Free
Eye Movements, Strabismus, Amblyopia and Neuro-ophthalmology  |   December 2014
Effects of Strabismic Amblyopia and Strabismus Without Amblyopia on Visuomotor Behavior: III. Temporal Eye–Hand Coordination During Reaching
Author Affiliations & Notes
  • Ewa Niechwiej-Szwedo
    Department of Kinesiology, University of Waterloo, Waterloo, Ontario, Canada
  • Herbert C. Goltz
    Department of Ophthalmology and Vision Sciences, The Hospital for Sick Children, Toronto, Ontario, Canada
    University of Toronto, Toronto, Ontario, Canada
  • Manokaraananthan Chandrakumar
    Department of Ophthalmology and Vision Sciences, The Hospital for Sick Children, Toronto, Ontario, Canada
  • Agnes M. F. Wong
    Department of Ophthalmology and Vision Sciences, The Hospital for Sick Children, Toronto, Ontario, Canada
    University of Toronto, Toronto, Ontario, Canada
  • Correspondence: Agnes M. F. Wong, Department of Ophthalmology and Vision Sciences, The Hospital for Sick Children, 555 University Avenue, Toronto, ON M5G 1X8, Canada; agnes.wong@sickkids.ca
Investigative Ophthalmology & Visual Science December 2014, Vol.55, 7831-7838. doi:10.1167/iovs.14-15507
  • Views
  • PDF
  • Share
  • Tools
    • Alerts
      ×
      This feature is available to authenticated users only.
      Sign In or Create an Account ×
    • Get Citation

      Ewa Niechwiej-Szwedo, Herbert C. Goltz, Manokaraananthan Chandrakumar, Agnes M. F. Wong; Effects of Strabismic Amblyopia and Strabismus Without Amblyopia on Visuomotor Behavior: III. Temporal Eye–Hand Coordination During Reaching. Invest. Ophthalmol. Vis. Sci. 2014;55(12):7831-7838. doi: 10.1167/iovs.14-15507.

      Download citation file:


      © ARVO (1962-2015); The Authors (2016-present)

      ×
  • Supplements
Abstract

Purpose.: To examine the effects of strabismic amblyopia and strabismus only, without amblyopia, on the temporal patterns of eye–hand coordination during both the planning and execution stages of visually-guided reaching.

Methods.: Forty-six adults (16 with strabismic amblyopia, 14 with strabismus only, and 16 visually normal) executed reach-to-touch movements toward targets presented randomly 5° or 10° to the left or right of central fixation. Viewing conditions were binocular, monocular viewing with the amblyopic eye, and monocular viewing with the fellow eye (dominant and nondominant viewing for participants without amblyopia). Temporal coordination between eye and hand movements was examined during reach planning (interval between the initiation of saccade and reaching, i.e., saccade-to-reach planning interval) and reach execution (interval between the initiation of saccade and reach peak velocity [PV], i.e., saccade-to-reach PV interval). The frequency and dynamics of secondary reach-related saccades were also examined.

Results.: The temporal patterns of eye–hand coordination prior to reach initiation were comparable among participants with strabismic amblyopia, strabismus only, and visually normal adults. However, the reach acceleration phase of participants with strabismic amblyopia and those with strabismus only were longer following target fixation (saccade-to-reach PV interval) than that of visually normal participants (P < 0.05). This effect was evident under all viewing conditions. The saccade-to-reach planning interval and the saccade-to-reach PV interval were not significantly different among participants with amblyopia with different levels of acuity and stereo acuity loss. Participants with strabismic amblyopia and strabismus only initiated secondary reach-related saccades significantly more frequently than visually normal participants. The amplitude and peak velocity of these saccades were significantly greater during amblyopic eye viewing in participants with amblyopia who also had negative stereopsis.

Conclusions.: Adults with strabismic amblyopia and strabismus only showed an altered pattern of temporal eye–hand coordination during the reach acceleration phase, which might affect their ability to modify reach trajectory using early online control. Secondary reach-related saccades may provide a compensatory mechanism with which to facilitate the late online control process in order to ensure relatively good reaching performance during binocular and fellow eye viewing.

Introduction
Eye–hand coordination is an integral component of many goal-directed activities, including reaching and grasping for objects, using tools, or catching a ball. Research has shown stereotypical eye–hand coordination patterns across various tasks.18 An important feature of this coupling is that saccades are usually initiated ~100 ms prior to the reach,5,9,10 with the eyes fixating on the target at approximately the time of hand peak acceleration and the hand achieving peak velocity at 100 to 200 ms later.9 It has been hypothesized that this temporal saccade-reach coordination pattern allows for acquisition of important sensory information during the early phase of reaching (i.e., during the acceleration phase), which facilitates online control and error correction during the reach deceleration phase. Indeed, reach trajectories exhibit high variability during the acceleration phase, which is significantly reduced during the deceleration phase. For example, Helson et al.11 showed that reach trajectory variability is reduced by a factor of 5 between the time of peak acceleration and movement endpoint. Thus, eye movements may play an important role in acquisition of sensory information during the early phase of the reach which can be used to modify the trajectory during the approach phase. 
Initiating eye movements prior to reaching offers several important advantages. For example, moving the eyes to fixate on the target provides a high-acuity image which can facilitate extraction of fine details, such as the object's texture. Even in cases when high-acuity resolution of target features is not required, moving the eyes to the target improves endpoint accuracy and precision.8,12,13 On the other hand, asking subjects to point to a previously fixed target results in a constant error due to remapping of target location associated with the eye movement.14,15 These studies indicate that information related to the efferent oculomotor command and the visual and extraretinal feedback associated with the eye movement are used by the manual system during reach planning and execution. Thus, optimal temporal eye–hand coordination is important for efficient execution of manual responses. 
Amblyopia is a neurodevelopmental disorder that affects spatial and temporal visual processing, as well as higher order perceptual functions, including form and motion perception and attention and decision making.1621 Previous studies have shown a clear distinction between strabismic and anisometropic amblyopia.18,22,23 For example, patients with strabismic amblyopia are more likely to have negative stereopsis and better contrast sensitivity than patients with anisometropia with a similar level of acuity loss in the amblyopic eye.18 Because vision provides very important input for guiding upper limb movements, our group endeavored to characterize visuomotor behaviors in adults with amblyopia, including the effects of anisometropic amblyopia on the planning and execution of saccadic eye movements,24 visually-guided reaching,25 and eye–hand coordination.26,27 We also reported the effects of strabismic amblyopia on saccades28 and reaching.29 In this study, we investigated eye–hand coordination in adults with strabismic amblyopia by comparing their performance to that of adults with strabismus only, without amblyopia, and to that of visually normal adults. 
Materials and Methods
Participants
The sample included 16 adults with strabismic amblyopia (9 males at a mean of 32 ± 9 years of age), 14 with strabismus only, without amblyopia (7 males at a mean of 30 ± 5 years of age), and 16 visually normal adults (9 males at a mean 31 ± 9 years of age). All participants underwent complete orthoptic assessment by a certified orthoptist, which included visual acuity testing using the Snellen chart, measurement of eye alignment by using the prism cover test, measurement of refractive errors, and stereoscopic acuity (stereoacuity) testing using the Titmus test. Detailed characteristics for participants with strabismic amblyopia and those with strabismus only can be found in a recent publication29 and in Supplementary Table S1. Briefly, all participants with amblyopia had visual acuity between 20/30 and 20/200 in the amblyopic eye, 20/20 or better in the fellow eye, and an interocular acuity difference of ≥2 lines. Strabismic amblyopia was defined as amblyopia in the presence of an eye misalignment of >8 prism diopters. The difference in refractive errors between the two eyes was <1 diopter in spherical or cylindrical power to rule out anisometropia. Participants with strabismus had visual acuity of only 20/25 or better in each eye. Nine of them had no stereopsis, two had stereoacuity of 3000 seconds of arc, and the remaining three had stereoacuity between 50 and 70 seconds of arc. Visually normal participants had normal or corrected-to-normal visual acuity of 20/20. Exclusion criteria included any ocular cause for reduced visual acuity, prior intraocular surgery, or any neurologic disease. The study was approved by the Research Ethics Board at The Hospital for Sick Children, and all protocols adhered to the guidelines of the Declaration of Helsinki. Informed consent was obtained from each participant. 
Apparatus
Detailed description of the apparatus and the experimental protocol can be found in our recent paper.29 Briefly, participants were seated at a table with their heads stabilized by a chin rest. Eye movements were recorded at 200 Hz, using an infrared video-based binocular pupil/iris tracking system (Chronos Vision, Berlin, Germany). Reaching movements were recorded at 200 Hz by using an infrared illumination-based motion capture system (Optotrak Certus 3020; Northern Digital, Waterloo, Ontario, Canada). The coordinate system was defined as an x-axis horizontal plane, a y-axis vertical plane, and a z-axis median plane (depth). Two infrared markers (4-mm diameter) were affixed to the index fingertip and wrist joint of the participant's right (dominant) hand. 
The visual stimulus was a white circle (visual angle of 0.25°) presented on a black background, generated by a customized Matlab script (MathWorks, Natick, MA, USA) and presented on a 20-inch cathode-ray tube computer screen (Diamond Pro 2070SB; resolution of 1600 × 1200 at 85 Hz) located 42 cm from the subject. Testing was conducted in a dimly lit room. 
Participants executed reaching movements under three viewing conditions: both eyes (BE), monocular amblyopic eye (AE), and monocular fellow eye (FE). For control participants and participants with strabismus only, views were was monocular with the dominant and nondominant eyes. Each viewing condition was collected in a block, and the order was randomized among the participants. At the start of each trial, the right hand was placed on the table, and the index finger was placed on the force-sensitive resistor. Participants fixated on a cross presented at midline. After a variable delay (1.5–3 seconds), the target was presented at 1 of 4 eccentricities: ±5° or ±10° along the azimuth at eye level. Participants were instructed to look and point to the target as fast and as accurately as possible. 
Participants completed 10 trials in each combination of the experimental conditions for a total of 240 trials. The intertrial interval varied among trials, and it was at least 5 seconds. Practice trials were completed prior to starting the experiment in order to familiarize the participants with the experimental procedure. 
Data Analysis
Temporal coordination between eye and hand movements was examined in two stages of the reaching movement: the planning stage (i.e., from target onset to reach initiation) and the execution stage (i.e., from reach onset to the end of movement). Figure 1 shows the temporal coordination obtained in a single trial from a participant with strabismic amblyopia, a participant with strabismus only, without amblyopia, and a visually normal participant. Eye–hand coordination during the planning stage was assessed by calculating the saccade-to-reach planning interval, that is, the time interval after the eyes fixated on the target (i.e., at the end of saccade) and the initiation of the reaching response (Fig. 1, A [arrow]). This was calculated on a trial-by-trial basis by subtracting saccade reaction time (latency) and saccade duration from the reach reaction time. It reflects the time that was available for planning of the reaching response after the saccade had been completed and the eyes were in the vicinity of the target. 
Figure 1
 
Saccade and reach velocity data from a single trial for a representative participant from each group, showing strabismic amblyopia (a), strabismus only (b), and visually normal (c) subjects. The saccade-to-reach planning interval is labeled A (arrow), and the saccade-to-reach-peak velocity interval is labeled B (arrow).
Figure 1
 
Saccade and reach velocity data from a single trial for a representative participant from each group, showing strabismic amblyopia (a), strabismus only (b), and visually normal (c) subjects. The saccade-to-reach planning interval is labeled A (arrow), and the saccade-to-reach-peak velocity interval is labeled B (arrow).
The planning stage of the reach response was also assessed by examining the frequency of trials when the hand movement was initiated prior to the eye movement. The accuracy and precision of the reaching response were compared between trials when reaching was initiated prior to or after the saccade. 
Eye–hand coordination during the reach execution stage was assessed by calculating the saccade-to-reach peak velocity (PV) interval, that is, the time interval between the end of the saccade and reach PV. This was calculated on a trial-by-trial basis by subtracting saccade reaction time and saccade duration from the time the hand reached PV (Fig. 1, B [arrow]). It reflects the duration of time after the eyes fixated on the target during the early part of reach execution. Visual information acquired during this interval, which includes the acceleration phase of the reach, can be used to make compensatory adjustments to the reach trajectory in the later part of the movement.21 
Eye–hand coordination during the reach execution stage was also assessed by examining the frequency of secondary saccades. As in our previous paper,27 secondary saccades that occurred during the reach and those that occurred >250 ms after the primary saccades were defined as reach-related saccades. We reasoned that these saccades were reach-related and were not secondary “corrective” saccades after the primary saccades under- or overshot because secondary corrective saccades typically occur with a latency of 100 to 250 ms.42,43 The amplitude, peak velocity, and latency (with respect to the initiation of the reach response) of the reach-related saccades were calculated. Secondary corrective saccades following primary saccades were reported in our previous paper.28 
Statistical Analysis
All continuous dependent variables (saccade-to-reach planning interval, saccade-to-reach PV interval, latency, amplitude, and PV of reach-related saccades) were submitted to a repeated-measures, mixed ANOVA with group (consisting of three levels: visually normal participants, participants with strabismic amblyopia, and participants with strabismus only) as a between-subjects factor and viewing condition (also three levels: both eyes, monocular fellow eye, and monocular amblyopic eye [i.e., dominant and nondominant eyes for control participants and participants with strabismus only]) as a within-subjects factor. 
The frequency of reach-related saccades was compared among groups using Pearson's chi-square statistic. The effect of Viewing Condition was then examined within each group using Pearson's chi-squared statistic. 
All statistical analyses were performed using SAS 9.2 software (SAS, Cary, NC, USA). Descriptive statistics were reported as means and corresponding standard deviations. Any main effects and interactions were analyzed further by using Tukey-Kramer post hoc tests to adjust for multiple comparisons. The significance level was set at P value of <0.05. Preliminary analysis showed that visual feedback of target had no significant effect on any outcome measures; therefore, data with or without visual feedback were collapsed for analysis and reporting. 
Results
Saccade-to-Reach Planning Interval
Figure 2 shows the cumulative probability distributions of saccade-to-reach planning intervals for visually normal participants, participants with strabismic amblyopia, and participants with strabismus only across viewing conditions. Saccade-to-reach planning interval was not significantly different among the groups (F2,43 = 1.11, nonsignificant [ns]) and the interaction between group and viewing condition was also not significant (F4,86 = 2.11, ns). Control participants initiated reaching at ~105 ms after the eyes fixated on the target, regardless of viewing condition (both eyes: 108 ± 82 ms; dominant eye: 98 ± 74 ms; nondominant eye: 110 ± 62 ms). For participants with strabismic amblyopia, the saccade-to-reach planning interval was 160 ± 94 ms viewing with both eyes, 150 ± 92 ms during fellow eye viewing, and 137 ± 104 ms during amblyopic eye viewing. Participants with strabismus only also had comparable saccade-to-reach planning intervals across viewing conditions (both eyes: 135 ± 86 ms; dominant eye: 126 ± 77 ms; nondominant eye: 150 ± 115 ms). 
Figure 2
 
Cumulative probability distributions for saccade-to-reach planning interval illustrating the temporal relationship between the eye and hand movements during the planning stage of the reaching movement. Each curve represents mean data from one viewing condition (both eyes: black; fellow [dominant] eye: green; amblyopic [nondominant] eye: red) for visually normal participants (solid lines), participants with strabismic amblyopia (dashed lines), and patients with strabismus only (dotted lines).
Figure 2
 
Cumulative probability distributions for saccade-to-reach planning interval illustrating the temporal relationship between the eye and hand movements during the planning stage of the reaching movement. Each curve represents mean data from one viewing condition (both eyes: black; fellow [dominant] eye: green; amblyopic [nondominant] eye: red) for visually normal participants (solid lines), participants with strabismic amblyopia (dashed lines), and patients with strabismus only (dotted lines).
As illustrated in Figure 2, saccades were initiated prior to reaching (i.e., positive saccade-to-reach planning interval) in the majority of trials in visually normal participants (98.1%) and participants with strabismic amblyopia (98.6%). Participants with strabismus only had significantly fewer trials where saccades were initiated prior to reaching (96.0%; χ2(df = 2) = 42.9; P < 0.0001). There were no significant differences among viewing conditions for control participants (both eyes: 98.3%; dominant eye: 97.3%; nondominant eye: 98.7%) or participants with strabismus only (both eyes: 96.2%; dominant eye: 96.4%; nondominant eye: 95.4%). In contrast, participants with amblyopia initiated saccades prior to reaching with slightly reduced frequency when viewing with the amblyopic eye (97.1%) in comparison to viewing with both eyes (99.2%) and fellow eye viewing (98.9%; χ2(df = 2) = 16.2; P = 0.0003). There were no differences in accuracy or precision of reaching movements between trials when the reach was initiated prior to or following a saccade. 
Saccade-to-Reach PV Interval
Cumulative probability distributions of the saccade-to-reach PV intervals for all participants across viewing conditions are plotted in Figure 3a. The cumulative probability distributions for participants with strabismic amblyopia and participants with strabismus only were clustered together and shifted toward an interval that was longer than that in visually normal participants, indicating that they extended the acceleration phase of the reach once the eyes fixated on the target. Statistical analysis confirmed a significant effect of group (F2,43 = 4.16; P = 0.022). As shown in Figure 3b, saccade-to-reach PV intervals were comparable across viewing conditions in visually normal participants (both eyes: 274 ± 98 ms; dominant eye: 278 ± 93 ms; nondominant: 294 ± 87 ms). Saccade-to-reach PV intervals were longer in participants with strabismic amblyopia (both eyes: 377 ± 109 ms; fellow eye: 377 ± 115 ms; amblyopic eye: 364 ± 141milliseconds) and in participants with strabismus only (both eyes: 358 ± 111 ms; dominant eye: 364 ± 102 ms; nondominant eye: 390 ± 151 ms). 
Figure 3
 
(a) Cumulative probability distributions for saccade-to-reach-peak velocity interval across viewing conditions illustrating the temporal relationship between the eye and hand movements during the execution stage of the reaching movement. Each curve represents mean data from one viewing condition (both eyes: black; fellow [dominant] eye: green; amblyopic [nondominant] eye: red) for visually normal participants (solid lines), participants with strabismic amblyopia (dashed lines) and participants with strabismus only (dotted lines). The cumulative probability distributions for participants with abnormal binocular vision were shifted toward intervals that were longer than those for control participants. (b) The mean saccade-to-reach peak velocity interval across viewing conditions. The interval was significantly longer in participants with abnormal binocular vision, regardless of viewing condition (P = 0.022). Error bars: ±1 SE.
Figure 3
 
(a) Cumulative probability distributions for saccade-to-reach-peak velocity interval across viewing conditions illustrating the temporal relationship between the eye and hand movements during the execution stage of the reaching movement. Each curve represents mean data from one viewing condition (both eyes: black; fellow [dominant] eye: green; amblyopic [nondominant] eye: red) for visually normal participants (solid lines), participants with strabismic amblyopia (dashed lines) and participants with strabismus only (dotted lines). The cumulative probability distributions for participants with abnormal binocular vision were shifted toward intervals that were longer than those for control participants. (b) The mean saccade-to-reach peak velocity interval across viewing conditions. The interval was significantly longer in participants with abnormal binocular vision, regardless of viewing condition (P = 0.022). Error bars: ±1 SE.
Reach-Related Secondary Saccades
Frequency.
The frequency of reach-related saccades was greater in participants with strabismic amblyopia (11.4%) and in participants with strabismus only (15.4%) than in visually normal participants (8.9%; χ2(df=2) = 66.4, P < 0.0001). Visually normal participants executed reach-related saccades less frequently during binocular viewing (6.3%) than during monocular viewing (dominant eye: 8.7%; nondominant eye: 11.9%; χ2(df=2) = 24.8; P < 0.0001). Similarly, participants with amblyopia initiated significantly fewer reach-related saccades when viewing with both eyes (7.5%) than when viewing with the fellow eye (14.0%) and with the amblyopic eye (12.7%; χ2(df=2) = 28.8; P < 0.0001). In contrast, participants with strabismus only had comparable frequency of reach-related saccades across all viewing conditions (both eyes: 14.1%; dominant eye: 15.6%; nondominant eye: 16.2%). 
Latency.
There were no significant differences between group and viewing condition for the latency of reach-related saccades. 
Amplitude of Reach-Related Saccades.
The interaction between group and viewing condition was significant for the amplitude of reach-related saccades (F4,79 = 5.54; P = 0.0006). As illustrated in Figure 4a, for visually normal participants, amplitude was not different among viewing conditions (both eyes: 0.99 ± 0.33°; dominant eye: 1.09 ± 0.44°; nondominant eye: 1.07 ± 0.43°). Similarly, participants with strabismus only had comparable amplitudes when viewing with both eyes (1.08 ± 0.44°), during dominant eye viewing (1.19 ± 0.52°) and nondominant eye viewing (1.05 ± 0.44°). In contrast, post hoc testing revealed that participants with amblyopia had significantly higher reach-related saccade amplitudes during amblyopic eye viewing (1.49 ± 0.48°) than during viewing with the fellow eye (0.92 ± 0.28°) or with both eyes (0.97 ± 0.36°). 
Figure 4
 
Kinematics of reach-related secondary saccades across viewing conditions. The amplitude (a) and peak velocity (b) of reach-related secondary saccades in participants with strabismic amblyopia were significantly higher during amblyopic eye viewing than those in visually normal participants and participants with strabismus only (P < 0.05).
Figure 4
 
Kinematics of reach-related secondary saccades across viewing conditions. The amplitude (a) and peak velocity (b) of reach-related secondary saccades in participants with strabismic amblyopia were significantly higher during amblyopic eye viewing than those in visually normal participants and participants with strabismus only (P < 0.05).
Peak Velocity of Reach-Related Saccades.
The interaction between group and viewing condition was also significant for the PV of reach-related saccades (F4,79 = 4.99; P = 0.001) (Fig. 4b). For visually normal participants, PV was not different between viewing conditions (both eyes: 72 ± 18 deg/s; dominant eye: 79 ± 25 deg/s; nondominant eye: 77 ± 20 deg/s). Participants with strabismus only also had comparable PV when viewing with both eyes (84 ± 29 deg/s), during dominant eye viewing (84 ± 29 deg/s) and nondominant eye viewing (83 ± 16 deg/s). In contrast, post hoc tests indicated that participants with amblyopia had significantly higher PV during amblyopic eye viewing (108 ± 26 deg/s) than when viewing with the fellow eye (76 ± 22 deg/s) and with both eyes (82 ± 28 deg/s). 
Effects of Reduced Acuity and Stereoacuity in Participants With Amblyopia
The saccade-to-reach planning interval and the saccade-to-reach PV interval were not significantly different between participants with amblyopia with different levels of loss of acuity and stereoacuity (Table). The only significant difference among participants with amblyopia was found for the amplitude (F4,23 = 17.83; P < 0.0001) and PV (F4,23 = 7.50; P < 0.001) of reach-related saccades. Post hoc tests showed that participants with negative stereopsis had greater saccadic amplitude and PV when viewing with the amblyopic eye than when viewing with both eyes and with fellow eye viewing (Table). 
Table.
 
Details of Eye-Hand Coordination During the Planning and Execution of Reaching for Participants With Amblyopia
Table.
 
Details of Eye-Hand Coordination During the Planning and Execution of Reaching for Participants With Amblyopia
Parameter Mild and Stereo+ (n = 5)* Mild and Stereo (n = 6)* Severe and Stereo (n = 5)
BE FE AE BE FE AE BE FE AE
Saccade-to-reach planning interval, ms 146 ± 105 132 ± 119 115 ± 76  172 ± 105 161 ± 77  171 ± 108 158 ± 65  154 ± 76  114 ± 111
Saccade-to-reach PV interval, ms 375 ± 76  367 ± 74  363 ± 112 400 ± 112 408 ± 116 409 ± 143 351 ± 125 348 ± 137 310 ± 145
Reach-related saccade kinematic
 Frequency, % 4.4 10.6* 6.5 10.5 19.9* 18.9* 6.7 10.2 11.0
 Amplitude, deg 1.00 ± 0.40 0.95 ± 0.17 1.07 ± 0.38  1.16 ± 0.33 1.15 ± 0.21 1.39 ± 0.27* 0.72 ± 0.26 0.62 ± 0.08 1.96 ± 0.36*
 Peak velocity, deg/s 94 ± 36 77 ± 14 89 ± 31 89 ± 23 91 ± 18 106 ± 17*  66 ± 27 55 ± 15 124 ± 24* 
Discussion
Our major findings are (1) participants with strabismic amblyopia, strabismus only, and visually normal participants had a comparable temporal pattern of eye–hand coordination prior to reach initiation; (2) participants with strabismic amblyopia and strabismus only extended the reach acceleration phase after the end of saccades, and they also initiated reach-related saccades with greater frequency than control participants did; (3) only participants with amblyopia and negative stereopsis exhibited differences in the kinematics of reach-related saccades. Specifically, the amplitude and PV were higher during amblyopic eye viewing than during other viewing conditions. 
Our findings indicate that the peripheral information about target location is normal in patients with strabismic amblyopia because these patients did not extend their planning time after fixating on the target, independent of their acuity or stereoacuity deficits. This finding is in contrast with our previous findings in patients with anisometropic amblyopia, in which those with severely reduced acuity (<20/200) and negative stereoacuity spent longer in the planning interval after fixating on the target prior to reaching initiation.27 These results can be explained by considering the mechanism of strabismic and anisometropic amblyopia. In the case of strabismic amblyopia, there is a stronger suppression of the central visual field, presumably to avoid diplopia, whereas suppression in the periphery is weaker or absent.3032 In contrast, in anisometropic amblyopia, suppression is uniform across the entire visual field. Our study extends previous findings that examined the effect of amblyopia on spatial perception23,30,3340 by showing that the temporal pattern of eye–hand coordination during reach planning (i.e., prior to reach initiation) toward peripheral targets is not altered in patients with strabismic amblyopia, which differs from patients with anisometropic amblyopia. 
In contrast to the planning interval, all patients with abnormal binocular vision (those with strabismic amblyopia and those with strabismus only) had a prolonged saccade-to-reach PV interval compared to visually normal participants, regardless of the extent of the acuity or stereoacuity deficit. These findings are consistent with our previous results in patients with anisometropic amblyopia, who also spent a similar duration in the acceleration phase after fixating the target, regardless of viewing condition.27 Our results can be considered in the context of the three error correction processes described by Elliott et al.41 to optimize the accuracy and precision of reaching movements, as follows: (1) fast, in which automatic online corrections are implemented early in the movement trajectory (i.e., during the reach acceleration phase); (2) slow, when online corrections are implemented late in the movement trajectory (i.e., during the reach deceleration phase); and (3) offline corrections, in which feedback at the end of the movement is used to program the next movement. 
The ability to implement fast, automatic online corrections during reaching requires an internal model,42,43 by which the central nervous system compares the intended motor command with the actual motor command (i.e., efference), as well as the expected sensory feedback (for a given motor command) with the actual sensory feedback.44 When there is a mismatch between the expected and actual efference and/or sensory feedback, the movement trajectory will be amended quickly without conscious awareness (i.e., implicit error correction).45,46 The effectiveness of this error correction process depends on a precisely calibrated internal model. Our results show that participants with abnormal binocular vision extend the acceleration phase after target fixation, indicating that patients' ability to correct trajectory errors using the early online correction process may be disrupted. 
Reach trajectory can be also modified via the slow online error correction process during the reach deceleration phase.41,47 Our study shows that participants with strabismic amblyopia and strabismus only initiated reach-related saccades more frequently than visually normal subjects, similar to participants with anisometropic amblyopia.27 Because patients' early online control process is disrupted, these reach-related saccades are initiated during the reach acceleration phase to acquire sensory information which could then be used to modify the reach trajectory during the deceleration phase, allowing patients to achieve relatively good reach performance. This is supported by our previous findings which showed that reach accuracy and precision were comparable in people with strabismic amblyopia, strabismus only, and visually normal subjects during binocular and fellow eye viewing.29 In contrast, both reach accuracy and precision were reduced during amblyopic eye viewing in participants with negative stereopsis.29 It is possible that the increased reaching errors may be related to a reduced ability to use the late online control process mediated via reach-related saccades. Specifically, the amplitude and PV of reach-related saccades were higher during amblyopic eye viewing in participants with amblyopia and negative stereopsis, indicating that the retinal error signal used to initiate these eye movements is less reliable (i.e., a larger retinal error signal is necessary to initiate these reach-related saccades). This disruption in initiating reach-related saccades may contribute to reduced reach accuracy and precision.29 Results from the current study help to elucidate a potential mechanism involved during the slow online error correction process, information acquired via reach-related secondary saccades is used to modify reach trajectory, but this process is limited by the quality of visual input, that is, the sensory uncertainty associated with that input. 
The current study concludes our detailed characterization of visuomotor behavior during reaching in adults with strabismic amblyopia and complements our previous work conducted in adults with anisometropic amblyopia. This body of work reveals how the visuomotor system adapts to disrupted visual input due to the presence of blur (anisometropia) or ocular misalignment (strabismus) during development. The most important finding is that regardless of the cause of amblyopia, patients adopt similar reaching strategies, which is evident under all viewing conditions, suggesting that the normal development of reaching is disrupted when high-grade binocular vision is not available during the developmental period. By including patients with strabismus only as another control group, we were able to show that binocularity, rather than visual acuity, is the most important factor contributing to the development of optimal eye–hand coordination. 
We cannot draw a direct link between our study and the functional impact on everyday activities. However, several researchers have investigated the functional significance of binocular vision by using complex visuomotor tasks and clinical test batteries4851 (for a comprehensive review please see the study by Grant and Moseley52) and found that some people with abnormal binocular vision have significant deficits in the performance of fine motor skills. Our studies elucidate the processes (i.e., planning or execution) that are likely disrupted during performance of these complex motor tasks that may help to develop targeted visuomotor therapies or training for people with amblyopia. 
Acknowledgments
Supported by MRC Operating Grant Program Grants 89763 and 57853 from the Canadian Institutes of Health Research, Leaders Opportunity Fund from the Canadian Foundation for Innovation, the Department of Ophthalmology and Vision Sciences and the Research Training Centre at The Hospital for Sick Children. 
Disclosure: E. Niechwiej-Szwedo, None; H.C. Goltz, None; M. Chandrakumar, None; A.M.F. Wong, None 
References
Bowman MC Johannson RS Flanagan JR. Eye-hand coordination in a sequential target contact task. Exp Brain Res. 2009; 195: 273–283. [CrossRef] [PubMed]
Bekkering H Sailer U. Commentary: coordination of eye and hand in time and space. Prog Brain Res. 2002; 140: 365–373. [PubMed]
van Donkelaar P. Eye-hand interactions during goal-directed pointing movements. Neuroreport. 1997; 8: 2139–2142. [CrossRef] [PubMed]
Johansson RS Westling G Backstrom A Flanagan JR. Eye-hand coordination in object manipulation. J Neurosci. 2001; 21: 6917–6932. [PubMed]
Abrams RA Meyer DE Kornblum S. Eye-hand coordination: oculomotor control in rapid aimed limb movements. J Exp Psychol Hum Percept Perform. 1990; 16: 248–267. [CrossRef] [PubMed]
Sailer U Eggert T Ditterich J Straube A. Spatial and temporal aspects of eye-hand coordination across different tasks. Exp Brain Res. 2000; 134: 163–173. [CrossRef] [PubMed]
Ma-Wyatt A Stritzke M Trommershauser J. Eye-hand coordination while pointing rapidly under risk. Exp Brain Res. 203: 131–145. [CrossRef] [PubMed]
Desmurget M Turner RS Prablanc C Russo GS Alexander GE Grafton ST. Updating target location at the end of an orienting saccade affects the characteristics of simple point-to-point movements. J Exp Psychol Hum Percept Perform. 2005; 31: 1510–1536. [CrossRef] [PubMed]
Helsen WF Elliot D Starkes JL Ricker KL. Temporal and spatial coupling of point of gaze and hand movements in aiming. J Mot Behav. 1998; 30: 249–259. [CrossRef] [PubMed]
Vercher JL Magenes G Prablanc C Gauthier GM. Eye-head-hand coordination in pointing at visual targets: spatial and temporal analysis. Exp Brain Res. 1994; 99: 507–523. [CrossRef] [PubMed]
Helsen WF Elliott D Starkes JL Ricker KL. Coupling of eye, finger, elbow, and shoulder movements during manual aiming. J Mot Behav. 2000; 32: 241–248. [CrossRef] [PubMed]
Prablanc C Echallier JE Jeannerod M Komilis E. Optimal response of eye and hand motor systems in pointing at a visual target. II. Static and dynamic visual cues in the control of hand movement. Biol Cybern. 1979; 35: 183–187. [CrossRef] [PubMed]
Bock O. Localization of objects in the peripheral visual field. Behav Brain Res. 1993; 56: 77–84. [CrossRef] [PubMed]
Henriques DY Klier EM Smith MA Lowy D Crawford JD. Gaze-centered remapping of remembered visual space in an open-loop pointing task. J Neurosci. 1998; 18: 1583–1594. [PubMed]
Henriques DY Medendorp WP Khan AZ Crawford JD. Visuomotor transformations for eye-hand coordination. Prog Brain Res. 2002; 140: 329–340. [PubMed]
Levi DM. Visual processing in amblyopia: human studies. Strabismus. 2006; 14: 11–19. [CrossRef] [PubMed]
Williams C Harrad R. Amblyopia: contemporary clinical issues. Strabismus. 2006; 14: 43–50. [CrossRef] [PubMed]
McKee SP Levi DM Movshon JA. The pattern of visual deficits in amblyopia. J Vis. 2003; 3 (5): 380–405. [PubMed]
Holmes JM Clarke MP. Amblyopia. Lancet. 2006; 367: 1343–1351. [CrossRef] [PubMed]
Birch EE. Amblyopia and binocular vision. Prog Retin Eye Res. 2013; 33: 67–84. [CrossRef] [PubMed]
Wong AM. New concepts concerning the neural mechanisms of amblyopia and their clinical implications. Can J Ophthalmol. 2012; 47: 399–409. [CrossRef] [PubMed]
Ho CS Giaschi D. Low and high-level motion perception deficits in anisometropic and strabismic amblyopia: evidence from fMRI. Vision Res. 2009; 49: 2891–2901. [CrossRef] [PubMed]
Hess RF Holliday IE. The spatial localization deficit in amblyopia. Vision Res. 1992; 32: 1319–1339. [CrossRef] [PubMed]
Niechwiej-Szwedo E Goltz HC Chandrakumar M Hirji ZA Wong AM. Effects of anisometropic amblyopia on visuomotor behavior, I: saccadic eye movements. Invest Ophthalmol Vis Sci. 2010; 51: 6348–6354. [CrossRef] [PubMed]
Niechwiej-Szwedo E Goltz H Chandrakumar M Hirji ZA Crawford JD Wong AM. Effects of anisometropic amblyopia on visuomotor behaviour: II. Visually-guided reaching. Invest Ophthalmol Vis Sci. 2011; 52: 795–803. [CrossRef] [PubMed]
Niechwiej-Szwedo E Goltz H Wong AMF. Deficits and adaptation of eye-hand coordination during visually guided reaching movements in people with amblyopia. In: Steeves JK Harris LR eds. Plasticity in Sensory Systems. New York: Cambridge University Press; 2013; 49–72.
Niechwiej-Szwedo E Goltz HC Chandrakumar M Hirji Z Wong AM. Effects of anisometropic amblyopia on visuomotor behaviour: III. Temporal eye-hand coordination during reaching. Invest Ophthalmol Vis Sci. 2011; 52: 5853–5861. [CrossRef] [PubMed]
Niechwiej-Szwedo E Chandrakumar M Goltz HC Wong AM. Effects of strabismic amblyopia and strabismus without amblyopia on visuomotor behavior, I: saccadic eye movements. Invest Ophthalmol Vis Sci. 2012; 53: 7458–7468. [CrossRef] [PubMed]
Niechwiej-Szwedo E Goltz H Chandrakumar M Wong AMF. Effects of strabismic amblyopia on visuomotor behaviour: Part 2. Visually guided reaching. Invest Ophthalmol Vis Sci. 2014; 55: 3857–3865. [CrossRef] [PubMed]
Sireteanu R Fronius M. Human amblyopia: structure of the visual field. Exp Brain Res. 1990; 79: 603–614. [CrossRef] [PubMed]
Sireteanu R Fronius M Singer W. Binocular ineraction in the peripheral visual field of humans with strabismic and anisometropic amblyopia. Vis Res. 1981; 21: 1065–1074. [CrossRef] [PubMed]
Hess RF Pointer JS. Differences in the neural basis of human amblyopia: the distribution of the anomaly across the visual field. Vision Res. 1985; 25: 1577–1594. [CrossRef] [PubMed]
Bedell HE Flom MC. Normal and abnormal space perception. Am J Optom Physiol Opt. 1983; 60: 426–435. [CrossRef] [PubMed]
Bedell HE Flom MC Barbeito R. Spatial aberrations and acuity in strabismus and amblyopia. Invest Ophthalmol Vis Sci. 1985; 26: 909–916. [PubMed]
Fronius M Sireteanu R. Pointing errors in strabismics: complex patterns of distorted visuomotor coordination. Vision Res. 1994; 34: 689–707. [CrossRef] [PubMed]
Fronius M Sireteanu R. Monocular geometry is selectively distorted in the central visual field of strabismic amblyopes. Invest Ophthalmol Vis Sci. 1989; 30: 2034–2044. [PubMed]
Levi DM Klein SA. Spatial localization in normal and amblyopic vision. Vision Res. 1983; 23: 1005–1017. [CrossRef] [PubMed]
Levi DM Waugh SJ Beard BL. Spatial scale shifts in amblyopia. Vision Res. 1994; 34: 3315–3333. [CrossRef] [PubMed]
Sireteanu R Baumer CC Sarbu C Iftime A. Spatial and temporal misperceptions in amblyopic vision. Strabismus. 2007; 15: 45–54. [CrossRef] [PubMed]
Sireteanu R Fronius M. Naso-temporal asymmetries in human amblyopia: consequence of long-term interocular suppression. Vision Res. 1981; 21: 1055–1063. [CrossRef] [PubMed]
Elliott D Hansen S Grierson LE Lyons J Bennett SJ Hayes SJ. Goal-directed aiming: two components but multiple processes. Psychol Bull. 2010; 136: 1023–1044. [CrossRef] [PubMed]
Wolpert DM Ghahramani Z. Computational principles of movement neuroscience. Nat Neurosci. 2000; (suppl 3): 1212–1217.
Diedrichsen J Shadmehr R Ivry RB. The coordination of movement: optimal feedback control and beyond. Trends Cogn Sci. 2009; 14: 31–39. [CrossRef] [PubMed]
Donaldson IM. The functions of the proprioceptors of the eye muscles. Philos Trans R Soc Lond B Biol Sci. 2000; 355: 1685–1754. [CrossRef] [PubMed]
Todorov E. Optimality principles in sensorimotor control. Nat Neurosci. 2004; 7: 907–915. [CrossRef] [PubMed]
Shadmehr R Smith MA Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010; 33: 89–108. [CrossRef] [PubMed]
Elliott D Helsen WF Chua R. A century later: Woodworth's (1899) two-component model of goal-directed aiming. Psychol Bull. 2001; 127: 342–357. [CrossRef] [PubMed]
O'Connor AR Birch EE Anderson S Draper H. Relationship between binocular vision, visual acuity, and fine motor skills. Optom Vis Sci. 2010; 87: 942–947. [CrossRef] [PubMed]
O'Connor AR Birch EE Anderson S Draper H. The functional significance of stereopsis. Invest Ophthalmol Vis Sci. 2009; 51: 2019–2023. [CrossRef] [PubMed]
Webber AL Wood JM Gole GA Brown B. The effect of amblyopia on fine motor skills in children. Invest Ophthalmol Vis Sci. 2008; 49: 594–603. [CrossRef] [PubMed]
Schiller PH Kendall GL Kwak MC Slocum WM. Depth perception, binocular integration and hand-eye coordination in intact and stereo impaired human subjects. J Clin Exp Ophthalmol. 2012; 3: 1–12. [CrossRef]
Grant S Moseley MJ. Amblyopia and real-world visuomotor tasks. Strabismus. 2011; 19: 119–128. [CrossRef] [PubMed]
Figure 1
 
Saccade and reach velocity data from a single trial for a representative participant from each group, showing strabismic amblyopia (a), strabismus only (b), and visually normal (c) subjects. The saccade-to-reach planning interval is labeled A (arrow), and the saccade-to-reach-peak velocity interval is labeled B (arrow).
Figure 1
 
Saccade and reach velocity data from a single trial for a representative participant from each group, showing strabismic amblyopia (a), strabismus only (b), and visually normal (c) subjects. The saccade-to-reach planning interval is labeled A (arrow), and the saccade-to-reach-peak velocity interval is labeled B (arrow).
Figure 2
 
Cumulative probability distributions for saccade-to-reach planning interval illustrating the temporal relationship between the eye and hand movements during the planning stage of the reaching movement. Each curve represents mean data from one viewing condition (both eyes: black; fellow [dominant] eye: green; amblyopic [nondominant] eye: red) for visually normal participants (solid lines), participants with strabismic amblyopia (dashed lines), and patients with strabismus only (dotted lines).
Figure 2
 
Cumulative probability distributions for saccade-to-reach planning interval illustrating the temporal relationship between the eye and hand movements during the planning stage of the reaching movement. Each curve represents mean data from one viewing condition (both eyes: black; fellow [dominant] eye: green; amblyopic [nondominant] eye: red) for visually normal participants (solid lines), participants with strabismic amblyopia (dashed lines), and patients with strabismus only (dotted lines).
Figure 3
 
(a) Cumulative probability distributions for saccade-to-reach-peak velocity interval across viewing conditions illustrating the temporal relationship between the eye and hand movements during the execution stage of the reaching movement. Each curve represents mean data from one viewing condition (both eyes: black; fellow [dominant] eye: green; amblyopic [nondominant] eye: red) for visually normal participants (solid lines), participants with strabismic amblyopia (dashed lines) and participants with strabismus only (dotted lines). The cumulative probability distributions for participants with abnormal binocular vision were shifted toward intervals that were longer than those for control participants. (b) The mean saccade-to-reach peak velocity interval across viewing conditions. The interval was significantly longer in participants with abnormal binocular vision, regardless of viewing condition (P = 0.022). Error bars: ±1 SE.
Figure 3
 
(a) Cumulative probability distributions for saccade-to-reach-peak velocity interval across viewing conditions illustrating the temporal relationship between the eye and hand movements during the execution stage of the reaching movement. Each curve represents mean data from one viewing condition (both eyes: black; fellow [dominant] eye: green; amblyopic [nondominant] eye: red) for visually normal participants (solid lines), participants with strabismic amblyopia (dashed lines) and participants with strabismus only (dotted lines). The cumulative probability distributions for participants with abnormal binocular vision were shifted toward intervals that were longer than those for control participants. (b) The mean saccade-to-reach peak velocity interval across viewing conditions. The interval was significantly longer in participants with abnormal binocular vision, regardless of viewing condition (P = 0.022). Error bars: ±1 SE.
Figure 4
 
Kinematics of reach-related secondary saccades across viewing conditions. The amplitude (a) and peak velocity (b) of reach-related secondary saccades in participants with strabismic amblyopia were significantly higher during amblyopic eye viewing than those in visually normal participants and participants with strabismus only (P < 0.05).
Figure 4
 
Kinematics of reach-related secondary saccades across viewing conditions. The amplitude (a) and peak velocity (b) of reach-related secondary saccades in participants with strabismic amblyopia were significantly higher during amblyopic eye viewing than those in visually normal participants and participants with strabismus only (P < 0.05).
Table.
 
Details of Eye-Hand Coordination During the Planning and Execution of Reaching for Participants With Amblyopia
Table.
 
Details of Eye-Hand Coordination During the Planning and Execution of Reaching for Participants With Amblyopia
Parameter Mild and Stereo+ (n = 5)* Mild and Stereo (n = 6)* Severe and Stereo (n = 5)
BE FE AE BE FE AE BE FE AE
Saccade-to-reach planning interval, ms 146 ± 105 132 ± 119 115 ± 76  172 ± 105 161 ± 77  171 ± 108 158 ± 65  154 ± 76  114 ± 111
Saccade-to-reach PV interval, ms 375 ± 76  367 ± 74  363 ± 112 400 ± 112 408 ± 116 409 ± 143 351 ± 125 348 ± 137 310 ± 145
Reach-related saccade kinematic
 Frequency, % 4.4 10.6* 6.5 10.5 19.9* 18.9* 6.7 10.2 11.0
 Amplitude, deg 1.00 ± 0.40 0.95 ± 0.17 1.07 ± 0.38  1.16 ± 0.33 1.15 ± 0.21 1.39 ± 0.27* 0.72 ± 0.26 0.62 ± 0.08 1.96 ± 0.36*
 Peak velocity, deg/s 94 ± 36 77 ± 14 89 ± 31 89 ± 23 91 ± 18 106 ± 17*  66 ± 27 55 ± 15 124 ± 24* 
Supplementary Table S1
×
×

This PDF is available to Subscribers Only

Sign in or purchase a subscription to access this content. ×

You must be signed into an individual account to use this feature.

×