eye movements, strabismus, amblyopia, and neuro … · 2011-08-04 · effects of anisometropic...

Effects of Anisometropic Amblyopia on VisuomotorBehavior, III: Temporal Eye-Hand Coordinationduring Reaching

Ewa Niechwiej-Szwedo,1 Herbert C. Goltz,1,2 Manokaraananthan Chandrakumar,1

Zahra Hirji,1 and Agnes M. F. Wong,1,2

PURPOSE. To examine the effects of anisometropic amblyopiaon the temporal pattern of eye-hand coordination during visu-ally-guided reaching.

METHODS. Eighteen patients with anisometropic amblyopia and18 control subjects were recruited. Participants executedreach-to-touch movements toward visual targets under threeviewing conditions: binocular, monocular amblyopic eye, andmonocular fellow eye viewing. Temporal coordination be-tween eye and hand movements was examined during reachplanning (interval between the initiation of saccade and reach-ing) and reach execution (interval between the initiation ofsaccade and reach peak velocity). The frequency and dynamicsof secondary saccades were also examined.

RESULTS. Patients with severe amblyopia spent a longer timeplanning the reaching response after fixating the target incomparison with control subjects and patients with mild am-blyopia (P � 0.029). In comparison with control subjects, allpatients extended the acceleration phase of the reach aftertarget fixation (P � 0.018). Secondary (reach-related) saccadeswere initiated during the acceleration phase of the reach andpatients executed these saccades with greater frequency thancontrol subjects (P � 0.0001). The amplitude and peak veloc-ity of reach-related saccades were higher when patientsviewed with the amblyopic eye in comparison with the otherviewing conditions (P � 0.001).

CONCLUSIONS. This is the first study to show that patients withanisometropic amblyopia modified the temporal dynamics ofeye-hand coordination during visually-guided reaching. Theyextended the planning and execution intervals after targetfixation and increased the frequency of secondary, reach-re-lated saccades. These may represent visuomotor strategies tocompensate for the spatiotemporal visual deficits to achievegood reaching accuracy and precision. (Invest Ophthalmol VisSci. 2011;52:5853–5861) DOI:10.1167/iovs.11-7314

Eye-hand coordination involves a complex interaction be-tween the visual, ocular, and manual motor systems. The

accuracy and precision of fine motor skills, such as reaching,grasping, and manipulating, depend on the ability to extractinformation from the environment and to coordinate the ap-propriate ocular and manual motor responses.1,2 Seeminglysimple actions consist of several submovements that are inte-grated optimally in space and time into seamless goal-directedbehavior.3 For example, to pick up a cup, vision is used todetect and localize the cup. Saccadic eye movements are thenexecuted to bring the image of the cup onto the fovea. Thereach movement is initiated while maintaining fixation on thecup.4 During the reaching movement, visual feedback is usedto monitor the reach trajectory and to update the motor com-mand when errors are detected.5–8

Spatiotemporal eye-hand coordination has been studied ex-tensively in visually-normal people (for review see Bekkeringand Sailer, 20024). Saccades typically precede hand movementby 50 to 100 ms during variety of manual tasks.9–12 Directingthe eyes to the target before initiation of hand movementallows the central nervous system (CNS) to obtain a high-resolution image of the target before the reach is initiated,which can facilitate programming of the reaching movement.In addition, when the eyes fixate on the target early during thereach trajectory (i.e., before the hand reaches peak velocity),visual feedback can be used to update the initial motor plan.Visual information can also be used during the decelerationphase in the latter part of the movement to fine tune the handtrajectory and to improve the performance (accuracy and pre-cision) of the reach.13 Indeed, Prablanc and colleagues re-ported that reaching performance improved substantiallywhen the hand movement was initiated at least 40 ms after theeyes fixated on the target.12 Taken together, these findingssuggest that the temporal delay between eye and hand move-ment initiation is not primarily a result of the smaller inertia ofthe eyeball than the arm, rather this delay serves to facilitatethe planning and execution of the reaching movement.

Amblyopia is a visual impairment of one eye caused byinadequate stimulation during early childhood that cannot becorrected by optical means.14 Despite extensive evidence ofspatiotemporal visual deficits in amblyopia,15–19 it is surprisingthat very few studies have examined how impaired spatiotem-poral vision in amblyopia affects motor functions such as visu-ally-guided eye and arm movements. Although the effects ofamblyopia on eye movements20–22 and some aspects of manualmotor control23–25 have been studied separately, the coordi-nation between the visual, ocular, and manual motor systemshas not been investigated previously in amblyopia.

We have previously reported that patients with anisome-tropic amblyopia had delayed saccade initiation when viewingwith the amblyopic eye in comparison with binocular or felloweye viewing and in comparison with control subjects.21 We

From the 1Department of Ophthalmology and Vision Sciences,The Hospital for Sick Children, Toronto, Ontario, Canada; and 2Uni-versity of Toronto, Toronto, Ontario, Canada.

Supported by Grants MOP 106663 from the Canadian Institutes ofHealth Research (CIHR), Leaders Opportunity Fund from the CanadianFoundation for Innovation (CFI), and the Department of Ophthalmol-ogy and Vision Sciences and Research Training Centre at The Hospitalfor Sick Children.

Submitted for publication February 1, 2011; revised March 18 andApril 17, 2011; accepted April 21, 2011.

Disclosure: E. Niechwiej-Szwedo, None; H.C. Goltz, None; M.Chandrakumar, None; Z. Hirji, None; A.M.F. Wong, None

Corresponding author: Agnes Wong, Department of Ophthalmol-ogy and Vision Sciences, The Hospital for Sick Children, 555 UniversityAvenue, Toronto, Ontario M5G 1X8, Canada; [email protected].

Eye Movements, Strabismus, Amblyopia, and Neuro-Ophthalmology

Investigative Ophthalmology & Visual Science, July 2011, Vol. 52, No. 8Copyright 2011 The Association for Research in Vision and Ophthalmology, Inc. 5853

also found that the manual reaction time and end-point perfor-mance (accuracy and precision) of the reach-to-touch move-ments in patients were comparable with control subjects in allviewing conditions. However, patients exhibited reduced peakacceleration and a prolonged acceleration phase during reach-ing.23 We postulated that patients with amblyopia optimizedtheir reaching performance by adopting different kinematicstrategies during planning (feedforward stage) and execution(feedback stage) of visually-guided reaching movements tocompensate for their degraded spatiotemporal vision. In ourprevious studies, we examined the dynamics of the saccadiceye movements21 and the kinematics of reaching movements23

separately. Because tight temporal coupling of eye and handmovements is important for optimal reaching performance, inthis article, we aimed to investigate further whether patientswith amblyopia adopt a different eye-hand temporal strategy tooptimize their performance. We examined the effects of aniso-metropic amblyopia on the temporal pattern of eye-hand co-ordination during the planning stage (defined as the intervalfrom target onset to the initiation of the reaching movement)and execution stage (defined as the interval from reach initia-tion to the end of movement) of visually-guided reach-to-touchmovements (referred to as reaching movements from hereonward). Specifically, we investigated whether patients spentlonger time planning the reaching movement and whetherthey extended the acceleration phase of the reach after theeyes fixated the target.

MATERIALS AND METHODS

Participants

Eighteen patients with anisometropic amblyopia were recruited (6males, age 26.4 � 10 years). The clinical details of all patients areshown in Table 1. All participants underwent a complete orthopticassessment by an unmasked certified orthoptist with 17 years clinicalexperience. The assessment included visual acuity testing using theSnellen chart (recorded as the last row in which a participant cancorrectly read all letters), measurement of eye alignment using theprism cover test, measurement of refractive errors, and stereoacuity

testing using the Titmus test. The fusion ability of patients who lackedstereopsis (negative Titmus test) was tested using the Worth four dottest and the Bagolini test. Anisometropic amblyopia was defined asamblyopia in the presence of a difference in refractive error betweenthe two eyes of �1 diopter (D) of spherical or cylindrical power.25–28

All patients had visual acuity between 20/30 and 5/400 in the amblyo-pic eye, 20/20 or better in the fellow eye, and an interocular acuitydifference �2 lines. Six patients were orthophoric and 12 had mono-fixation syndrome associated with their anisometropic amblyopia29;that is, they had a microtropia �8 prism diopters (as a result of a fovealscotoma arising from the anisometropia; it is not the cause of theamblyopia), inability to bifixate, and presence of fusional vergence.Twelve patients had mild amblyopia (amblyopic eye acuity 20/60 orbetter) and 6 had severe amblyopia (amblyopic eye acuity 20/100 orworse). Eighteen visually normal participants (7 males, age 30.7 � 11years) served as control subjects. They had normal or corrected-to-normal visual acuity of 20/20 or better in each eye, and stereoacuity�40 seconds of arc. Exclusion criteria were any ocular cause forreduced visual acuity, prior intraocular surgery, or any neurologicdisease. The study was approved by the Research Ethics Board at TheHospital for Sick Children and all protocols adhered to the guidelinesof the Declaration of Helsinki. Informed consent was obtained fromeach participant. The saccade data from 12 patients21 and the reachingdata of 13 patients23 have been reported separately in two previousreports. These two sets of data, however, have not been analyzedtogether previously to investigate the temporal relationship betweensaccades and reaching movements, which was the purpose of thepresent study.

Apparatus

Eye movements were recorded at 200 Hz using an infrared video-basedbinocular pupil/iris tracking system (Chronos Vision, Berlin, Ger-many). The system has a maximum resolution of 6 minutes of arc.Linearity is �0.5% for both horizontal and vertical eye movements,over a range of �20°. Before each experiment, a horizontal and verticalcalibration was performed for each eye using fixation targets at fivelocations: 0° and �10° horizontally and vertically.

Reach-to-touch movements of the upper right limb were recorded(Optotrak Certus 3020 system; Northern Digital, Waterloo, Canada), an

TABLE 1. Clinical Characteristics of Patients with Anisometropic Amblyopia

Patient Age (y)

Visual Acuity(Snellen Chart) Refractive Error

Stereoacuity(sec arc) Fusion AlignmentRE LE RE LE

1 33 20/15 20/30 �0.75 �2.00 140 NA Orthophoria2 29 20/50 20/15 �2.50 � 0.75 � 50 �0.25 3000 NA Monofixation RE3 17 20/20 20/40 pl �0.25 � 94 �1.00 � 1.00 � 92 80 NA Orthophoria4 14 20/50 20/15 �3.25 � 1.25 � 90 �2.00 50 NA Orthophoria5 18 20/15 20/40 Plano �2.00 � 0.25 � 130 60 NA Orthophoria6 20 20/15 20/50 Plano �1.50 120 NA Orthophoria7 35 20/15 20/60 �4.25 �0.75 3000 NA Monofixation LE8 36 20/15 20/400 �5.25 �12.00 Negative Suppress Monofixation LE9 25 20/40 20/15 �1.00 � 0.25 � 22 Plano 400 NA Monofixation RE

10 28 20/20 20/400 �4.00 �6.00 � 1.75 � 90 Negative Fused* Monofixation LE11 21 20/30 20/15 �1.50 Plano 3000 NA Monofixation RE12 20 5/400 20/20 �2.00 �3.00 � 0.75 � 15 Negative Fused† Monofixation RE13 19 20/20 20/40 �3.50 � 1.50 � 90 �3.50 � 2.50 � 102 200 NA Monofixation LE14 36 20/15 20/40 �1.50 �1.50 � 1.00 � 15 200 NA Monofixation LE15 56 20/100 20/20 �4.00 �2.25 Negative Fused* Monofixation RE16 16 20/200 20/15 none �2.75 Negative Fused* Monofixation RE17 25 20/50 20/20 �1.50 � 1.50 � 80 �3.00 � 2.50 � 80 120 NA Orthophoria18 26 20/100 20/15 �2.00 Plano 3000 NA Monofixation RE

LE, left eye; NA, not tested (Titmus stereo was positive); RE, right eye.* Fused using Worth 4-dot test.† Fused using Bagolini test.

5854 Niechwiej-Szwedo et al. IOVS, July 2011, Vol. 52, No. 8

infrared illumination-based motion capture system. This system is non-invasive and allows for precise 3-D motion tracking of the limb (spatialaccuracy 0.1 mm, resolution 0.01 mm, sampling frequency 200 Hz).The coordinate system was defined as follows: x-axis, horizontal plane;y-axis, vertical plane; z-axis, median plane. The system was calibratedbefore starting the experiment by using a four-marker digitizing probeto define the coordinate frame for the reaching movement. Twoinfrared markers (4 mm diameter) were affixed to the index fingertipand wrist joint of the participant’s right (dominant) hand. A 15-mmdiameter force-sensitive resistor (FSR; Tekscan, Boston, MA), wasplaced on the table at the participant’s midline 28 cm from thecomputer screen and 17 cm from the participant. The FSR was used totrigger the initiation of each trial and to control when the visual targetwas switched off during a trial.

Experimental Conditions and Procedure

The visual stimulus was a white circle (visual angle 0.25°) presented onblack background generated by a custom-written program (in MATLAB,version 7.6.0; The MathWorks, Natick, MA) and presented on a 20-inchcomputer screen (Diamond Pro 2070SB; resolution 1600 � 1200 at 85Hz; NEC-Mitsubishi, Itasca, IL) located 42 cm from the subject using avisual stimulus generator (ViSaGe; Cambridge Research Systems, Kent,UK). The distance from the starting position of the index finger to thecomputer screen was 43 cm in 3-D space. Testing was conducted in adimly lit room. The target was presented at four eccentricities: �5°or�10°, all along the horizontal axis at eye level and in random order.

Participants were seated at a table with their heads stabilized witha chin rest. There were three viewing conditions: binocular (BE),monocular amblyopic eye (AE), and monocular fellow eye (FE) view-ing, and data were collected in blocks. For control participants, view-ing was binocular, monocular left eye, and monocular right eye. Par-ticipants wore a black patch during monocular viewing. The order ofviewing conditions was randomized among the participants. At thestart of each trial, the right hand was placed on the table and the indexfinger was placed on the FSR. Participants fixated on a cross presentedat midline. After a variable delay (1.5 to 3 seconds), the target waspresented in the horizontal plane and participants were instructed tolook and touch the target located on the computer screen 28 cm (fromthe starting position of the hand) in front of the subject as fast and asaccurately as possible. On 50% of the trials, the target remained visiblethroughout the trial (target ON condition). On the remaining 50% ofthe trials, the target was switched off at the onset of hand movement,i.e., as soon as the finger was lifted off the FSR (target OFF condition).On these trials, participants were instructed to touch the locationwhere they had seen the target. The target ON and OFF conditionswere randomly interleaved.

Participants completed 10 trials in each combination of the exper-imental conditions for a total of 240 trials. The intertrial interval variedamong trials and it was at least 5 seconds. Practice trials were com-pleted before starting the experiment to familiarize the subjects withthe experimental procedure. We did not perform a separate test toascertain specifically how well each patient could see the target.However, all patients, including those with severe amblyopia, exe-cuted spatially and temporally appropriate eye and hand responsesduring practice trials, indicating that they were able to detect thetarget, although patients with severe amblyopia might not have seenthe target clearly.

Data Analysis

Eye position data were filtered using a second-order, dual-pass Butter-worth filter with a cutoff frequency of 50 Hz. Hand position data werealso filtered using a second-order dual-pass Butterworth filter with acutoff frequency of 7.5 Hz. Eye and hand velocity were obtained usinga two-point differentiation method. A custom-written program (inMatlab) was used to identify saccades using a velocity threshold of 20°per second, while the initiation of hand movement was defined aswhen the velocity of the finger y-coordinate (i.e., vertical axis) ex-

ceeded 30 mm per second. The end of the reaching movement wasdefined as when the finger reached the computer screen and thevelocity of the finger z-coordinate fell and stayed below 30 mm persecond. All trials were inspected visually to ensure that the saccadesand reaching movements were identified correctly by the program.

Temporal coordination between eye and hand movements wasexamined 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 reach movement). Typical trials illus-trating eye-hand coordination when reaching to a 10° target duringbinocular viewing for a control subject and two patients (one withmild and one with severe amblyopia) are shown in Figure 1. Eye-handcoordination during the planning stage of the reaching response wasassessed by calculating the time interval after the eyes fixated on thetarget (i.e., at the end of saccade) and the initiation of the reachingresponse (from here on, we will refer to this interval as the saccade-to-reach planning interval, as depicted by the red arrow in Fig. 1). Thesaccade-to-reach planning interval was calculated on a trial-by-trialbasis by subtracting saccade reaction time (latency) and saccade dura-tion from the reach reaction time (see Fig. 1). It reflects the time thatwas available for planning of the reaching response after the saccadehad been completed and the eyes were in the vicinity of the target.

The planning stage of the reaching response was also assessed byexamining the frequency of trials when the hand movement wasinitiated before the eye movement. The accuracy and precision werecompared between trials when reaching was initiated before or afterthe saccade.

FIGURE 1. Representative data showing the temporal relationship be-tween eye and hand movements on a typical trial during binocularviewing of a 10° target for (a) a control subject, (b) a patient with mildamblyopia, and (c) a patient with severe amblyopia. The eye tracingsrepresent the right eye of the control subject and the fellow eye ofpatients. The dotted gray vertical line depicts the time when theprimary saccade was completed, whereas the solid gray vertical linedepicts the time when the hand reached peak velocity. Saccade-to-reach planning interval (indicated by the red arrow) reflects theduration of time that was available for planning of the reaching re-sponse after the primary saccade had been completed and the eyeswere in the vicinity of the target. Saccade-to-reach-peak velocity inter-val (indicated by the blue arrow) reflects the duration of time after theeyes fixated the target during the early part of reach execution. Pa-tients were more likely to have extended planning and executionintervals after fixating the target in comparison with the controlsubjects.

IOVS, July 2011, Vol. 52, No. 8 Eye-Hand Coordination during Reaching in Amblyopia 5855

Eye-hand coordination during the execution stage of the reachingresponse was assessed by calculating the time interval between theend of the saccade and the hand reaching peak velocity (PV; from hereon, we will refer to this interval as the saccade-to-reach PV interval, asdepicted by the blue arrow in Fig. 1). Saccade-to-reach PV interval wascalculated on a trial-by-trial basis by subtracting saccade reaction timeand saccade duration from the time the hand reached PV (from targetonset; see Fig. 1). It reflects the duration of time after the eyes fixatedon the target during the early part of reach execution. Visual informa-tion acquired during this interval, which includes the accelerationphase of the reach, can be used to make compensatory adjustments tothe reach trajectory in the later part of the movement.30

Eye-hand coordination during the execution stage of the reachingresponse was also assessed by examining the frequency of secondarysaccades. In this article, secondary saccades which occurred during thereach and which occurred �250 ms after the primary saccades weredefined as reach-related saccades. We reasoned that these saccadeswere reach-related and were not secondary “corrective” saccades afterthe primary saccades under- or overshot because secondary “correc-tive” saccades typically occur with a latency of 100 to 250 ms.31–33 Theamplitude, peak velocity, and latency (with respect to the initiation ofthe reaching response) of the reach-related saccades were calculated.Secondary corrective saccades after primary saccades have been de-scribed in our previous report.21

Statistical Analysis

All continuous dependent variables (saccade-to-reach planning inter-val, saccade-to-reach PV interval, latency, amplitude, and peak velocityof reach-related saccades) were submitted to a repeated-measuresmixed ANOVA with group (three levels: control subjects, patients withmild amblyopia, patients with severe amblyopia) as a between-subjectsfactor and viewing condition (three levels: binocular, monocular fel-low eye, monocular amblyopic eye; for control subjects, binocular,monocular left eye, monocular right eye) as a within-subjects factor.

The frequency of reach-related saccades was compared betweenpatients and control subjects using Pearson’s �2 statistic. The effect ofviewing condition was then examined within each group using Pear-son’s �2 statistic.

All statistical analyses were performed using a statistical softwarepackage (SAS 9.2, Cary, NC). Descriptive statistics were reported as themean and corresponding SD. Any main effects and interactions wereanalyzed further using Tukey-Kramer post hoc tests to adjust for mul-tiple comparisons. The significance level was set at P � 0.05. Prelim-inary analysis showed that visual feedback of target had no significanteffect on any outcome measures, therefore, data with or without visualfeedback were collapsed for analysis and reporting.

RESULTS

Figure 1 shows representative eye and hand velocity tracingfrom a control subject, a patient with mild amblyopia, and apatient with severe amblyopia during binocular viewing of a10° target. The control subject showed a stereotypical patternof eye-hand coordination where the saccade was initiated�100 ms before reaching (Fig. 1a). In contrast, both patientsshowed longer saccade-to-reach planning intervals and longersaccade-to-reach PV intervals, which were more evident in thepatient with severe amblyopia (Fig. 1c) than the one with mildamblyopia (Fig. 1b).

Eye-Hand Temporal Coordination during thePlanning Stage of Reaching

There was a significant interaction between group and viewingcondition (F(4,66) � 2.88; P � 0.029) for mean saccade-to-reachplanning interval. As shown in Figure 2a, control subjectsinitiated reaching approximately 110 � 65 ms after the eyesfixated on the target, regardless of viewing condition. Post hoc

tests showed no significant difference for saccade-to-reachplanning intervals between control subjects and patients withmild amblyopia (binocular, 120 � 84 ms; fellow eye, 137 � 84ms; amblyopic eye, 102 � 91 ms). In contrast, patients withsevere amblyopia had longer saccade-to-reach planning inter-vals during all three viewing conditions (binocular, 197 � 43ms; fellow eye, 181 � 51 ms; amblyopic eye, 152 � 70 ms) incomparison with control subjects and patients with mild am-blyopia.

Figure 2b shows the cumulative frequency distributions ofsaccade-to-reach planning intervals for control subjects andpatients with mild and severe amblyopia for all viewing con-ditions. The saccade-to-reach planning interval was positivewhen the eyes fixated on the target prior to reach initiation andnegative when the eyes fixated on the target after reach initi-ation. As illustrated in Figure 2b, saccades were initiated priorto reaching in the majority of trials in control subjects (98.8%)and patients (96.7%; �(df 1) � 34.07; P � 0.0001). For control

FIGURE 2. (a) The saccade-to-reach planning interval across the threeviewing conditions in patients with mild and severe amblyopia, and innormal participants. The saccade-to-reach planning interval is relatedto the planning stage of the reaching response. It reflects the time thatwas available for planning of the reaching response after the saccadehad been completed and the eyes were in the vicinity of the target.Patients with severe amblyopia had a significantly longer saccade-to-reach planning interval in comparison with patients with mild ambly-opia, and with control subjects (P � 0.02). Error bars indicate �1 SE.(b) Cumulative frequency distributions for saccade-to-reach planninginterval illustrating the temporal relation between the eye and handmovements during the planning stage of the reaching movement. Anegative saccade-to-reach planning interval (left tail of the distribution)indicates that the reach was initiated before the saccade. Each curverepresents data from one viewing condition for control subjects, pa-tients with mild amblyopia, and patients with severe amblyopia.


subjects, there were no significant differences among viewingconditions (binocular, 98.5%; monocular left eye, 98.7%; mon-ocular right eye, 99.1%; �(df 2) � 1.45; P � 0.482). In contrast,a significant difference among viewing conditions was foundfor patients with mild amblyopia (�(df 2) � 56.79; P � 0.0001);they initiated saccades before reaching with reduced fre-quency when viewing with the amblyopic eye (93.4%), incomparison with binocular (97.3%) and fellow eye viewing(98.9%). Similarly, patients with severe amblyopia initiatedsaccades before reaching with reduced frequency when view-ing with the amblyopic eye (97.5%), compared with binocular(99.9%) and fellow eye viewing (99.8%; �(df 2) � 15.31; P �0.001).

Because patients initiated saccades before reaching on areduced number of trials when viewing with the amblyopiceye, that is, they initiated reaching before saccades more oftenthan usual, we examined whether this reverse eye-hand tem-poral coupling affected end-point accuracy or precision ofreaching. Regardless of severity level, performance in patientswas comparable whether saccades were initiated before orafter the reaching movement. For patients with mild amblyo-pia, there was no difference in performance when saccadeswere initiated before (accuracy 0.29 � 4.29 mm; precision3.73 � 1.93 mm) or after (accuracy 0.28 � 4.89 mm; precision3.65 � 2.88 mm) the reach. Similarly, for patients with severeamblyopia, there was again no difference in performance whensaccades were initiated before (accuracy �1.59 � 11.09 mm;precision 4.97 � 5.68 mm) or after the reach (accuracy 3.03 �4.82 mm; precision 5.61 � 4.08 mm).

Eye-Hand Temporal Coordination during theExecution Stage of Reaching

Saccade-to-Reach PV Interval. Cumulative frequency dis-tributions of the saccade-to-reach PV intervals for control sub-jects and patients with mild and severe amblyopia were plottedfor all viewing conditions in Figure 3a. The frequency distribu-tions for both groups of patients were shifted toward longerintervals in all viewing conditions in comparison with controlsubjects, suggesting that patients extended the accelerationphase of the reach once the eyes fixated on the target duringthe execution stage. There was a significant interaction be-tween group and viewing condition (F(4,66) � 3.21; P �0.018). As shown in Figure 3b, control subjects had compara-ble saccade-to-reach PV intervals in all viewing conditions(binocular, 306 � 114 ms; right eye, 314 � 105 ms; left eye,300 � 101 ms). In comparison with control subjects andregardless of severity level, patients had significantly longersaccade-to-reach PV intervals when viewing with the amblyo-pic eye (mild amblyopia, 359 � 127 ms; severe amblyopia,363 � 61 ms) and when viewing with the fellow eye (mildamblyopia, 386 � 111 ms; severe amblyopia, 388 � 51 ms).Post hoc tests showed that during binocular viewing pa-tients with severe amblyopia (409 � 44 ms) had significantlylonger saccade-to-reach PV in comparison with patients withmild amblyopia (344 � 104 ms) and control subjects (306 �114 ms).

Frequency of Reach-Related Saccades. The frequency ofreach-related saccades was significantly greater in patients(mild amblyopia, 14.1%; severe amblyopia, 21.8%) than incontrol subjects (11.8%) (�2

(df 2) � 85.14; P � 0.0001). Asshown in Figure 4a, control subjects executed reach-relatedsaccades with greater frequency when viewing monocularly(right eye, 13.2%; left eye, 13.6%) in comparison with binocularviewing (8.6%; �2

(df 2) � 21.09; P � 0.0001). In contrast, patientswith amblyopia executed reach-related saccades with comparablefrequency across all three viewing conditions. In patients withmild amblyopia, the frequency was 14.6% during binocular view-

ing, 13.7% during fellow eye viewing, and 13.8% during amblyo-pic eye (�2

(df 2) � 0.31; P � 0.854). Similarly, in patients withsevere amblyopia, the frequency was 20.2% during binocularviewing, 23.7% during fellow eye viewing, and 21.6% duringamblyopic eye viewing (�2

(df 2) � 1.69; P � 0.423).Latency of Reach-Related Saccades. There was a signifi-

cant interaction between group and viewing condition for thelatency of reach-related saccades (F(4,62) � 4.62; P � 0.003;Fig. 4b). For control subjects, the latency was not differentbetween viewing conditions (binocular, 146 � 59 ms; righteye, 158 � 52 ms; left eye, 155 � 59 ms). For patients withmild amblyopia, the reach-related saccade latencies were lon-ger in comparison with control subjects but not differentbetween viewing conditions (binocular, 184 � 74 ms; felloweye, 201 � 45 ms; amblyopic eye, 207 � 71 ms). In contrast,patients with severe amblyopia had significantly longer reach-related saccade latencies when viewing with the amblyopiceye (252 � 124 ms) in comparison with binocular viewing(113 � 22 ms) and fellow eye viewing (129 � 48 ms).

FIGURE 3. (a) Cumulative frequency distributions for saccade-to-reach-peak velocity interval by viewing eye condition illustrating thetemporal relation between the eye and hand movements during theexecution stage of the reaching movement. Each curve represents datafrom one viewing condition for control subjects, patients with mildamblyopia, and patients with severe amblyopia. The frequency distri-butions were shifted toward longer intervals for patients with mild andsevere amblyopia compared with control subjects. (b) Mean saccade-to-reach peak velocity intervals were significantly longer for patientswith mild and severe amblyopia in comparison with control subjects inall viewing conditions. During binocular viewing patients with severeamblyopia also had significantly longer saccade-to-reach PV intervals incomparison with patients with mild amblyopia (P � 0.018). Error barsindicate �1 SE.


Amplitude of Reach-Related Saccades. The interactionbetween group and viewing condition was significant for am-plitude (Fig. 4c) of reach-related saccades (F(4,62) � 9.04; P �0.0001). For control subjects, amplitude was not differentbetween viewing conditions (binocular, 0.90° � 0.28°; righteye, 0.98° � 0.39°; left eye, 1.00° � 0.41°). Patients with mildamblyopia had comparable amplitudes during binocular view-ing (0.90° � 0.28°), fellow eye viewing (0.85° � 0.33°), andamblyopic eye viewing (1.09° � 0.37°). Patients with severeamblyopia had higher reach-related saccade amplitudes duringamblyopic eye viewing (1.49° � 0.28°) in comparison withviewing with the fellow eye (0.68° � 0.31°) or binocularly(0.79° � 0.16°).

Peak Velocity of Reach-Related Saccades. The interac-tion between group and viewing condition was also significantfor peak velocity (Fig. 4d) of reach-related saccades (F(4,62) �6.53; P � 0.001). For control subjects, peak velocity was notdifferent between viewing conditions (binocular, 70° � 19°per second; right eye, 73° � 19° per second; left eye, 76° �28° per second). Patients with mild amblyopia had comparablepeak velocities during binocular viewing (76° � 25° per sec-ond) and during fellow eye viewing (73° � 27° per second).Post hoc testing indicated that peak velocity was higher duringamblyopic eye viewing (87° � 21° per second) in comparisonwith the other viewing conditions and with control subjects.

Patients with severe amblyopia also had higher peak velocitiesduring amblyopic eye viewing (97° � 24° per second). How-ever, peak velocities were lower during fellow eye (58° � 20°per second) and binocular (59° � 15° per second) viewing.

DISCUSSION

This study examined the effects of impaired spatiotemporalvision on the temporal pattern of eye-hand coordination duringthe planning and execution stages of visually-guided reachingmovements in patients with mild and severe anisometropicamblyopia. The major findings are: (1) patients with severeamblyopia spent a longer time planning the reach after the eyesfixated on the target before they initiated the hand movement;(2) all patients extended the acceleration phase of the reachingmovement after the eyes fixated on the target; (3) patientsexecuted reach-related saccades with greater frequency; and(4) the reach-related saccades in patients had longer latency,higher amplitude, and higher peak velocity during amblyopiceye viewing.

Eye-Hand Coordination during the Planning Stageof ReachingDirecting the fovea of the eyes to the target before reachinitiation allows the use of high-resolution visual feedback to

FIGURE 4. Mean metrics of reach-related saccades. (a) Patients initiated reach-related saccades more frequently in comparison with controlsubjects. (b) Patients with mild amblyopia had longer reach-related saccade latencies of in all viewing conditions in comparison with controlsubjects. For patients with severe amblyopia, the reach-related saccade latencies were longer during amblyopic eye viewing in comparison withbinocular and fellow eye viewing (P � 0.003). (c) Patients with mild and severe amblyopia had higher reach-related saccade amplitudes duringamblyopic eye viewing in comparison with other viewing conditions (P � 0.0001). (d) Patients with mild and severe amblyopia had higherreach-related saccade peak velocities during amblyopic eye viewing in comparison with other viewing conditions (P � 0.001).


plan the reaching response before the limb movement begins.Indeed, visually normal participants typically move their eyesto the target before initiating hand movement even duringexperiments when they are not specifically instructed to movetheir eyes.10,11 In addition, the central nervous system may alsouse extraretinal eye position signals (i.e., efference copy orproprioception) generated by the orienting saccades to updatethe early motor plan to improve reach performance.4,34

Regardless of viewing condition, control subjects in ourstudy initiated reaching approximately 110 ms after the eyesfixated on the target. In contrast, patients with severe ambly-opia spent a significantly longer time planning the reachingmovement after fixating on the target before the hand move-ment was initiated, regardless of viewing condition. Patientsmay have extended the planning interval to compensate fortheir poor acuity during amblyopic eye viewing to improvereaching performance. Interestingly, the extended planninginterval was also evident during fellow eye and binocularviewing. This finding might be surprising at first glance be-cause the fellow eye had acuity of at least 20/20, and becausebinocular acuity in 10 patients was comparable with fellow eyeacuity (we did not collect binocular acuity in the other 8patients because this was not part of our original protocol).However, despite normal acuity, deficits in the fellow eye havebeen well-documented in people with amblyopia, includingsecond-order spatial loss,35,36 impaired motion processing,37,38

deficient contour integration,39,40 and impaired perception ofimages of natural scenes.41 It has been hypothesized that thesehigher-order deficits exist because second-order neurons arebinocular and they require normal binocular input during de-velopment. Thus, anomalous binocular vision during early de-velopment leads to higher-order cortical deficits, which can bedetected during monocular viewing with either the amblyopicor fellow eye. This hypothesis is supported by anatomic andneurophysiologic studies which showed that early-onset mon-ocular deprivation leads to a reduced proportion of function-ally binocular neurons in primary visual cortex42–44 and extra-striate cortex.45 In addition, suppression of the fellow eye bythe amblyopic eye has been documented in cats,46,47 mon-keys,42 and in humans.48 Furthermore, binocular suppressionis also evident in monkeys42 and humans,48 suggesting thatwhile amblyopia disrupts predominantly the excitatory inter-actions between the two eyes, cortical inhibitory binocularconnections are less susceptible to abnormal visual experi-ence. Our results thus provide additional support to the grow-ing body of evidence that abnormal visual processing35–38,41,49

and altered motor behavior23 are also present during felloweye and binocular viewing in patients.

Patients with mild amblyopia and control subjects had com-parable reach planning intervals after fixating on the target. Inagreement with previous studies,12,50,51 control subjects initi-ated saccades before reaching on � 98% of trials. In contrast,patients with mild or severe amblyopia initiated reaching be-fore saccades on significantly more trials when viewing withthe amblyopic eye. More importantly, despite this reversal ineye-hand coupling in patients, reaching accuracy and precisionwere comparable between trials when saccades were initiatedprior to the reach and those when saccades were initiated afterthe reach. Three explanations are possible. One possibility fora lack of difference in reaching performance between thesetwo types of trials may be due to the relatively small number oftrials in which reaching was initiated before saccades. Anotherpossibility is that our subjects did not have to extract any finedetails from the visual target when they performed our rela-tively simple motor task. It remains to be seen whether pa-tients would show altered eye-hand coupling in more difficultvisuomotor tasks. A third, and more likely, possibility is thatgood spatial reaching performance was achieved due to the

substantial difference between saccade and reaching duration.In this study, the mean saccade duration was approximately 40ms, whereas the mean reaching duration was approximately550 ms for control subjects and approximately 650 ms forpatients. This substantial difference between saccade andreaching duration meant that the eyes were able to fixate onthe target well in advance of the hand reaching the target.Thus, both patients and control subjects had enough time toupdate the target’s location by using retinal and/or extraretinalfeedback to adjust the hand approach trajectory and to modifythe landing position of the hand. The ample time allowed themto achieve good reaching accuracy and precision, even in trialswhen the hand movement was initiated before the saccade.

Eye-Hand Coordination during the ExecutionStage of Reaching

Tight coupling between saccades and early kinematic markersof the reaching response has been reported by Helsen andcolleagues.10 They found a strong positive correlation betweenthe time when the eyes fixated on the target and the time whenthe hand reached peak velocity. They suggested that this tem-poral sequence might facilitate optimal extraction of visualinformation for guiding movement. When the eyes fixate onthe target at a time when the hand is in the early phase ofmovement, high-resolution visual feedback of the target can beacquired to update the reach plan and used to make compen-satory adjustments to the hand reach trajectory in the finalapproach phase. Indeed, Helsen and colleagues50 showed thatthe tight eye-hand temporal coupling might be responsible forreducing the spatial variability of the hand trajectory in theinterval between peak velocity and the end of the primarysubmovement (i.e., before the corrective movement began) bya factor of five. We have previously shown that patients extendthe acceleration phase of the reaching movement23; in thisstudy, we examined specifically whether the extended accel-eration phase is related to the time of target fixation.

Consistent with the results in our previous study with asmaller sample size,23 we found that the duration of accelera-tion phase after target fixation was extended in both patientgroups and under all viewing conditions in comparison withcontrol subjects. Despite a considerable difference in visualacuity between patients with mild (range 20/30 to 20/60) andthose with severe amblyopia (acuity 20/100 or worse), wefound that the duration of acceleration phase was extendedcomparably in all patients after fixating on the target duringmonocular fellow eye and amblyopic eye viewing.

In contrast, the duration of the acceleration phase aftertarget fixation was affected differentially by the severity ofamblyopia during binocular viewing. Specifically, the acceler-ation interval after target fixation was shorter in patients withmild amblyopia (but still longer than in control subjects) com-pared with patients with severe amblyopia. One possible ex-planation is that binocular vision provides important informa-tion for both movement planning and online control,52–55 andthat even residual binocularity may provide some advantageduring the execution of reaching movements. In this study, allpatients with mild amblyopia had residual stereopsis, whereasthe majority of patients (five out of six) with severe amblyopiahad no stereopsis. The reduced acceleration interval in patientswith mild amblyopia might be due to their ability to useresidual binocular information to program a more precise ini-tial motor plan or to make online compensatory adjustmentsduring the reaching movement.

Reach-Related Saccades

Primary saccades to visual targets usually undershoot the tar-get’s location by approximately 10%.31 Numerous studies have


documented that primary saccades are usually followed bysecondary corrective saccades with a latency of 100 to 250ms.32,33,56 In the present study, we examined secondary sac-cades that occurred after the onset of the reaching movement(which we defined as reach-related saccades) and that werenot temporally associated with primary saccades (i.e., latency�250 ms after the primary saccade). We reasoned that thefunction of secondary saccades initiated during reach execu-tion is to facilitate the online control of the reaching response.To the best of our knowledge, reach-related saccades have notbeen reported previously even in visually-normal individuals.Our study is the first to show that visually-normal people madereach-related saccades more frequently when viewing monoc-ularly compared with binocular viewing, indicating that binoc-ular vision provides important input for programming andexecution of reaching movements.57,58

The frequency of reach-related saccades was greater inpatients with amblyopia and did not differ among viewingconditions. Overall, patients with severe amblyopia initiatedreach-related saccades most frequently, while patients withmild amblyopia had frequency of reach-related saccades com-parable with control subjects when control subjects viewedmonocularly. Although we found some differences betweenpatients and controls for the latency of reach-related saccades,these saccades were initiated during the acceleration phase ofthe reaching movement on the majority of trials. Because visualinformation acquired early in the trajectory can be used tomake compensatory adjustments later in the trajectory, thereach-related saccades that were executed relatively early dur-ing the reaching movement may play a functional role infacilitating reaching performance. The frequency pattern andthe latency of reach-related saccades suggest that they might bean adaptive strategy and/or compensation that patients devel-oped to maintain good reaching accuracy and precision in faceof their spatiotemporal visual deficits.

Although patients had a similar frequency of reach-relatedsaccades across viewing conditions, the peak velocity of thesereach-related saccades were higher during amblyopic eye view-ing in comparison with the other viewing conditions and withcontrol subjects. In addition, patients with severe amblyopiahad higher amplitude and peak velocity of reach-related sac-cades during amblyopic eye viewing (but not during binocularor fellow eye viewing) in comparison with patients with mildamblyopia. These results suggest that reach-related saccadesare most likely initiated based on a retinal error signal, whichmay be impaired due to visual positional uncertainty whenpatients viewed with the amblyopic eye.59,60 During amblyo-pic eye viewing, patients with severe acuity impairment mighthave less reliable retinal position error signals of the target/hand image such that the visual error must be larger to bedetected and before a reach-related saccade is initiated. This, inturn, leads to higher amplitude and peak velocity of reach-related saccades when viewing with the amblyopic eye.

In conclusion, we demonstrated that patients with aniso-metropic amblyopia modified the temporal dynamics of eye-hand coordination during visually-guided reaching and that theseverity of amblyopia affected the strategies that patients used.Patients with severe amblyopia extended the planning stagebefore reach initiation after the target was acquired by theprimary saccade. All patients extended the acceleration phaseof the reaching movement after the eyes fixated on the targetand executed more reach-related saccades during the acceler-ation phase of the reach, irrespective of their level of visualacuity. We propose that the extended planning and executionintervals after target fixation and the additional reach-relatedsaccades are strategies that patients developed to compensatefor their spatiotemporal visual deficits, allowing them to

achieve good accuracy and precision during visually-guidedreaching.

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