in children and adults, even during binocular viewing. For example, the reading speed of adults with strabismic amblyopia during binocular viewing was ~67% of that found in an education-matched control group [
In summary, accumulating evidence demonstrates a significant saccade-related deficit in the amblyopic eye, which is evident regardless of amblyopia etiology. The impairment manifests as a delay in movement initiation and reduced precision of target localization. Moreover, saccade deficits are associated with acuity loss, and may be greater in adults with strabismic and mixed amblyopia [
Smooth pursuit involves conjugate eye movements that stabilize the image of a moving target on the fovea. Cortical networks involved in smooth pursuit include areas in the parietal and frontal, as well as subcortical areas, with some overlap with the saccade network [
Von Noorden led the first investigation into the effects of strabismic amblyopia on smooth pursuit and reported lower pursuit velocity and increased saccade frequency (i.e., catch-up saccades) [
Vergence involves disjunctive eye movements to fixate objects presented at different viewing distances [
The effect of amblyopia on vergence eye movements was examined by Kenyon et al. [
To summarize, deficits in eye movements are mainly seen during amblyopic eye viewing for saccades and smooth pursuit in adults with amblyopia. Given that the hallmark of amblyopia is an impairment in binocular vision, vergence movements are also affected; however, this should be examined in more detail with a larger cohort of patients. Importantly, eye movements have not been examined in children with amblyopia, which presents a significant gap in our understanding of how abnormal visual experience affects oculomotor development. Examining eye movements in children with amblyopia during the course of development will provide insight into the plasticity of the visuomotor system.
Investigating upper limb movements provides insight into the neural control of visuomotor behaviour. For example, simple motor responses, such as a button press, have been used to assess the speed of sensorimotor processing, whereas reaching movements have been used to examine visuomotor mapping, motor planning (i.e., feedforward control), and feedback control [
Visuomotor control has been first studied in amblyopia using a manual reaction time paradigm to assess the speed of information processing during a simple stimulus detection task. Results showed increased reaction time for centrally presented targets during amblyopic compared to fellow eye viewing [
Given that central vision deficits are the hallmark of amblyopia, delayed response initiation for targets presented centrally is not surprising. The manual reaction time to peripheral targets was subsequently assessed during monocular viewing by Chelazzi et al. in a group of people with amblyopia and esotropia which ranged from 6 to 40 PD [
Altogether, these studies provide important insight into the effect of amblyopia on the speed of target detection during visuomotor processing. First, the delay in motor response initiation is longer in individuals with strabismic amblyopia compared to anisometropic amblyopia. Second, response initiation is delayed not only for centrally presented targets, but also for peripheral targets presented within 10 deg eccentricity. Third, poorer visual acuity is associated with increased manual response delay, but this relation appears to be stronger for centrally presented targets as compared to responses evoked by peripheral stimuli. Fourth, delays in response initiation persist in strabismic amblyopia after equating stimulus contrast between the two eyes. Overall, these results are consistent with studies that found increased saccade latency during amblyopic compared to fellow eye viewing. Importantly, the delay in both saccade and manual response initiation appears to be greater in individuals with strabismic compared to anisometropic amblyopia.
Abnormal space perception in humans with amblyopia has been documented using a variety of experimental tasks, such as stimulus bisection, alignment, drawing, or pointing [
Most studies that examined spatial processing in amblyopia focused on perceptual alignment tasks, while only a few examined upper limb reaching/pointing responses. Given the dual visual processing streams [
In summary, two main findings emerge from studies that examined the effects of abnormal visual input during development on spatial processing. First, amblyopia is associated with spatial localization deficits across both perceptual (i.e., alignment) and motor (i.e., pointing) tasks. Second, spatial errors are greater in individuals with strabismic amblyopia. Two prominent models have been proposed to explain anomalous spatial processing in amblyopia. Hess et al. used the term “tarachopia” (i.e., scrambled vision) to describe the idea that neural representation of visual input from the amblyopic eye is distorted, which is also referred to as topographical disarray [
To gain a better understanding into how abnormal visual experience during development affects the control of upper limb movements, recent studies used kinematics to examine performance on reach-to-touch [
Optimal motor performance can be operationally defined as movements that are performed fast and accurately, while minimizing the energy and mental costs [
Feedforward and feedback control processes have been examined in adults with amblyopia using kinematics for two different experimental tasks: reach-to-touch [
To summarize, detailed kinematic analysis revealed that decorrelated binocular visual experience during development is associated with a neural adaptation of the motor control system that involves an adjustment of the speed-accuracy trade-off function [
The planning and execution of reach-to-grasp movements is more complex compared to reach-to-touch because in addition to the transport component, grasping involves interacting with an object. In other words, in addition to localizing the target in egocentric coordinates to plan the reach movement [
Precision grasping has been studied in adults and children with amblyopia using a task that involves gripping cylindrical objects. The first study included a group of 20 adults with amblyopia (10 with strabismus and 10 with anisometropia; amblyopic eye acuity 0.20-2.80 logMAR) [
Two other studies examined prehension in amblyopia while manipulating the environmental context. First, the effects of object contrast and lighting on prehension were examined in 13 adults with strabismic or mixed mechanism amblyopia [
The second study examined prehension to objects surrounded by distractors/flankers in 20 adults with amblyopia. Using this experimental approach provides greater ecological insight into the effects of amblyopia on prehension because the objects that we interact with everyday are usually in proximity to other objects [
To summarize, significant prehension deficits have been found in adults with amblyopia during binocular viewing when interacting with high-contrast objects in a well-lit environment. In general, prehension was performed slower and the greatest impact was seen on grasp execution, rather than the reach component. The two measures commonly used to assess grasping are peak grip aperture and grasp duration. It is the latter measure that seems to be more impaired in amblyopia, which provides important insight into the nature of the control mechanism that is disrupted. First, results from Grant et al. [
Results from adult studies are consistent with studies that examined prehension kinematics in a large cohort of 55 children with amblyopia aged 5 to 9 years old [
The fact that stereoacuity seems to be important for prehension and fine motor skills is also supported by a recent study that examined the effects of a newly developed binocular treatment (dichoptically presented iPod game) on fine motor skills in 18 children with mixed amblyopia etiology (mean age 8.5 yrs) [
Altogether, the accumulating evidence suggests that better binocular visual function, specifically stereoacuity, could provide a critical sensory input for the optimal development of prehension and other fine motor skills. Importantly, research shows that younger children seem to be affected to a greater extent compared to older children or adults. The improved performance of adults may be due to extensive practice and learning of compensatory strategies; for example, adaptation might involve relying on haptic feedback more when grasping and manipulating objects. However, studies with a larger sample size of adults and children over a larger age range (i.e., >9 yrs old) are required to establish a more definitive relation between stereoacuity and prehension performance, as well as the contribution of stereoacuity to motor learning. Using kinematics will provide useful insight into which aspects of sensorimotor control are affected, and how the system adapts to compensate for the abnormal visual experience during development.
Maintaining postural stability while standing or navigating through the environment is of paramount importance for everyday function. Sensorimotor integration is key for postural stability control. Vision, along with vestibular and somatosensory inputs, provides sensory information about the position of the body in relation to the environment to ensure upright balance and forward progression during gait [
There is a dearth of studies that examined the effect of amblyopia on balance and gait. Odenrick et al. provided the first report which included 23 children with strabismic amblyopia (the group also included 12 children with strabismus without amblyopia, aged 4.5-10.5 years) [
The next study that examined the effect of impaired stereovision on adaptive gait included 16 adults (9 were amblyopic (5 had negative stereopsis), 7 were strabismic only (5 had negative stereopsis)) [
Finally, a recent study compared postural stability in a cohort of children with amblyopia (
To summarize, evidence from a limited number of studies indicates that decorrelated binocular experience during development has a significant impact on the control of postural stability in children. Parallel research in adults with strabismus revealed reduced stability during quiet stance in comparison to a control group [
The goal of this paper was to provide a synthesis of current knowledge highlighting the changes associated with amblyopia across the three motor systems: oculomotor, manual, and postural. The accumulating body of research indicates that decorrelated visual experience during the early childhood years has a significant impact on visuomotor behaviour, including eye movements and upper limb reaching and grasping, as well as postural stability control. Examination of performance measures across different tasks shows that deficits are clearly evident during amblyopic eye viewing. These deficits include increased latency, slower execution, and reduced movement precision. Importantly, binocular viewing is also associated with some behavioural deficits, such as reduced reading speed, slower prehension, and decreased postural stability. In-depth kinematic analysis revealed that patients adapt compensatory strategies to improve performance. These compensatory behaviours involve secondary corrective eye movements, adjustment of the speed-accuracy trade-off function, and increased reliance on somatosensory feedback when manipulating objects. It is possible that the compensatory behaviours that are seen during binocular and fellow eye viewing depend on higher level cortical plasticity involving changes in connectivity and function of large cortical networks beyond the primary visual areas [
Accumulating evidence indicates that binocularity, rather than just monocular visual acuity, is the critical sensory input contributing to optimal development of the sensorimotor control system. Correlated binocular experience during sensitive periods of development may be necessary for the normal development of the sensorimotor systems involved in the execution of eye movements, upper limb movements, and postural stability. Most intriguingly, developing innovative therapies that target the visuomotor system might facilitate the recovery of binocularity [
The authors declare that there is no conflict of interest regarding the publication of this paper.