The effects of object height and visual information on the control of obstacle crossing during locomotion in healthy older adults

The effects of object height and visual information on the control of obstacle crossing during locomotion in healthy older adults

Gait & Posture 55 (2017) 126–130 Contents lists available at ScienceDirect Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost Full l...

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Gait & Posture 55 (2017) 126–130

Contents lists available at ScienceDirect

Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost

Full length article

The effects of object height and visual information on the control of obstacle crossing during locomotion in healthy older adults

MARK



Sho Kunimunea,b, , Shuichi Okadaa a b

Graduate School of Human Development and Environment, Kobe University, 3-11 Tsurukabuto, Nada-ku, Kobe-shi, Hyogo, 657-8501, Japan Department of Rehabilitation, Midorigaoka Hospital, 3-13-1, Makamicho, Takatsuki-shi, Osaka, 569-1121, Japan

A R T I C L E I N F O

A B S T R A C T

Keywords: Vision Obstacle crossing Gait Older adults

In order to safely avoid obstacles, humans must rely on visual information regarding the position and shape of the object obtained in advance. The present study aimed to reveal the duration of obstacle visibility necessary for appropriate visuomotor control during obstacle avoidance in healthy older adults. Participants included 13 healthy young women (mean age: 21.5 ± 1.4 years) and 15 healthy older women (mean age: 68.5 ± 3.5 years) who were instructed to cross over an obstacle along a pressure-sensitive pathway at a selfselected pace while wearing liquid crystal shutter goggles. Participants were evaluated during three visual occlusion conditions: (i) full visibility, (ii) occlusion at T-1 step (T: time of obstacle crossing), and (iii) occlusion at T-2 steps. Toe clearances of both the lead and trail limb (LTC and TTC) were calculated. LTC in the occlusion at T-2 steps condition was significantly greater than that in other conditions. Furthermore, a significant correlation was observed between LTC and TTC in both groups, regardless of the condition or obstacle height. In the older adult group alone, step width in the occlusion at T-2 steps condition increased relative to that in full visibility conditions. The results of the present study suggest that there is no difference in the characteristics of visuomotor control for appropriate obstacle crossing based on age. However, older adults may exhibit increased dependence on visual information for postural stability; they may also need an increased step width when lacking information regarding their positional relationship to obstacles.

1. Introduction In addition to supporting postural stability, gait cycle modulation, and navigation, vision is essential for obstacle avoidance in environments in which humans must coordinate their movement in response to the presence or movement of other objects [1–4]. Crowded living spaces, uneven surfaces, and busy roadways require individuals to continually monitor and avoid obstacles along their paths [3]. In order to prevent trips and/or falls, sufficient toe clearance must be maintained while navigating such environments. Previous studies examining the effect of visual field occlusion on obstacle avoidance determined that visual information is critical for navigating cluttered environments [5–9]. The visual system exerts feedforward control that allows one to adjust the toe clearance of the lead limb based on visual information obtained while approaching an object [5,7]. Timms et al. [10] further reported that visual information obtained at least two steps prior to reaching the obstacle is required to maintain appropriate toe clearance of the lead limb. In contrast, that of the trail limb depends on proprioceptive feedback from the lead limb,



as the trail limb cannot be observed in the visual field [11,12]. However, results regarding the correlation between toe clearance of the lead and trail limbs remain inconsistent [5,7]. Because falls due to tripping increase with age, it is important to clarify potential alterations in visuomotor control experienced by older adults during obstacle crossing to reduce the risk of fall-related injuries. Published data indicate that older individuals increasingly rely on vision for the maintenance of postural stability, while experiencing both decreased gait velocity and longer reaction times in responding to visual stimuli [13–15]. In addition, prolonged single-leg positions are associated with the high risk of falling observed in older adults [12,16,17]. Uiga et al. [18] reported that older individuals tend to look downward more frequently and move their eyes more quickly than young people do. Nevertheless, no studies have investigated the duration of obstacle visibility required for obstacle avoidance. Thus, we aimed to investigate differences in the duration of obstacle visibility required by younger and older participants for appropriate visuomotor control during obstacle avoidance, and to examine the potential mechanisms underlying these differences. We hypothesized

Corresponding author at: Graduate School of Human Development and Environment, Kobe University, 3-11 Tsurukabuto, Nada-ku, Kobe-shi, Hyogo, 657-8501, Japan. E-mail address: [email protected] (S. Kunimune).

http://dx.doi.org/10.1016/j.gaitpost.2017.04.016 Received 14 September 2016; Received in revised form 5 April 2017; Accepted 12 April 2017 0966-6362/ © 2017 Elsevier B.V. All rights reserved.

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equipment (Walk Way MW-1000: Anima Co., Ltd.) was placed along the walking path, which contained one of three different styrofoam obstacles (depth = 5 cm, width = 70 cm, heights = 2.5 cm, 5 cm, and 10 cm) that had been colored red to improve visibility. Obstacles remained unfixed to prevent falls associated with contact. Movements were recorded using a digital camera (HDR-CX590 V: SONY Corp., Tokyo, Japan) located alongside the obstacle. Participants were instructed to cross obstacles with their right foot first so that the right leg was defined as the lead limb. Start position was four or five steps away from the obstacle, and participants were allowed to practice and determine their start positions prior to beginning the experiment [10]. They were also instructed to keep the same walking pace throughout the experiment. Participants wore liquid crystal shutter goggles (S-13031 Takei equipment Co., Ltd.) to allow adjustments to the degree of visual field occlusion (graying of visual field), and walked along a pressure-sensing mat (30 cm × 30 cm) that recorded the pressure associated with each heel contact. The mat was adjusted according to the initial position and walking pattern of each participant. To avoid the influence of stride adjustments, the mat was covered with a thin sheet so that participants could not determine its position. Older participants were equipped with a harness in order to prevent the occurrence of falls. We further confirmed that the harness had no effect on walking speed. Participants were asked to cross obstacles under three different, randomly ordered visual conditions: (i) full visibility, (ii) occlusion at T2 steps, and (iii) occlusion at T-1 step, where T refers to the time of obstacle crossing (Fig. 2). Participants underwent three trials for each condition and each obstacle height (18 perturbed and 18 unperturbed). To avoid the influence of fatigue, participants were provided adequate opportunities for rest as necessary. The fear of visual-field occlusion was evaluated by inquiry.

that young people would determine the appropriate toe clearance based on visual information until two steps before the obstacle, while older individuals would require additional visual information. Thus, even if the field of vision is occluded just prior to the obstacle, they would be unable to plan movements in advance, resulting in higher toe clearance in an attempt to avoid objects of uncertain height. 2. Materials and methods 2.1. Participants Twenty-eight healthy women were divided into two groups: a young adult group (n = 13; mean age = 21.5 ± 1.4 years (range = 19–23 years); mean height = 162.4 ± 3.1 cm; weight = 53.9 ± 6.2 kg) and an older adult group (n = 15; mean age = 68.5 ± 3.5 years (range = 63–74 years); mean height = 156.3 ± 4.7 cm; weight = 51.1 ± 4.2 kg). Since it is necessary to unify the participants’ perception with respect to the height of a certain obstacle, only female participants were recruited to avoid drastic height differences among participants. Participants were recruited from the student population at Kobe University (young) or the Silver Human Resources Center (older). All participants exhibited normal vision, which was confirmed via an evaluation of past medical history, and could walk outdoors without glasses (normal vision and contact lenses only). No participants reported visual difficulties, including those associated with perception of distance, or any neuromuscular/orthopedic disorders that may have affected their participation in the study. Assessment of older participants using the Mini Mental State Examination (MMSE) revealed no significant decline in cognitive function (score = 28.6 ± 2.1, cut off point = 24) [19]. No participants in the older adult group had experienced a fall within the past 6 months. All participants provided written informed consent prior to participation. The present study was approved by the ethics committee at our institution (2014 acceptance number: 118) and conformed to the tenets of the Declaration of Helsinki.

2.3. Data analysis The trial data were converted to image data using motion analysis software (Media Blend: DKH. Co., Ltd, Tokyo, Japan.). Toe clearance of the lead limb (LTC) was defined as the vertical distance from the front edge of the obstacle to the large toe of the lead limb during obstacle crossing. Toe clearance of the trail limb (TTC) was defined as the vertical distance from the front edge of the obstacle to the large toe of the trail limb. Secondary outcome measures included trail foot placement, step length, step width, walking speed, and crossover time for the lead limb. Step length and step width were measured at the point at which the lead limb crossed over the obstacle. Trail foot placement, defined as the distance from the first toe of the left foot to the obstacle at the final step, was calculated using motion analysis software. Other measures were automatically calculated by the gait analysis equipment. Group differences in the results of the TUG and STS were analyzed using independent samples t-tests. Obstacle-crossing parameters were analyzed using a mixed-design analysis of variance model (ANOVA) for

2.2. Protocol We evaluated the physical function of all participants using the Timed Up & Go test (TUG) and Sit to Stand test (STS). In the TUG, mobility was assessed by measuring the time required to stand up from a standard armchair, walk a distance of 3 m, turn around, walk back to the chair, and sit down again. A pressure-sensing mat (T.K.K.5806: Takei Equipment Co., Ltd., Tokyo, Japan) located on the seat of the chair was used to collect data. In the STS, participants were asked to stand up 10 times with their arms folded on the same pressure-sensing mat. Each assessment was performed twice, and the shorter times were chosen as the representative values for each participant. Participants were then asked to walk along a pathway containing an obstacle at a self-selected pace, cross over the obstacle, and continue walking for at least five additional steps (Fig. 1). Gait analysis

Fig. 1. Experimental environment. The mat was covered with a sheet in order to prevent adjustments in stride that may have occurred due to the perception of the mat.

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obstacle heights (Fig. 3). Furthermore, a significant correlation between LTC and TTC was observed in both groups regardless of condition or obstacle height (Table 2). 3.5. Secondary outcome measures Step width exhibited an interaction between age and visual condition (F(2,208) = 5.22, p < 0.01). In the older adult group, step width in the occlusion at T-2 steps condition was significantly greater than in the full visibility condition (p < 0.01). No main effect of age or interaction was observed for other measurement items.

Fig. 2. Visual conditions. The different visual conditions are shown: (i) full visibility: full field of view throughout walking; (ii) occlusion at T-1 step: visual field occluded one step before obstacle; (iii) occlusion at T-2 steps: visual field occluded two steps before obstacle. T: time of obstacle crossing. R: right foot; L: left foot.

4. Discussion The present study aimed to investigate the difference between healthy young and older participants with regard to the duration of obstacle visibility required for appropriate visuomotor control during obstacle avoidance, and to examine the potential mechanisms underlying these differences. The results of the TUG and STS experiments, like those of previous studies [13,20,21], indicated an association between decreases in physical ability and aging, although all participants in the present study exhibited relatively high physical function. Furthermore, our results suggest that the observed differences in performance were not due to psychological factors, as participants reported little fear during the occlusion conditions. We observed an association between LTC and occlusion condition. There was no interaction between age and visual condition, and similar effects of visual condition on LTC were obtained for both the young and older adult groups. The observed increases in LTC in the occlusion at T2 steps condition align with the results of previous studies involving young adults, in which recognition of final foot-placement in the lower visual field is associated with control of toe clearance, and that the trajectory of the lead limb is planned at least two steps prior to reaching the obstacle via a feedforward control mechanism [10]. In the occlusion at T-2 steps condition, neither younger nor older adults were able to identify the relative positions of their trail foot and the obstacle, which may have resulted in a slight increase in toe clearance. LTC was greater in older adults than in younger adults. Some studies have reported that toe clearance increases with age due to declining muscle strength, mobility, and ability to perceive position [16,22]. Accordingly, we hypothesized that, although older people can recognize the positional relationship between themselves and obstacles in the same timeframe as younger people, high toe clearance may be adopted as a strategy for enhancing safety to avoid falls or to compensate for age-related changes in positional perception. We did observe an interaction between age and visual condition with regard to TTC. TTC in young participants was similar to LTC, and was significantly greater in the occlusion at T-2 steps condition than in the other conditions. In contrast, TTC was significantly greater for older adults in the occlusion at T-2 steps condition than in the full visibility condition. There was no significant difference in TTC between the occlusion at T-1 step and occlusion at T-2 steps conditions in older participants; however, significant correlations were observed between LTC and TTC in both groups. Our findings differ from those of a previous study in which age and walking speed had no influence on TTC [12]. However, these authors did not investigate LTC, leaving the relationship between TTC and LTC to be determined. Therefore, our results align with those of reports suggesting that TTC is coordinated and determined by motor planning during the approach phase, as well as by motor feedback regarding LTC [11,15]. Previous studies have also suggested that participants have difficulty controlling the trajectory of the trail limb in altered visual field conditions [11,12,15]. Although LTC and TTC were correlated in the occlusion at T-1 step condition, the level of attention paid to postural stability during obstacle crossing may have differed among participants of the older adult group. This may have influenced the degree of TTC, thereby resulting in a lack of

age (×2), visual condition (×3), and obstacle height ( × 3). Bonferroni correction for multiple comparisons was utilized for post hoc analysis. Paired t-tests and Pearson’s correlation coefficient were then used to compare LTC and TTC. All statistical analyses were conducted using SPSS Version 23.0J (IBM Corp., Japan), and the level of significance was set at p < 0.05. 3. Results 3.1. TUG, STS, and fear of obstacle crossing Results of the TUG and STS indicated that young adults exhibited significantly greater physical function than older adults for all measures (TUG: t = 3.10, p < 0.05; STS: t = −4.93, p < 0.01) (Table 1). No participants reported any fear of obstacle crossing. 3.2. LTC For LTC, significant main effects of age (F(1,26) = 9.41, p < 0.05) and visual condition (F(2,208) = 36.26, p < 0.01) were observed. LTC was significantly greater in the older adult group than in the younger group (p < 0.05). This difference was more pronounced in the occlusion at T-2 steps condition than in the full visibility (p < 0.01) and occlusion at T-1 step conditions (p < 0.01). 3.3. TTC For TTC, an interaction between age and visual condition was observed (F (2,208) = 6.70, p < 0.05). TTC was significantly greater in the older adult group than in the young adult group (p < 0.05). For young people, TTC was significantly greater in the occlusion at T-2 steps condition than in the full visibility (p < 0.01) and occlusion at T1 step conditions (p < 0.01). In contrast, TTC was significantly greater for older adults in the occlusion at T-2 steps condition than in the full visibility condition only (p < 0.05). Additionally, a main effect of obstacle height was observed (F(2,208) = 16.20), and TTC was significantly greater for obstacle heights of 2.5 cm than for obstacle heights of 5 cm (p < 0.05) and 10 cm (p < 0.01). 3.4. Correlations between LTC and TTC LTC was significantly greater than TTC in all conditions and for all Table 1 Physical function of participants.

TUG (second) STS (second)

Young adults

Older adults

P value

5.12 ± 0.73 11.10 ± 1.87

5.99 ± 0.74 17.64 ± 4.73

< 0.05 < 0.01

Average and comparison between younger and older adults are shown for TUG and STS. TUG: Timed Up & Go test; STS: Sit to Stand test.

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Fig. 3. The results of toe clearance. Average and standard error for LTC (left column) and TTC (right column) are shown with respect to each obstacle height. The three visual conditions are represented as follows: (i) full visibility, (ii) occlusion at T-1 step, and (iii) occlusion at T-2 steps. T: time of obstacle crossing; LTC: toe clearance of the lead limb; TTC: toe clearance of the trail limb. Table 2 Correlation between LTC and TTC. Conditions Obstacle height (cm) Young adults Older adults

Full visibility 2.5

5 **

.84 .84**

Occlusion at T-1 step 10

*

.62 .72**

2.5 *

.59 .75**

5 **

10 *

.82 .79**

Occlusion at T-2 steps

.57 .69**

2.5 *

.60 .79**

5 **

.75 .82**

10 *

.52 .58*

.72** .67**

: p < 0.05, **: p < 0.01. The correlation coefficient between LTC and TTC at each condition and height of each obstacle is shown. T: time of obstacle crossing; LTC: toe clearance of the lead limb; TTC: toe clearance of the trail limb.

*

trail limb may correspond with that of the lead limb in conditions during which working memory and proprioception are maintained, suggesting that working memory is more important than visual information in adjusting LTC and TTC. However, further studies are required to assess the function of working memory in relation to use of visual information during obstacle crossing. Previous studies have revealed that dependence on vision for maintaining postural stability increases with age [13,14]. In the present study, step width was greater in the occlusion at T-2 steps condition than in the remaining conditions for older adults. For older individuals, stepping over obstacles forces individuals to adopt a single-leg stance for a longer period of time, which may lead to postural instability [16,25]. Novack et al. [26] reported that older adults exhibited greater postural instability on the side of obstacle crossing than young people. Other researchers have therefore suggested that older adults adopt a strategy in which they widen the base of support in order to combat instability [27]. Our findings suggest that this strategy was adopted in the final step before reaching the obstacle, when participants were unable to identify the relative positions of their trail foot and the obstacle. Consequently, visual occlusion may have affected lateral stability in older participants. Participants practiced to determine their starting position and ascertain the existence of obstacles in advance, allowing them to walk at a constant pace and step in the same location via feedforward control. Thus, this may have resulted in motor learning, which may

significant difference between the T-1 and other conditions. In addition, we observed that TTC decreased with increasing obstacle height, and that there was no interaction between visual condition and obstacle height in the young adult group, consistent with the findings of previous studies [10,11]. Our findings extend the results of previous work, as we observed this result for older adults as well. However, in the present study, we used an obstacle height of 10 cm, as a previous study reported that older adults exhibited difficulties crossing objects of 8 cm or higher [14]. Patla et al. [7] used obstacles with heights up to 26 cm. We believe that our results may therefore be more applicable to daily life. We also observed that TTC was lower than LTC in the present study, consistent with the results of a study by Patla et al. [7], in which falls tended to occur when the trail limb failed to step over an obstacle. A significant correlation was observed between LTC and TTC, indicating that if the motion of the lead limb is appropriate and LTC is sufficient, missteps of the trail limb can be prevented. However, no consensus regarding the relevance of LTC and TTC has been reached. Heijhem et al. [23] and Lajoie et al. [24] further suggested that planning of movements may be associated with stored visual information regarding the shape and position of the obstacle, indicating the importance of working memory in obstacle crossing. Haijhem et al. [23] reported that movement of the trail limb is performed according to memory in the approach phase, and according to positional information of the extremities during obstacle crossing. Consequently, movement of the 129

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have influenced visuomotor control during the experimental conditions. Previous studies have reported that older individuals exhibit delayed responses to the sudden appearance of obstacles [14–16], and that eye movements and obstacle crossing may improve following intervention [18]. Therefore, our findings may be more applicable to familiar than non-familiar settings. A final limitation worth consideration is that in order to unify the participants’ perception with respect to the height of a certain obstacle, only female participants of similar height were chosen. As no reports to date have been published regarding gender differences in the use of visual information during obstacle crossing, future research should focus on investigating such differences. Furthermore, reports have indicated that older adults with fall experiences and a higher risk of falls differ from healthy individuals in terms of eye movements and obstacle avoidance [18]. Thus, further studies should evaluate eye movement in older adults with previous falls and those at high risk for falling.

[10]

5. Conclusion

[15]

[7]

[8]

[9]

[11]

[12] [13]

[14]

Our findings suggest that there are no differences in patterns of visually-guided obstacle crossing when walking at a constant pace or in a familiar environment between healthy young and older adults, and that feedforward control is utilized for determination of appropriate LTC in both groups. However, older individuals may exhibit increased dependence on visual information for postural stability, adopting an increased step width during conditions of instability.

[16] [17] [18]

[19]

Conflict of interest

[20]

None.

[21]

Acknowledgments

[22]

We would like to thank all who participated in this study and Editage (www.editage.jp) for English language editing.

[23]

References

[24]

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