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Motor Control, 2013, 17, 95-104 © 2013 Human Kinetics, Inc.

Official Journal of ISMCwww.MC-Journal.com

RESEARCH NOTE

Hansen is with Nipissing University, North Bay, Ontario, Canada. Hayes and Bennett are with the Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, UK.

Integration of Alternating Monocular Samples During Goal-Directed Aiming

Steve Hansen, Spencer J. Hayes and Simon J. Bennett

The current study examined the effect of interocular delay in a manual aiming task that required accurate end-point placement, but not precise control of a grip aper-ture. Participants aimed in binocular, monocular, or alternating monocular vision conditions. For the latter, 25ms monocular samples were provided to alternate eyes without delay (0ms), or a delay of 25 or 50ms. The interocular delay resulted in a longer movement time, caused by a longer time-to-peak and time-after-peak velocity, and a reduction in peak velocity. We suggest that the change in kinematics reflect a strategic response to preserve terminal aiming accuracy and variability when faced with an informational perturbation. These findings indicate that the response to the interocular delay between alternating monocular samples depends on the task-specific information used to control that behavior.

Keywords: monocular, alternating, binocular, integration, aiming

Individuals can, within certain temporal limits, integrate binocular or mon-ocular visual samples (intraocular) such that they maintain normal performance (i.e., outcome accuracy and/or movement kinematics) in tasks such as locomotion (Assaiante, Marchand, & Amblard, 1989), one-handed ball catching (Bennett, Ashford, & Elliott, 2003), prehension (Bennett, Elliott, Weeks, & Keil, 2003), as well as serial (Elliott, Chua, & Pollock, 1994) and discrete aiming (Elliott, Pol-lock, Lyons, & Chua, 1995). However, it has recently been shown that participants experience far more difficulty integrating monocular samples provided alternately to each eye (i.e., interocular). For instance, while one-handed ball catching can be performed equally well with binocular or monocular vision (Olivier, Weeks, Lyons, Ricker, & Elliott, 1998; Bennett, Ashford, et al., 2003), the capacity to gather useful visual information from alternating monocular samples deteriorates when there is an interocular occlusion as short as 20 ms (Bennett, Ashford, Rioja, Coull, & Elliott, 2006). When reaching to grasp a static target, a change in movement kinematics is exhibited even when alternating monocular samples are received without delay. This effect is evident irrespective of the duration of the monocular sample (50 ms in Wilson, Pearson, Matheson, & Marotta, 2008; 25 ms in Hansen, Hayes, & Ben-nett, 2011), and has been associated with an impaired ability to integrate alternating images (i.e., alternating vision could prevent a binocular percept).

96 Hansen, Hayes and Bennett

To date, interocular integration of monocular samples for the purpose of visuo-motor control has been investigated using prehensile-type tasks that demand precise control of grip aperture as the hand approaches either a static (Wilson et al., 2008; Hansen et al., 2011) or moving target (Bennett et al., 2006; Olivier et al., 1998). Such tasks are typically reliant on binocular disparity as a source of information regarding the changing relationship between the target and the fingers and thumb of the grasping hand (Bennett, Van der Kamp, Savelsbergh, & Davids, 2000; Melmoth & Grant, 2006). Indeed, having brought the hand near the target, fine binocular disparity contributes to the precise control of two effectors (or one grip aperture) relative to two target locations on the object to be grasped (Melmoth, Storoni, Todd, Finlay, & Grant, 2007). The purpose of the current study was to further examine integration of alternating monocular samples during the execu-tion of a manual aiming task that did not require the control of a grip aperture, but still required perception of target and effector location in depth (i.e., static and dynamic). By removing the need to perform a precision grasp, we sought to deter-mine if the task-specific sources of information useful for the control of manual aiming movements have a general intolerance to interocular delays similar to that exhibited in prehensile-type actions (Hansen et al., 2011; Wilson et al., 2008). To this end, participants completed aiming movements on a digitizing tablet to targets located at three distances under binocular vision, monocular vision, and three alternating monocular conditions that differed with respect to the interocular delay. Given the two-dimensional nature of the aiming task, similar terminal accu-racy and movement kinematics were expected in binocular and monocular vision conditions; for a comparison between visuo-motor control of two-dimensional and three-dimensional aiming see Coull, Weir, Tremblay, Weeks, & Elliott (2000). In alternating monocular conditions, it was anticipated that a perturbation to perception of depth-related information would influence movement kinematics associated with planning and/or online control (for a review of the on-line control of goal-directed action see Elliott, Hansen, Grierson, Lyons, Bennett, & Hayes; 2010). Moreover, these adaptations would lead to an overall increase in movement time, but would preserve measures of terminal accuracy.

Materials and Methods

Participants

Twelve undergraduate students from the host University were recruited to partici-pate. All participants had normal vision, or had corrected to normal vision, and were right hand dominant. No financial or academic compensation was provided. Informed consent was acquired before completion and all procedures were approved by the local ethical guidelines and conducted in accordance with the 1964 declara-tion of Helsinki.

Apparatus

Liquid crystal goggles (translucent technologies) were worn throughout testing. The state of the goggles (i.e., opaque, transparent) was controlled by TTL input from a slave pc (Dell Precision 380), linked to a master pc (Dell Dimension 4600) that

Integration of Alternating Monocular Samples 97

also controlled the timing of stimulus presentation. Both pc’s were running Win-dows XP operating system, and were interfaced to each other using custom-written routines in Matlab (R14, Mathworks Inc). Aiming movements were recorded on the master pc when a hand-held mouse was moved on a Wacom Intuos digitizing tablet (A3 Wide). Samples of position data in the x and y axes were recorded at 200 Hz and then converted to an 85 Hz digital signal by extracting the cumulative displacement between each screen refresh. The accuracy of the tablet was 0.5 mm, and the aspect ratio was set such that 1 mm movement of the mouse corresponded to 1 mm movement of a cursor shown on the display of the master pc.

Participants sat on a custom-modified barber chair, with an incorporated chin rest that kept the head in a stable position, at a distance of 600mm (horizontal and vertical) from the lead edge of the master pc monitor (21-inch CRT, Iiyama Pro Master 513). The monitor was mounted in a wooden frame such that the screen was facing the ceiling, at a height of 650mm from the floor. The digitizing tablet was placed on a table beside the barber chair, and oriented such that movement of the mouse was parallel to the cursor movement on the master pc monitor. A material screen with an incorporated sleeve was placed between the barber chair and table, thus preventing vision of the participant’s right arm, digitizing tablet and mouse.

Task and Procedure

The task was to move a cursor as quickly and as accurately as possible from a home position into the center of a target and then click the right mouse button. The requirement to mouse click upon termination of the aiming movement increased the complexity of the task relative to aiming tasks that are completed when the cursor passes through the target (e.g., Bennett & Davids, 1998), or lands on the target (e.g., Hansen, Tremblay & Elliott, 2008). However, since the goal of the task was to complete an aiming movement with a single effector it was substantially different from prehensile-type actions that require two effectors (finger and thumb) to be precisely located at two target locations on the object to be grasped. In this respect, the current aiming task closely resembled other goal-directed actions where an indi-vidual has to reach-out and push a button (e.g., pushing a button on the radio or in an elevator). The home position was a red circle (10 mm diameter) located coincident with the midline of the participant and approximately 300 mm horizontally from their torso. A white circle (5 mm diameter) represented the position of the mouse cursor on the screen. A red unfilled circle (10 mm diameter) represented the target, and was presented at one of three distances from the home position (near = 250, mid = 300, far = 350 mm). Each trial began with the goggles in the binocular state. The participant first had to place the cursor in the home position, after which the goggles entered a no-vision opaque state. Participants then self-initiated the trial by clicking the left mouse button, after which the goggles entered their relevant visual state for that particular trial. There were five visual conditions: binocular, monocular (right eye only), and alternating monocular samples (25 ms) provided to the right and then left eye with 0, 25 or 50 ms interocular delay. In the alternating monocular conditions, both of the goggles lenses were in the opaque state for the duration of the interocular delay. Therefore, one cycle in the alternating monocular conditions consisted of a right eye sample (25 ms), a no-vision interocular delay (0, 25, or 50 ms), a left eye sample (25 ms), and then another no-vision interocular

98 Hansen, Hayes and Bennett

delay. Once the goggles began cycling, the participants moved the cursor toward and into the target circle as quickly and as accurately as possible. The trial was terminated when the participants clicked the right mouse button. After each trial, the goggles returned to the binocular state and participants moved the cursor back to the home position in readiness for the subsequent trial. All stimuli were presented on a black background.

Upon entering the laboratory, participants completed the Titmus test of static stereoscopic vision (Coutant, 1993), that showed that they had normal levels with the majority of participants had a stereoacuity of at least 60 arcsec. Nb. one participant had a stereoacuity of 120 arcsec. Next, participants were given a familiarization that consisted of 5 trials to each of the 3 target locations under binocular vision. They then completed the experimental protocol. This was arranged into 5 blocks, each block comprising 10 trials to each of the 3 target locations (N = 150 trials). Vision condition was constant within a block (see Wilson et al. 2008), thus ensuring that participants did not plan for the worse-case scenario (i.e., the most perturbed visual condition), and also permitting a less biased examination of adaptation effects (i.e., trials 1–5 vs. trials 6–10 per combination of independent variables). Blocks were pseudo-randomized such that all vision conditions were received in a different order between participants. Presentation of target location was fully randomized.

Data Analysis and Reduction

The two-dimensional position data were filtered using a zero-phase digital filter with low pass cut-off of 20 Hz, and then differentiated using a central difference algorithm to obtain a velocity profile. A custom-written MATLAB routine extracted the following dependent measures from the primary movement (y) axis: Movement time—the time between velocity exceeding 0.4 m/s and the participant clicking the right mouse button (i.e., movement end); peak velocity; time-to-peak velocity, and time-after-peak velocity. Constant error and variable error of position of the mouse cursor relative to the center of the target circle in both the primary and secondary axis of movement were also calculated. Constant error was defined as the distance between the center of the target and the center of the cursor at the movement end-point. Negative constant error values indicate endpoint locations that were to the left and/or target undershoots. Variable error was defined as the standard deviation of the endpoint locations around the average constant error. Intraparticipant means of each dependent measure were calculated and submitted to separate 5-vision condition (binocular, monocular, alternating 0ms delay, alternating 25ms delay, alternating 50ms delay) by 2-block (trials 1–5, trials 6–10) by 3-target distance (250, 300, 350 mm) repeated-measures ANOVA. Main effects and significant interactions were investigated using Tukey’s HSD with alpha set at p < .05. For the purpose of brevity, only significant effects are reported.

Results

Movement Accuracy

Main effects of target distance were indicated for constant error in the primary axis, (F(2, 22) = 42.63, p < .001), whereas for variable error there were main effects

Integration of Alternating Monocular Samples 99

of target distance in both the primary, (F(2, 22) =17.08, p < .001), and secondary axis of movement, (F(2, 22) =13.94, p < .001). Participants exhibited significantly greater undershoot of the target in the near (-4.3 mm) than in the middle (-1.3 mm), or far target conditions (-0.4 mm). Participants were significantly less variable in the primary axis as the target distance increased (near = 4.6 mm; middle = 3.5 mm; far =2.4 mm). Similarly, participants were less variable in the secondary axis when aiming to the far (1.7 mm) than the near (2.9 mm) or middle (2.7 mm) targets. The analysis also revealed a significant three-way interaction of vision condition, block, and target distance for variable error in the secondary axis of movement (F(8,88) =2.34, p < .026). However, post hoc analysis failed to reveal significant differences for relevant comparisons (e.g., increases or decreases in consistency within block at a single target distance under a single vision condition, or at a single target distance under multiple vision conditions).

Movement Kinematics

Main effects of vision condition, (F(4,44) = 25.13, p < .001), and target distance, (F(2,22) = 132.23, p < .001), were identified for movement time. Participants completed their movements in a similar amount of time in the binocular (1190 ms), monocular (1272 ms), and alternating vision without delay conditions (1274 ms). However, participants spent significantly longer completing their movements in alternating monocular vision with a 25 ms delay (1422 ms), as well as with a 50 ms interocular delay (1538 ms; see Table 1). As expected, movement time was lengthened for each increase in target distance (near = 1153 ms, middle = 1318 ms, far = 1547 ms).

Table 1 Group Means (Standard Error of the Mean) for the Dependent Measures as a Function of Vision Condition

Binocular Monocular Alt-0ms Alt-25ms Alt-50ms

Constant Error

Primary Axis (mm)

-1.9 (0.4) -1.6 (0.4) -1.4 (0.4) -2.7 (0.4) -2.4 (0.4)

Constant Error

Secondary Axis (mm)

0.4 (0.2) 0.5 (0.2) 0.5 (0.2) 0.1 (0.2) 0.2 (0.2)

Variable Error

Primary Axis (mm)

3.0 (0.3) 3.1 (0.4) 3.6 (0.5) 3.4 (0.4) 4.2 (0.7)

Variable Error

Secondary Axis (mm)

2.7 (0.4) 2.2 (0.2) 2.2 (0.3) 2.2 (0.3) 2.8 (0.3)

Movement Time (ms) 1190 (44) 1271(44) 1273 (41) 1422 (42) 1537 (38)

Time-To Peak

Velocity (ms)

812 (38) 892 (38) 884 (35) 1030 (37) 1114 (34)

Time-After Peak

Velocity (ms)

378 (12) 379 (11) 389 (12) 391 (11) 424 (12)

Peak Velocity (mm/s) 469 (22) 456 (23) 450 (23) 412 (25) 385 (24)

100 Hansen, Hayes and Bennett

Analysis of time-to-peak velocity revealed main effects of vision condition, (F(4,44) = 23.26, p < .001), and target distance, (F(2,22) = 100.49, p < .001). Time-to-peak velocity was similar in the binocular, monocular, and alternating monocular without delay conditions, and was significantly shorter than in alternating monocular conditions with an interocular delay. Time-to-peak velocity lengthened significantly for each increase in target distance (near = 772 ms, middle = 926 ms, far = 1142 ms). Analysis of time-after-peak velocity revealed main effects of vision condition, (F(4, 44) = 4.12, p < .007), and target distance, (F(2, 22) = 7.98, p < .003). Participants spent significantly longer in the final portion of their move-ments when there was a 50 ms interocular delay than in the binocular or monocular conditions (see Table 1). They also spent more time in the final portion of their movement when moving to the far target (405 ms) than the near target (380 ms). Time-after-peak velocity when moving to the mid target was intermediate (392 ms) between the other two locations.

For peak velocity, there was a main effect of vision condition, (F(4,44) = 14.44, p < .001), and target distance, (F(2,22) = 44.33, p < .001), as well as an interaction between these factors, (F(8,88) = 3.36, p < .002; see Figure 1). Peak velocity was similar in binocular, monocular and alternating monocular without delay condi-tions, and was significantly higher than in alternating conditions with 25 ms or 50 ms interocular delay (see Table 1). With the exception of the alternating condition

Figure 1 — Group Average Peak Velocity (mm/s) as a Function of Visual Condition and Target Distance. Error Bars Represent Standard Error.

Integration of Alternating Monocular Samples 101

with a 50 ms interocular delay, peak velocity was lower when moving to the near target than far target. The introduction of a 50 ms interocular delay resulted in no scaling of peak velocity to target distance, as well as a lower peak velocity com-pared with all other conditions.

DiscussionThe results of the current study are consistent with those on prehensile actions (Hansen et al., 2011; Wilson et al., 2008) in showing that participants modified their movement kinematics following the introduction of an interocular delay (25 ms) between alternating monocular samples. Specifically, peak velocity was reduced and time-to-peak velocity was lengthened, thereby contributing to an increase in time to complete the aiming movement. A further significant change in movement kinematics was observed when the interocular delay was lengthened to 50 ms. Participants exhibited an even longer time-to-peak and time-after-peak velocity, as well as failing to scale peak velocity to each target distance. However, there was no significant influence of visual condition on constant and variable error, thus indicating that the modifications to movement kinematics were successful in maintaining terminal accuracy. Importantly, whereas previous work on reaching to grasp a static target reported a general intolerance for alternating monocular vision (Hansen et al., 2011), we found here that the movement kinematics were unchanged when alternating monocular samples were provided consecutively and without an interocular delay.

To explain these findings, it is relevant to consider what different sources of information are useful for control of prehension and manual aiming, and how that information influences the process of visual integration. It has been shown that prehensile movements, comprising a reach that brings the hand toward a static target followed by a grasp that closes the fingers and thumb onto preselected points on the target surface, are disrupted by perturbation of binocular disparity (Bradshaw, Elliott, Watt, Hibbard, Davies, & Simpson, 2004; Melmoth & Grant, 2006; Melmoth et al., 2007). In normal (i.e., unperturbed) conditions of binocular and monocular vision (random or blocked presentation), differences in movements kinematics are less obvious, but have been observed during the latter stages of the reach and grasp (Melmoth et al., 2007). Accordingly, it has been suggested that binocular disparity contributes to online control of the reach and the grasp, while vergence (i.e., extraretinal input) provides information on target distance that is used for initial reach planning. More specifically, it has been argued that coarse binocular disparity (i.e., disparity when the point of fixation does not coincide with the target of interest) is used to initially control the reduction in distance between hand and target, whereas fine binocular disparity contributes to planned grip forma-tion and closure of the fingers and thumb onto preselected grip points (Melmoth et al., 2007). Presenting alternating samples without an interocular delay during reach-to-grasp tasks would seem to disrupt the perception of one, or both forms of binocular disparity, which then impact the on-line control and grasp formation processes (Hansen et al., 2011).

In manual aiming, there is no requirement to grasp an object, but it is still necessary to exhibit accurate and precise control of the effector as it moves close

102 Hansen, Hayes and Bennett

to a small target. Typically, the eyes are located on the target well before the effec-tor arrives in the region of (para) fovea (Deconinck, van Polanen, Savelsbergh, & Bennett, 2011; Helsen, van den Berg, Tremblay, & Elliott, 2004), thus providing the opportunity for extraretinal (e.g., vergence, efference copy) and retinal contribu-tions. In the majority of situations, extraretinal and monocular retinal (e.g., motion parallax and/or constriction within the retinal image) input provides sufficient information to perform manual aiming similar to that exhibited with binocular vision (cf., Coull et al., 2000). However, this does not imply that binocular input would not be used if it was available. Rather, redundancy in the available perceptual information (e.g., binocular disparity, monocular parallax), provides participants with the opportunity to maintain performance when faced with a change of condi-tions (i.e., binocular vs. monocular).

In the current study, sufficient information was perceived from alternating monocular samples received consecutively and without delay. This could have been based of interocular integration of monocular input, with alternate images being fused into a binocular percept or superimposed into a monocular percept. On the other hand, intraocular integration could have occurred if input to one eye persisted over a 25 ms delay (i.e., the duration of the ignored monocular sample), leading to a continuous monocular percept. Similar limits of interocular and intraocular integration have been reported in one-handed catching (Bennett et al., 2006), where the timing of hand closure is based upon coarse binocular disparity (Bennett et al., 2000; Rushton & Wann, 1999), and monocular retinal input (e.g., expansion and/or relative rate of expansion; Savelsbergh, Whiting, & Bootsma, 1991). Together, the implication is that task-specific sources of information used during the control of prehensile and manual aiming movements influence the toler-ance to interocular delay.

Our results are also consistent with the suggestion that the participant’s expectation regarding the upcoming stimulus condition influences the motor response (Elliott et al., 2010; Flatters et al., 2012; Hansen, Glazebrook, Anson, Weeks, & Elliott, 2006; Tijtgat, Bennett, Savelsbergh, De Clercq & Lenoir, 2010). For instance, with the introduction of an interocular delay, participants modified kinematic measures associated with planning, as well as on-line control (50 ms interocular delay only), to adapt to the informational perturbation. In terms of move-ment planning, had participants simply underestimated (or overestimated) target distance in advance of movement onset in these alternating monocular conditions, it could be expected that both magnitude and time-to-peak velocity would have been reduced (or increased) in accord with the target distance effect. This was not the case and is consistent with the movement being planned using information on target distance from extraretinal input, as well as form in depth from alternating monocular samples (Ross & Hogben, 1974). Nevertheless, it would appear that participants’ recognized, based on experience of previous trials, that they would have difficulty during on-line control in the alternating monocular conditions, thus resulting in the use a more cautious strategy that involved moving more slowly and spending longer during the latter stages of the movement as the cursor came into the vicinity of the target. This strategy was developed early in a block (i.e., no difference between trials 1–5 vs. trials 6–10) and was effective in maintaining terminal accuracy within acceptable bounds.

Integration of Alternating Monocular Samples 103

ConclusionTo maintain manual aiming accuracy when alternating monocular vision samples were separated by an interocular delay, participants moved with a reduced limb velocity and overall longer movement time. No such modification to the movement kinematics was observed when alternating monocular samples were received con-secutively and without delay. These findings are consistent with the hypothesis that task-specific sources of information have different tolerance to interocular delay.

Acknowledgment

We gratefully acknowledge the contributions of Mark Hallam during data collection and analysis.

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