Human Eye Movements during Visually Guided Stepping

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<ul><li><p>This article was downloaded by: [McMaster University]On: 16 October 2014, At: 13:15Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK</p><p>Journal of Motor BehaviorPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/vjmb20</p><p>Human Eye Movements during Visually Guided SteppingMark A. Hollands a , Dilwyn E. Marple-Horvat a , Sebastian Henkes a &amp; Andrew K. Rowan aa University of Bristol , Bristol, U.K.Published online: 14 Jul 2010.</p><p>To cite this article: Mark A. Hollands , Dilwyn E. Marple-Horvat , Sebastian Henkes &amp; Andrew K. Rowan (1995) Human EyeMovements during Visually Guided Stepping, Journal of Motor Behavior, 27:2, 155-163, DOI: 10.1080/00222895.1995.9941707</p><p>To link to this article: http://dx.doi.org/10.1080/00222895.1995.9941707</p><p>PLEASE SCROLL DOWN FOR ARTICLE</p><p>Taylor &amp; Francis makes every effort to ensure the accuracy of all the information (the Content) contained in thepublications on our platform. However, Taylor &amp; Francis, our agents, and our licensors make no representations orwarranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinionsand views expressed in this publication are the opinions and views of the authors, and are not the views of orendorsed by Taylor &amp; Francis. The accuracy of the Content should not be relied upon and should be independentlyverified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims,proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arisingdirectly or indirectly in connection with, in relation to or arising out of the use of the Content.</p><p>This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyoneis expressly forbidden. Terms &amp; Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions</p><p>http://www.tandfonline.com/loi/vjmb20http://www.tandfonline.com/action/showCitFormats?doi=10.1080/00222895.1995.9941707http://dx.doi.org/10.1080/00222895.1995.9941707http://www.tandfonline.com/page/terms-and-conditionshttp://www.tandfonline.com/page/terms-and-conditions</p></li><li><p>Journal of Motor Behavior, 1995, Vol. 27. No. 2, 155-163 </p><p>Human Eye Movements During Visually Guided Steppina </p><p>Y </p><p>Mark A- Hollands Dilwyn E. Marple-Horvat Sebastian Henkes Andrew K. Rowan University of Bristol Bristol, U.K. </p><p>ABSTRACT. Visually guided locomotion was studied in an experiment in which human subjects (N = 8) had to accurately negotiate a series of irregularly spaced stepping-stones while in- frared reflectometry and electrooculography were used to con- tinuously record their eye movements. On average, 68% of sac- cades made toward the next target of footfall had been completed (visual target capture had occurred) while the foot to be positioned was still on the ground; the remainder were completed in the first 300 ms of the swing phase. The subjects gaze remained fixed on a target, on average, until 51 ms after making contact with it, with little variation. A greater amount of variation was seen in the timing of trailing footlift relative to visual target capture. Assuming that subjects sampled the vis- ual cues as and when they were required, visual information appeared most useful when the foot to be positioned was still on the ground. Key words: eye movements, locomotion, visuomotor </p><p>he environment through which we move consists of T irregular terrain cluttered with obstacles. As a result, a walking animal needs more than the simple reflex re- sponses or stereotyped rhythms, provided by spinal cir- cuitry, to perform purposeful actions efficiently. Su- praspinal motor control centers process a constant flow of incoming information and regulate gait patterns ac- cordingly. Most of the adaptations are in response to vis- ual cues, but the nature of these cues and how they are used to modify the basic locomotor synergy has not, un- til recently, received much attention. </p><p>Lee, Lishman, and Thomson (1982) investigated regu- lation of gait in long jumping and found fairly stereo- typed stride patterns during the run up to the board; ac- cumulated positional errors were regulated only in the last few strides before arrival at the take-off board. Dur- ing this homing-in phase, athletes regulated the verti- cal impulse of their steps to adjust their flight times so they would accurately strike the board. That they ad- </p><p>justed flight times rather than the spatial parameters of their gait suggests that the athletes were using informa- tion about how far in time they were from the board; time to contact was specified directly by the inverse of the rate of dilation of the retinal image of the board. (This information is available in the absence of information re- garding speed and distance from the board [Lee, 1980; see also Schiff &amp; Detwiler, 19791.) Vertical impulse also seemed to be the controlled parameter for varying step length when running (Warren, Young, &amp; Lee 1986). The visual information used to control vertical impulse was apparently provided by the optic variable time, which specifies time to contact when the velocity of an ap- proaching object remains constant. </p><p>In both long jumping and running, visual cues become important the moment that the process of avoidance or homing-in to the visual target needs to begin. The dis- tance of this point relative to the target depends upon several factors, such as speed of approach and the com- plexity of the adjustments that need to be made. Cutting, Springer, Braren, and Johnson (1992) divided this dis- tance into several components and calculated that by far the largest was the reaction time distance; the distance required to modify footfall was the least significant com- ponent. Gaze must therefore be adjusted so that informa- tion about an obstacle or footfall target can be received at least as far away as the sum of these components. </p><p>Once within the domain where visual cues are neces- sary, the timing of the visual sampling in relation to the </p><p>Correspondence address: Mark A. Hollands. Department of Physiology, University of Bristol School of Medical Science, University Walk, Brktol, BS8 ITD, U.K. E-mail address: M. HollandsQbristol.ac.uk </p><p>155 </p><p>Dow</p><p>nloa</p><p>ded </p><p>by [</p><p>McM</p><p>aste</p><p>r U</p><p>nive</p><p>rsity</p><p>] at</p><p> 13:</p><p>15 1</p><p>6 O</p><p>ctob</p><p>er 2</p><p>014 </p></li><li><p>M. A. Hollands, D. E. Marple-Horvat, S. Henkes, &amp;A. K. Rowan </p><p>step cycle is important, rather than the quantity. For ex- ample, with intermittent illumination during stepping, a very brief or instantaneous availability of visual informa- tion at particular points in time is more beneficial than longer lasting illumination at other times (see Assaiante, Marchand, &amp; Amblard, 1989). Laurent and Thomson (1988) went some way to determining when visual cues are most beneficial by measuring the effect of intermit- tent visual sampling on the ability of subjects to walk toward and step onto a static target (subjects shortened or lengthened their strides to attain the required loca- tion). A brief pulse of light was given either during the stance phase or the swing phase of the foot to be posi- tioned. When the light was delivered during the swing phase, locomotion became awkward and ill-coordinated. Laurent and Thomson concluded that visual information is most useful at particular times in the locomotor se- quence, specifically, that it is more beneficial to planning if received when the foot to be repositioned is still on the ground (see also Assaiante et al., 1989). </p><p>Visual cues are therefore used to regulate step length only at critical points in time, perhaps depending on the size of the adjustment that is needed. The greater the re- quired adjustment, the longer the time that is needed (Patla, Robinson, Samways, &amp; Armstrong, 1989). </p><p>The reason why sampling must occur at specific points in the action sequence presumably reflects the mecha- nisms used in altering gait: changing either step length or direction or both. Step length could be adjusted by changing reach at heel strike or by delaying or advancing heel strike; although this could occur late in the swing phase of the leg, such adjustment can easily leave the in- dividual off balance and can require further compensa- tory movements (which is, at best, inefficient). Hence, the use of the vertical impulse to regulate step length (Lee et al., 1982; Warren et al., 1986), in combination with more complex task-specific adaptations, is rendered necessary by important balance requirements (Patla et al., 1989). </p><p>Change in direction (to avoid obstacles or reach foot- fall targets) has been investigated by Patla, Prentice, Rob- inson, and Neufield (1991). A visual cue, delivered at two different times during walking, prompted subjects to al- ter direction by 60". They were unable to do this during the ongoing step but rarely failed when the cue to change was given on the previous step. Patla et al. concluded that subjects must plan direction change in the previous step so the acceleration of the body's center of mass toward the landing foot can be reduced to near zero. This allows translation of the center of mass toward the limb about to start the swing phase to begin earlier. </p><p>It has therefore been demonstrated that the visual cues associated with complex locomotor behavior need be used only at certain points in time during the step cycle. Evidence suggests that, while walking or running, visual cues are most useful when the foot to be positioned is on the ground. This is consistent with the theory of Lee et al., 1982, that step length is determined almost entirely </p><p>by the vertical component of the impulse applied during the stance phase. Other evidence suggests that informa- tion required to regulate step length is needed at different times, depending on the size of the required adjustment. The time required to preplan a change in direction ap- pears to be constrained by the mechanics involved in moving the body's center of mass to the required lo- cation. </p><p>In the experiments described above, visual information was given only at certain times during the step cycle, and the moment that an individual required visual informa- tion to perform precise footfall was inferred from how well subjects performed the given task under the different conditions. In contrast, our objective was to directly measure the point in time during the step cycle when vis- ual information is sampled and what that information comprises, which we achieved by accurately measuring eye movements continuously during a task that required precise placement of the feet at every step. Working on the assumption that individuals sample the most benefi- cial visual cues as and when they are required, this method should yield information on their nature and ex- actly when during the step cycle they are required to allow precision stepping. </p><p>Method </p><p>The Locomotor Tusk In this experiment, subjects were required to walk </p><p>upon a series of stepping-stones, arranged so as to de- mand precise foot placement at every step. Two different techniques were used to continuously record eye move- ments. The underlying rationale was that if the recorded eye movements could be related to the targets of footfall, the results should provide information regarding how and when visual cues are used in relation to the step cycle. </p><p>Subjects were asked to walk along a pathway of 18 irregularly spaced stepping-stones. The stones measured 10 X 10 cm and were attached to a 1.8- X 7-m length of heavy-duty white paper. We designed the small size of the stones and the irregularity of their spacing to necessitate visual sampling at every step. We also arranged the stones in a way that would require rela- tively large lateral movements of the walker's body and perhaps generate eye movements with a relatively large horizontal component. The stepping-stones consisted of pieces of copper-clad fiberglass (printed circuit board material) and were interconnected with multistrand equipment wire (invisible to the subject, beneath the pa- per sheet) and earthed. The configuration of stepping- stones is illustrated in Figure 1. </p><p>Footfall was recorded via sim- ple logic circuits connected to copper strips attached to the soles of the subjects' footwear. The circuit for each foot was arranged so that the output was 0 V at rest, </p><p>Stepping-stones. </p><p>Monitoring footfall. </p><p>156 Journal of Motor Behavior </p><p>Dow</p><p>nloa</p><p>ded </p><p>by [</p><p>McM</p><p>aste</p><p>r U</p><p>nive</p><p>rsity</p><p>] at</p><p> 13:</p><p>15 1</p><p>6 O</p><p>ctob</p><p>er 2</p><p>014 </p></li><li><p>Human Eye Movements </p><p>I I I </p><p>I I I </p><p>I I </p><p>0 </p><p>0 </p><p>0 0 O m 0 </p><p>FIGURE 1. Diagram showing the configuration of the stepping-stones. Filled squares represent targets for left footfall con- tact, unfilled squares targets for right. The arrow indicates direction of walking. </p><p>rising to around 5 V when the foot was in contact with the earthed stepping-stone. </p><p>Two methods of measur- ing eye movement were used simultaneously: electroocu- logruphy (EOG) and infrured reflectometry (IR). </p><p>Electrooculography was used only to measure hori- zontal eye movements. Silver chloride-coated recording electrodes were placed as close to the outer comer of each eye as was practical, and an earthing electrode was placed in the middle of the forehead. To obtain infrared reflectometry, we mounted two infrared transmitter- detector pairs on a pair of lightweight spectacle frames so as to illuminate the nasal and temporal halves of the left eye (Carpenter, 1977). The whole arrangement was placed below the line of sight in the subject's peripheral visual field. The positioning of the emitterdetector is critical in achieving linear and symmetrical output re- cording differentially between the two detectors for left and right eye movements and was adjusted relative to the eye for each individual until such a signal was received. Correct positioning also minimized the effect of vertical eye movements. </p><p>Figure 2 shows a scatter graph of 2,400 consecutive data points taken from a walk lasting 12 s (the same walk illustrated in Figure 3). Clear correlation can be seen be- tween the EOG and IR data (r = .91, N = 2,400) sug- gesting that these two techniques provided an accurate representation of eye movements actually made. </p><p>Monitoring eye movement. </p><p>Eye movement signals obtained by using these two techniques and contact signals for each foot were digi- tized and recorded on tape for later analysis. </p><p>Electronic equipment required for both the eye move- ment and foot contact signals was placed on a mobile trolley that was pushed at an unobtrusive distance be- hind the subjects during the walks. Signals were fed via an umbilicus of screened coaxial cables to an adjacent room containing the digitizing and recording apparatus. </p><p>Subject...</p></li></ul>

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