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Low Vision  |   May 2013
Dual Cognitive Task Affects Reaching and Grasping Behavior in Subjects With Macular Disorders
Author Affiliations & Notes
  • Shahina Pardhan
    Vision and Eye Research Unit, Postgraduate Medical Institute, Cambridge, United Kingdom
  • Sander Zuidhoek
    Royal Dutch Visio, Haren, The Netherlands
Investigative Ophthalmology & Visual Science May 2013, Vol.54, 3281-3288. doi:10.1167/iovs.12-11045
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      Shahina Pardhan, Sander Zuidhoek; Dual Cognitive Task Affects Reaching and Grasping Behavior in Subjects With Macular Disorders. Invest. Ophthalmol. Vis. Sci. 2013;54(5):3281-3288. doi: 10.1167/iovs.12-11045.

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Abstract

Purpose.: Subjects with macular disorders need longer time to plan and execute a reaching and grasping task compared with normally sighted controls. In everyday life it is normal to perform reaching and grasping movements while simultaneously carrying out a cognitively demanding task. We investigated whether a simultaneous “counting task” further affects the ability to reach and grasp an object in subjects with visual impairment (VI). As the visually guided action is considered to be solely under the control of the automatic parieto–premotor pathway, we hypothesize that there will be minimal effect of the counting task, needing working memory and attention, which is mediated by other pathways, on the performance of the reaching and grasping tasks.

Methods.: Fourteen subjects with VI and 14 age-matched controls reached out and grasped a target while carrying out a counting task (“easy,” “difficult,” “no count”). A motion analysis system recorded and reconstructed the 3D hand and finger movements.

Results.: Significant differences (P < 0.05) occurred for various indices between the two visual groups. Significant interaction effects occurred between the two groups for “onset time,” “time after maximum grip,” and “time after maximum velocity,” indicating that the dual task affects both the planning of the movement and the ability to carry out “online corrections.”

Conclusions.: In both groups, the onset time was affected by the counting task, which requires attention and working memory. In VI subjects, the dual task affected “online corrections,” suggesting that visually guided movements are not solely under the control of automatic processes.

Introduction
Prehensile movements of reaching and grasping are generally measured through two components: transport and grasping. The transport component is normally measured using kinematic indices such as peak velocity, time taken to attain peak velocity, and deceleration times. The grasping component is represented by the maximum grip aperture. Both the transport and grasping components are closely coordinated during the execution of the movement. 1,2 General parameters, onset time, and movement duration give information about the initial planning and the overall ability to carry out the task. Prior to starting a movement, the location of the target will inform the planning of the movement that will determine indices such as time to attain maximum grip aperture. Once the movement has commenced, corrections to the movement trajectory to compensate for any errors in the initial planning, and to add dynamic visual and proprioceptive feedback (online control), are determined by time after maximum grip aperture and time after maximum velocity. 3  
In normal reaching and grasping behavior, both the ventral and dorsal visual streams of the brain are involved. 3,4 The ventral stream is believed to be involved in the identification of the target. Initially, research 5 speculated that the dorsal stream established the spatial location of the target: the “where” system. Later work, however, postulated that the dorsal stream is mainly used for computing the visuomotor transformations required for the guiding of action and is not (strictly) used for the conscious localization of targets. 1,6,7 Recent research suggests that there may be as many as three pathways emerging from the dorsal stream, consisting of projections to the prefrontal and premotor cortices, and a major projection to the medial temporal lobe that courses both directly and indirectly through the posterior cingulate and retrosplenial cortices. 8 These three pathways support conscious and nonconscious (automatic) visuospatial processing, including spatial working memory, visually guided action, and navigation, respectively. 
The prefrontal pathway is involved in spatial working memory (area 46). This pathway is involved in tasks that require conscious, active spatial processing of the visual input and whose input would add content to visual representation. The second pathway, premotor, is responsible for the translation of visual input into motor coordinates, thereby mediating eye movements and tasks such as reaching and grasping. This pathway, unlike the prefrontal, is believed not to require attention but to be independent of visual consciousness. In reaching and grasping tasks, visuomotor transformations are mediated by the premotor pathway. The prefrontal pathway, which is involved in conscious active spatial processing, would not normally be involved in the reaching and grasping task unless visual–spatial working memory processes, such as the conscious judging or mental manipulation of spatial attributes, are required. Processing in these different visual streams can be disrupted independently of one another. 
Various studies have demonstrated how reaching and grasping behavior is altered with brain or ocular dysfunctions. In visual form, agnosia, which arises from damage to the ventral stream, the perceptual system is affected, whereas the visuomotor (reaching and grasping) system remains intact. 9 Optic ataxia, which affects the dorsal area of the brain, results in difficulties in reaching and grasping, whereas the ability to describe the orientation and location of the object remains unaffected, 10,11 implying that the parieto–premotor pathway is disrupted, but that the ventral and parieto–prefrontal pathways remain functional. Literature also provides evidence of how reaching and grasping are affected in subjects with various visual deficits including those with stereo-deficiency 12 ; with artificially restricted peripheral fields of view 1315 ; with glaucoma 16 ; with macular disorders 1721 ; and who were blind from birth. 22  
Previous studies have also investigated the effect of a simultaneous cognitive task on balance and postural stability, 2326 and whether a dual task paradigm can be used to identify older individuals who are more susceptible to falls. 27,28 Data suggest that the extra cognitive demand has a negative effect on balance performance, 26 even though the cognitive task by itself may not have an effect on postural stability. Another study reported that a simultaneous reaching and grasping task decreased the performance of an auditory task in normal subjects. 29  
Recent work from our laboratory has shown that visual impairment, in subjects with macular disorders, affects reaching and grasping behavior when compared with normally sighted subjects. 17,1921 More specifically, subjects with macular disorders need more time to plan and initiate the movement (increased onset time). These subjects also require longer “time after maximum grip aperture” and “time after maximum velocity” has been attained, implying that the initial movement planning is insufficient and that more time for “online corrections” is also required to complete the movement accurately. In healthy subjects it is assumed that these “online corrections” are carried out by the parieto–premotor pathway, which is thought to be implicit and automatic. 8  
In this study we build on our previous findings to explore whether a simultaneous cognitive task, such as a counting backward task requiring working memory and attention, would influence the reaching and grasping behavior further in subjects with central visual impairment. Visually guided action is thought to be mediated only by the parieto–premotor pathway. Processing in this pathway is believed to be implicit and automatic (i.e., not to depend on attention or working memory processing). Thus, we hypothesize that “online corrections” of the reaching and grasping movement would not be influenced by tasks that require attentional and/or working memory processes. Hence, indices that denote online processes in reaching and grasping, such as “time after maximum grip aperture” and “time after maximum velocity,” which are thought of as automatic and under the control of the premotor pathway, would remain unaltered by the additional counting exercise of the dual task. However, if the simultaneous execution of the counting task, requiring working memory and attention, affected the time to carry out the “online corrections,” then it is likely that other pathways, such as the parietal–prefrontal pathway, that mediate attention and working memory, also influence these “online corrections,” implying a sharing of common resources. In addition, if the data do suggest the sharing of common resources, it would be interesting to explore whether the “difficulty” of the counting task will influence the results. 
Materials and Methods
Subjects
Fourteen subjects with reduced vision (VI), diagnosed with binocular macular disorders by an ophthalmologist, and who were attending the University's low vision clinic, took part. The mean demographics of the subjects are given in Table 1. Six subjects had dry age-related macular degeneration, six had early onset macular changes due to Stargart's disease, and two had neovascularization. Binocular visual acuity and contrast sensitivity were measured, given that reaching and grasping activities are usually carried out using habitual vision of both eyes. Contrast sensitivity was measured using the Pelli Robson chart at 1 meter (m). Contrast sensitivity was scored letter by letter (0.05 log units). LogMAR (logarithm of the minimum angle of resolution) acuity was measured using the Bailey Lovie chart at the normal working distance of 6 m. For visual acuity, letter-by-letter scoring (0.02 log) was used. If subjects were unable to read the largest letters on the logMAR chart at 6 m, the chart distance was reduced to either 3, 1.5 m, or less and testing repeated until an acuity measure was obtained. A conversion factor was then applied to obtain the correct logMAR score used for distances other than 6 m. Both contrast sensitivity and visual acuity measurements were carried out under normal room illumination (100 cd/m2) using the best corrected spectacle prescription, using trial lenses (sphere and cylinder) for the distance tested. None of these subjects had any measurable stereopsis (TNO and Titmus stereo test). 
Table 1. 
 
The Mean Demographics of All Subjects
Table 1. 
 
The Mean Demographics of All Subjects
Age, y Duration, y Contrast Sensitivity, log LogMAR Acuity, log
Normally sighted subjects (n = 14)
 Mean 71.14 n/a 1.73 −0.03
 SD 10.77 0.08 0.04
 Range 53–84 1.65–1.85 −0.1 to 0
Subjects with reduced vision (VI) (n = 14)
 Mean 70.87 14.41 1.05 0.98
 SD 10.77 14.46 1.39 0.39
 Range 51–83 0.75–36 0.45–1.65 0.2–1.38
Age-matched older subjects with normal vision (visual acuity of 6/6 in each eye and CS score > 1.65 log units, without any history of amblyopia or any diagnosed ocular pathology) were recruited. A t-test showed no significant difference in age between the normally sighted group and subjects with macular disorders (t 26 = −0.06, P = 0.94). 
All subjects (subjects with VI and normally sighted controls) were corrected optimally, as determined by a subjective refraction, for the working distance of 40 cm. This optimal prescription was given using full aperture trial lenses (sphere and cylinder). Informed consent was obtained after the nature and possible consequences were explained. Ethical clearance was obtained from the University's Ethical Committee and Declarations of Helsinki were observed. 
Apparatus and Stimuli
Data collection and data analysis were performed using a purpose-built camera system (Vicon 460‐6 Motion Analysis System; Vicon, Oxford, UK). Vicon 460 consists of a 460 data-station, with six high-resolution cameras (Mcam2) located at different positions in the laboratory. The Mcam2 offers 1280 × 1024 pixel resolution with a speed of up to 1000 frames per second. Each camera has a ring of light-emitted diode (LED) strobe lights fixed around the lens. As the subject's hand moves through the capture area, the light from the strobe is reflected back into the camera lens and stimulates a light-sensitive plate creating a video signal. The Vicon Workstation controls the cameras and strobes and also collects the signals. The signals are then transferred to a computer on which the Vicon software (Polygon Version) was installed. The Vicon software (Polygon) collated and processed the data from all six cameras by combining the original calibration data to reconstruct the digital motion in three dimensions (kinematic data). In addition, two video cameras videotaped the sessions. In this way the participant's hand movements were completely recorded. 
Six circular reflective markers were attached with small pieces of nonallergic adhesive tape to the dominant hand of the subjects and at the center of the target. Each marker had a diameter of 9.5 mm. The markers were placed at the following six anatomic positions and were at least 1 cm apart: nail of the index finger, middle of the index finger, base of the index finger, head of the radius at the wrist, nail of the thumb, and base of the thumb. 
Procedure
Subjects sat comfortably in front of a table (83 × 108 cm) covered with a black cloth. The target was a round white cylinder 4 cm high of one of two different diameters (4.0 and 7.5 cm). Two object distances were used (36 or 56 cm) with the cylinder positioned along the participant's midline. The two different sizes and two different distances were used to introduce a degree of variability and also to ensure that subjects did not just reach out and grasp a target because they knew its position and size. All subjects confirmed that they could see both target sizes at the distances at which they were placed. 
Subjects were instructed to make natural reaches with their right hand and pick up the target with their thumb and index finger only. Reaches were made under binocular viewing conditions with normal room illumination. All subjects were examined for hand dominancy prior to starting the experiment with the Edinburgh Handedness Questionnaire and they were all right handed. Subjects were instructed to keep their eyes closed between trials and to open them only when they heard the word “start” to commence a new trial. This prevented subjects from previewing the target size and location. To carry out a dual task, the reaching and grasping and cognitive (counting backward) tasks were carried out simultaneously. Three measurements were taken for each size and distance parameter for each dual task condition. Two sizes (with three measurements for each) and two distances (three measurements for each) resulted in 12 trials per dual task condition, giving a total of 36 trials. This was then repeated three times in different blocks, randomly interleaved, giving a total of 108 trials per subject over the three dual task conditions. 
We introduced the duality of the task by asking the subjects to count backward from a number set by the experimenter while carrying out a reaching and grasping movement. Two counting tasks were used: (1) Subjects were asked to count backward in steps of two from a random number (between 1 and 100) chosen by the examiner, (e.g., 97, 95, 93, and so on [easy task]); (2) subjects were asked to count backward in steps of four (difficult task). A pilot study had been conducted with six subjects. Different counting tasks were explored and all subjects confirmed that the second counting task (counting backward in steps of four) was always more difficult that the first (counting backward in steps of two). All subjects thought that a more difficult task of counting backward in steps of six was going to be impossible to manage for the dual task. The chosen starting number and the difficulty of the task were varied between trials, so that subjects were not able to recall the sequence of numbers. Subjects started the counting task before the reaching task was initiated and with their eyes closed. As soon as they heard the word “start” they had to open their eyes and reach out and grasp the target while counting at the same time. Trials in which subjects stopped counting when they heard the word “start,” or at any time during the movement, were discounted. All trials were video recorded, which enabled the experimenter to examine, post trial during data analysis, whether there were any errors in the counting task or even if the subject stopped any of the two tasks in the dual task. Trials were viewed using two video cameras (Sony Corporation of America, New York, NY) placed 1.5 m on either side of the participant. The participant was not aware of the video recording. Each trial was video recorded. Post trial viewing of each video recorded trial ensured that the participant had carried out the dual task and that they had carried out the counting task accurately as instructed by the examiner. If counting had stopped within the trial or the participant gave incorrect answers then the trial was discounted. The video recording was used only to ensure that the dual task was carried out and that the counting task answers were accurate. It was not used to examine any kinematic index or to examine the accuracy of any other kinematic data. Postviewing of the recorded trials was carried out in real time. No subject made more than 5% errors in the counting task. If errors were made or if the subject stopped counting or the movement, trials were discarded from the final analysis. Subjects with macular disorders did not make any more errors than the normally sighted group. The video recording also enabled us to ascertain that subjects did not open their eyes prior to the commencement of the trial (before the word “start”). 
Training was given before the commencement of data collection. Training time was unlimited and it was deemed to be complete when subjects felt that they were ready to undertake the experiment. They also had to make no errors in three consecutive trials with the “difficult task.” To decrease any subject variability introduced due to different latencies at the beginning of the trial, and to obtain accurate measurements for the total time, measurement, and analysis commenced when the marker on the finger tip moved on the computer screen. The trial also ended as soon as the target was picked up, to avoid any latency between the target being picked up and the vertical movement of the hand stopping. 
Measurements
Parameter Relating to Overall Planning of the Movement.
  •  
    Onset Time (s): the time between the audible signal and participants moving their hand from the starting position. This was assessed as the time recorded in the system between the commencement of the experiment denoted by the word “start” and the movement of the marker on the index finger tip.
Parameter Relating to the Transport Component.
  •  
    Maximum Velocity (mm/s): maximum speed of the movement.
  •  
    Time taken to attain Maximum Velocity. Time between the movement starting and when the maximum velocity is attained. This is independent of onset time.
Parameters Relating to the Grasping Component.
  •  
    Maximum Grip Aperture (mm): calculated as the maximum distance between the thumb tip and index nail markers.
  •  
    Time taken to attain Maximum Grip Aperture. Time between the movement starting and when the maximum grip is attained. This is independent of onset time.
Parameters Relating to Online Control.
  •  
    Time after Maximum Velocity (s): time taken from maximum velocity to the time that the object is grasped. This parameter explores the on-line control of the transport component.
  •  
    Time after Maximum Grip Aperture (s): time taken from maximum grip aperture to the time that the object is grasped. This parameter explores the online control of the grasping component.
Results
All subjects could complete the task adequately and no subject made >5% errors in total in the counting tasks. Trials with errors were discarded. When questioned offline, subjects (both visually impaired and normally sighted) reported that it was difficult to carry out the dual task compared with the single reaching task. In addition all subjects could count accurately when asked to do so with their eyes closed, indicating an ability to carry out the task accurately. No significant differences (t-test, P > 0.05) occurred between the time taken to carry out the same counting task by either group. 
To ensure that there were no differences in the ability to use their hands to reach out and grasp an object, irrespective of whether they had normal or degraded vision, a pilot task was carried out. Subjects were asked to keep their eyes closed and when they heard the word “start” were instructed to extend their limb as if they were reaching and grasping a hypothetical object. This “time to start the movement without the influence of their vision” was recorded (Vicon motion analysis system). There was no significant difference in the time taken to start the movement between the two groups (P > 0.05). The pilot task and this measurement are different from the “onset time” measured in the main experiment (see below) in which subjects used their vision (normal or degraded) to carry out a reaching and grasping movement. No differences were obtained in the onset time (P > 0.05) between the two groups. 
Initially, data for the two visual groups were examined individually to ascertain whether dual tasking affected the groups differently. Table 2 shows the results of repeated-measures ANOVA for the different levels of the cognitive task (no counting, easy task, and difficult task) for each of the two groups. 
Table 2. 
 
Repeated-Measures ANOVA for the Different Levels of the Cognitive Task (No Counting, Easy Task, and Difficult Task) Carried Out Individually for Each of the Two Groups
Table 2. 
 
Repeated-Measures ANOVA for the Different Levels of the Cognitive Task (No Counting, Easy Task, and Difficult Task) Carried Out Individually for Each of the Two Groups
Normally Sighted Only Visually Impaired (VI) Only Combined Normally Sighted and Visually Impaired (VI)
Kinematic index 1: ANOVA 2: Tukey's post hoc analysis 3: ANOVA 4: Tukey's post hoc analysis 5: Visual Group (VI) vs. normal) 6: Interaction: Visual group vs. counting task 7: Size 8: Distance
Onset time, s F 2,64 = 9.05; P < 0.001) non/diff* F 2,104 = 13.39; P < 0.001 non/easy* non /diff* F 1,84 = 15.37; P < 0.001 F 2,168 = 3.83; P = 0.022 ns ns
Max velocity, m/s ns n/a ns n/a ns ns ns F 1,84 = 10.21; P = 0.001
Time to max velocity, s F 2,64 = 8.98; P = 0.003 non/easy*
non/diff*
F 2,104 = 27.97; P < 0.001 non/easy* non/diff* F 1,84 = 12.714; P = 0.006 ns ns F 1,84 = 12.05; P = 0.001
Time after velocity, s ns n/a F 2,104 = 16.123; P < 0.001 non/easy* non/diff* F 1,84 = 25.76; P = 0.002 F 2,168 = 6.85; P = 0.001 ns F 1,84 = 9.42; P = 0.002
Max grip aperture, mm ns n/a ns n/a ns ns F 1,84 = 4.33; P = 0.04 ns
Time to max grip aperture, s ns n/a ns n/a F 1,84 = 4.44; P = 0.003 ns ns F 1,84 = 8.34; P = 0.003
Time after max grip aperture, s ns n/a F 2,104 = 11.564; P < 0.001 non/easy*
non /diff*
F 1,84 = 13.81; P < 0.001 F 2,168 = 11.32; P < 0.001 ns F 1,84 = 11.26; P = 0.001
In the normally sighted group, the onset time was longer in the presence of a cognitive task (F 2,64 = 9.05; P < 0.001). Post hoc analysis for onset time showed a significant difference between the no-count and the difficult task only (P = 0.03) (Table 2). Time to maximum velocity was also affected. It took significantly longer to attain maximum velocity in the normally sighted group while carrying out a counting task (F 2,64 = 8.98; P = 0.003). Post hoc analysis showed that even the easy task affected reaching and grasping behavior (P < 0.001) when compared with the no-counting task. No other index was affected by the dual task in normally sighted subjects, suggesting that online corrections (as denoted by time after maximum velocity and time after maximum grip aperture) were not affected by the dual task in the normally sighted group. 
In subjects with macular disorders (VI), in addition to the onset time (F 2,104 = 13.39; P < 0.001) and time to maximum velocity (F 2,104 = 27.97; P < 0.001), other indices were also affected including “time after maximum velocity” (F 2,104 = 16.123; P < 0.001) and “time after maximum grip aperture” (F 2,104 = 11.564; P < 0.001). Post hoc analysis showed that even the easy task affected reaching and grasping behavior (P < 0.002). Interestingly, there were no significant differences between the easy and the difficult cognitive task. 
A mixed within–between repeated-measures ANOVA was performed combining the visual group (normally sighted versus visually impaired group) for the three counting condition (3) (no counting, easy task, difficult task) × object distance (2) × object size (2) (Table 2). 
Onset Time
The onset time was significantly longer for subjects with reduced vision compared with normally sighted subjects (F 1,84 = 15.37; P < 0.001) and there was a significant interaction with the cognitive task (F 2,168 = 3.83; P = 0.022) as shown by Figure 1. Post hoc analysis shows significant differences between the two groups for the no count (P = 0.024), easy task (P = 0.002), and difficult task (P = 0.001). 
Figure 1
 
Onset Time was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.05). Vertical bars: 0.95% confidence intervals.
Figure 1
 
Onset Time was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.05). Vertical bars: 0.95% confidence intervals.
Maximum Velocity
Maximum velocity was not affected by the size or the visual group. No significant interaction occurred. As expected, the maximum velocity was significantly affected by the distance of the object but not by the size of the object. 
Maximum Grip Aperture
Maximum grip aperture was not affected by the dual task or by the visual group. As expected, it was affected by the size of the object but not by the distance at which the object was placed. 
Time to Maximum Velocity
The time to maximum velocity was significantly longer in subjects with visual impairment compared with normally sighted subjects (F 1,84 = 12.714; P = 0.006). Although the simultaneous counting task increased this index in both groups of subjects, there were no significant interaction effects, indicating that the dual task did not adversely affect the behavior of subjects with macular disorders when compared with normally sighted subjects. 
Time After Maximum Velocity
The time after maximum velocity was significantly longer in subjects with reduced vision compared with normal subjects (F 1,84 = 25.76; P = 0.002). There was a significant interaction with the cognitive task (F 2,168 = 6.85; P = 0.001) as shown by Figure 2. Subjects with reduced vision needed a longer time after maximum velocity was attained to complete the movement. Post hoc analysis shows a significant difference between the two groups for the no count (P = 0.03), for the easy task (P = 0.002), and for the difficult task (P < 0.001). 
Figure 2
 
Time after Maximum Velocity was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.001). Vertical bars: 0.95% confidence intervals.
Figure 2
 
Time after Maximum Velocity was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.001). Vertical bars: 0.95% confidence intervals.
Time After Maximum Grip Aperture
The time spent after maximum grip aperture was significantly longer in subjects with reduced vision (F 1,84 = 13.81; P < 0.001) and a significant interaction was obtained (F 2,168 = 11.32; P < 0.001) as shown in Figure 3. Post hoc analysis show no significant difference between the two groups for the no count (P = 0.69) but significant differences for the easy task (P = 0.001) and the difficult task (P = 0.0002). 
Figure 3
 
Time after Maximum Grip Aperture was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.05). Vertical bars: 0.95% confidence intervals.
Figure 3
 
Time after Maximum Grip Aperture was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.05). Vertical bars: 0.95% confidence intervals.
Discussion
This study builds on the previous work from our laboratory, which has shown that degrading the central visual input, as in subjects with macular disorders, leads to the need for an increased time to start the movement and also to carry out “online corrections.” Data from this study provide evidence that the introduction of a simultaneous cognitive task further increases the time required to perform the movement. Significant interactions between the dual and the single tasks in the two visual groups demonstrate that the counting task affects the same three kinematic indices: onset time, time after maximum velocity, and time after maximum grip aperture. The significant interaction effect obtained for onset time for the dual task demonstrates that, in subjects with VI, even longer time is needed to plan and start the movement, when compared with normally sighted subjects. 
Why should the dual task further affect the overall planning, as demonstrated by increased onset time, in both visually impaired subjects and in normally sighted subjects? Our data do not support the hypothesis as outlined earlier in the introduction, that visually guided action is mediated by the automatic, implicit parieto–premotor pathway only. Our data suggest that a commonality of resources must exist for representing the target in the peripersonal space for the visually guided motor action and for carrying out the cognitive task simultaneously. Since the counting task would not encompass visual/spatial processing, the most likely common resource would be attention linked to the working memory. The visual/spatial representation of the target, which is required to plan the movement and to initiate the decision to start it, must also draw on attentional resources that are then, obviously, not so abundantly available during the dual task. Indeed it has been shown that visuomotor action is susceptible to interference from multiple visual inputs and therefore is less effective at guiding actions online when multiple targets are attended. 30 The fact that our data show that the dual task affects normally sighted subjects as well as subjects with VI indicates that the initial planning of the movement shares resources during the dual task, demonstrating the importance of attention and working memory processes in planning the reaching and grasping action in both groups. Relating this finding to the different visual streams, we would suggest that the ventral as well as the dorsal parieto–prefrontal pathways are involved: the former in identifying the target, the latter in controlling eye movements (and visual selective attention) in a top-down fashion and possibly in consciously estimating the target's position. 
In line with our previous studies we found that, once the movement was planned, no significant differences in the maximum velocity and maximum grip aperture occurred between the two visual groups. In addition, these kinematic indices were not affected by the dual task, suggesting that maximum grip aperture, which represents the quality of the intrinsic spatial characteristics, was not affected by the dual task. Our data suggest that, in subjects with macular disorders, the intrinsic spatial properties of the target are processed and translated correctly into motor coordinates before the commencement of the movement. The location of the target was also translated correctly as indicated by similar maximum velocities in the two groups that were not affected by the simultaneous counting task. 
The dual task resulted in an increased time after maximum grip aperture and time after maximum velocity was attained, indicating decreased efficiency in making “online corrections” in VI subjects. Interestingly, the counting task did not affect these indices in normally sighted subjects. These data also do not support our hypothesis as outlined earlier in the introduction, in that “online control” is totally automatic and is mediated by the automatic, implicit parieto–premotor pathway only. In subjects with VI, these “online corrections” are influenced by the cognitive nonvisual dual task, again indicating the involvement of attention and working memory during these online corrections. We hypothesize that this is also most likely to be mediated by a parietal–prefrontal route involved in spatial working memory. 8 This requires further investigation, possibly by a direct measure of brain activity. 
It is possible that the decreased performance shown by subjects with macular disorders may also be attributed to the fact that they are likely to use their peripheral vision, which is linked to increased uncertainty and decreased accuracy when compared with central vision. 31,32 A direct comparison with the study 32 would not be justified because their data were from younger subjects who would not normally use their peripheral vision, whereas our subjects with macular disorders may have adapted to using their peripheral visual field. To test this further, a study in which the behavior of two groups of subjects with macular disorders, those who use their peripheral retinal locus and those who do not, would be required. Unfortunately, this is beyond the scope of this study. 
Interestingly, the two levels of task difficulty used in this study did not show significant differences. Although significant differences existed between the easy counting task and the single task, there were fewer differences between the easy and difficult counting tasks. A number of possible reasons may explain this: (1) the difficult dual task did not require significantly more attention than the easy task; (2) a capacity issue occurs in which the same behavior is shown irrespective of the level of counting difficulty beyond a certain threshold; (3) the conscious representation and/or selection of the target in space in visually impaired subjects is perturbed by even a seemingly simple cognitive task; and (4) the difficult task was just not significantly different from the easy task. Further investigations could reveal the answer to these by using different and/or a more demanding cognitive task(s). 
We acknowledge some limitations in this study: the use of only two very different object sizes may have made it easy for subjects to memorize the sizes of the objects and mask any differences in maximum grip aperture in the dual task condition. In addition, in subjects with macular disorders, because the clarity and the representation of visual space and target have deteriorated, it is very likely that these subjects use extra foveal preferred retinal locations that would contribute to the decrease in ability to complete the movement efficiently. Indeed, reduced accuracy in performance has been shown in normal subjects who were asked to pick up targets placed in their peripheral field. 32 It would have therefore been useful to examine whether our subjects used their peripheral vision while carrying out the task. It is likely that they did. However, without explicitly measuring this, it is difficult to know exactly. In addition, it has been reported that monocular vision alone as opposed to binocular viewing can adversely affect some reaching and grasping indices. 33 It is likely that our subjects had very little or no binocular vision. However, although no stereopsis was shown in subjects with macular disorders, the employment of the “best monocular acuity” as opposed to binocular acuity was not explicitly tested. It is appreciated that the Frisby stereoscopic test may have been a more useful test compared to the Titmus and TNO tests as contrast detection may have been better maintained for the visually impaired subjects. In addition, although care was taken to ensure that the same protocol for the dual task was followed by all subjects, there is a possibility that different counting strategies may have been used by subjects. Postviewing of the video-taped trials enabled 5% of the trials to be discounted, for example, when subjects had stopped counting or had ceased the reaching and grasping movement during the dual task trial, or when the counting task scores were not accurate. Unfortunately, it was not possible to explore if subjects used different counting strategies. 
Further studies, including carefully designed experiments to examine “online corrections,” such as those that change the location of the target during the course of the movement, 34 may provide more information about the underlying processes that govern this behavior. Nevertheless, data from this study provide evidence that, for subjects with visual impairment caused by macular disorders, it is important to recognize that a simultaneous cognitive task decreases their ability to carry out a simple reaching and grasping task even further, affecting both the overall planning and further decreasing the ability to correct a movement once it has commenced. 
Acknowledgments
Supported by the Vision and Eye Research Institute (VERU). 
Disclosure: S. Pardhan, None; S. Zuidhoek, None 
References
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Figure 1
 
Onset Time was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.05). Vertical bars: 0.95% confidence intervals.
Figure 1
 
Onset Time was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.05). Vertical bars: 0.95% confidence intervals.
Figure 2
 
Time after Maximum Velocity was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.001). Vertical bars: 0.95% confidence intervals.
Figure 2
 
Time after Maximum Velocity was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.001). Vertical bars: 0.95% confidence intervals.
Figure 3
 
Time after Maximum Grip Aperture was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.05). Vertical bars: 0.95% confidence intervals.
Figure 3
 
Time after Maximum Grip Aperture was significantly longer in subjects with macular disorders (VI) with a significant interaction obtained with the dual task (P < 0.05). Vertical bars: 0.95% confidence intervals.
Table 1. 
 
The Mean Demographics of All Subjects
Table 1. 
 
The Mean Demographics of All Subjects
Age, y Duration, y Contrast Sensitivity, log LogMAR Acuity, log
Normally sighted subjects (n = 14)
 Mean 71.14 n/a 1.73 −0.03
 SD 10.77 0.08 0.04
 Range 53–84 1.65–1.85 −0.1 to 0
Subjects with reduced vision (VI) (n = 14)
 Mean 70.87 14.41 1.05 0.98
 SD 10.77 14.46 1.39 0.39
 Range 51–83 0.75–36 0.45–1.65 0.2–1.38
Table 2. 
 
Repeated-Measures ANOVA for the Different Levels of the Cognitive Task (No Counting, Easy Task, and Difficult Task) Carried Out Individually for Each of the Two Groups
Table 2. 
 
Repeated-Measures ANOVA for the Different Levels of the Cognitive Task (No Counting, Easy Task, and Difficult Task) Carried Out Individually for Each of the Two Groups
Normally Sighted Only Visually Impaired (VI) Only Combined Normally Sighted and Visually Impaired (VI)
Kinematic index 1: ANOVA 2: Tukey's post hoc analysis 3: ANOVA 4: Tukey's post hoc analysis 5: Visual Group (VI) vs. normal) 6: Interaction: Visual group vs. counting task 7: Size 8: Distance
Onset time, s F 2,64 = 9.05; P < 0.001) non/diff* F 2,104 = 13.39; P < 0.001 non/easy* non /diff* F 1,84 = 15.37; P < 0.001 F 2,168 = 3.83; P = 0.022 ns ns
Max velocity, m/s ns n/a ns n/a ns ns ns F 1,84 = 10.21; P = 0.001
Time to max velocity, s F 2,64 = 8.98; P = 0.003 non/easy*
non/diff*
F 2,104 = 27.97; P < 0.001 non/easy* non/diff* F 1,84 = 12.714; P = 0.006 ns ns F 1,84 = 12.05; P = 0.001
Time after velocity, s ns n/a F 2,104 = 16.123; P < 0.001 non/easy* non/diff* F 1,84 = 25.76; P = 0.002 F 2,168 = 6.85; P = 0.001 ns F 1,84 = 9.42; P = 0.002
Max grip aperture, mm ns n/a ns n/a ns ns F 1,84 = 4.33; P = 0.04 ns
Time to max grip aperture, s ns n/a ns n/a F 1,84 = 4.44; P = 0.003 ns ns F 1,84 = 8.34; P = 0.003
Time after max grip aperture, s ns n/a F 2,104 = 11.564; P < 0.001 non/easy*
non /diff*
F 1,84 = 13.81; P < 0.001 F 2,168 = 11.32; P < 0.001 ns F 1,84 = 11.26; P = 0.001
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