- Email: [email protected]
Role of impaired vision during dual-task walking in young and older adults
Accepted Manuscript Title: ROLE OF IMPAIRED VISION DURING DUAL-TASK WALKING IN YOUNG AND OLDER ADULTS Authors: V. Krishnan, Y. Cho, O. Mohamed PII: DOI: Reference:
S0966-6362(17)30229-1 http://dx.doi.org/doi:10.1016/j.gaitpost.2017.06.006 GAIPOS 5452
To appear in:
Gait & Posture
Received date: Revised date: Accepted date:
19-8-2016 18-5-2017 9-6-2017
Please cite this article as: Krishnan V, Cho Y, Mohamed O.ROLE OF IMPAIRED VISION DURING DUAL-TASK WALKING IN YOUNG AND OLDER ADULTS.Gait and Posture http://dx.doi.org/10.1016/j.gaitpost.2017.06.006 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ROLE OF IMPAIRED VISION DURING DUAL-TASK WALKING IN YOUNG AND OLDER ADULTS Krishnan V1*, Cho Y2*, and Mohamed O1 1 2
Department of Physical Therapy, California State University Long Beach, CA, 90840 United States Department of Psychology, California State University Long Beach, CA, 90840 United States
*
Both authors contributed equally to the manuscript
Corresponding Author Vennila Krishnan, PT, PhD Associate Professor Director, Clinical Rehabilitation And Biomechanics (CRAB) Laboratory Department of Physical Therapy, ET 118 1250 Bellflower Blvd California State University Long Beach, CA 90840 Phone: 562-985-4155 Fax: 562-985-4069 Email: [email protected] Conflict of interest statement The authors do not have any financial or personal relationships with other people or organizations that could inappropriately influence their work. HIGHLIGHTS
Higher dual-task walking cost was seen with simulated impaired vision and in older adults Higher dual-task cognitive cost was seen with simulated impaired vision, but not with aging When faced with simulated impaired vision, both young and older adults prioritize walking over cognition Future work should aim to evaluate this finding in adults with real visual impairment
ABSTRACT While cognitive-motor interference in dual-task activities is well established, it is still unknown how such interference is influenced by concurrent visual challenges. Nineteen communitydwelling healthy, cognitively intact, older adults (Mean ± SD = 71.45 ± 1.25 years, 6 males) and nineteen young adults (Mean ± SD = 22.25 ± 0.68 years, 4 males) performed a cognitive-singletask (serial subtraction by 3), a walking-single-task and a cognitive-walking-dual-task under normal, blurred and peripheral-vision-loss conditions (artificially imposed using goggles). Gait parameters and the number of correct responses were measured. Dual task costs for both walking 1
and cognition were computed. Results showed that higher walking cost was seen with impaired vision (p = .05) and with older adults (p = .03); greater cognitive cost was seen with impaired vision (p = .01), but no difference in cognitive cost was seen between young and older adults. Thus, when faced with impaired vision, both young and older adults appear to allocate less attention to cognition than to walking, and thus prioritize walking. Future work should explore whether dual-task training under visual challenge could reduce cognitive-motor interference and reduce fall risks in older adults. Keywords: dual-task cost; vision; cognitive-motor interference; prioritization; elderly
2
INTRODUCTION Dual-tasking is the ability of the brain to perform tasks that have different attentional demands and to perform two tasks at once [1]. For example, walking (motor challenge) and simultaneously thinking (cognitive challenge) could cause a cognitive-motor interference (CMI) that might affect performance in either of the tasks or both tasks [2]. CMI could be determined by the reduced dualtask (DT) performance compared to the single-task (ST) performance, represented as a cost for walking (walking cost) and as a cost for cognition (cognitive cost) [2, 3]. For example, CMI in walking performance could be reflected by a slow gait speed, shorter stride length, reduced cadence, increased stride duration, and longer double limb support phases. When older adults perform a simultaneous cognitive task, they exhibit both increased walking and cognitive costs [46], which were associated with increased risk of falling [6, 7]. Several studies have shown that impaired vision such as blurred vision and peripheral-vision-loss causes deterioration in postural control [8] and in walking [9-11]. Other studies have shown that blurred vision that reduces visual acuity, edge contrast sensitivity, and depth perception tends to result in greater risk for loss of balance while walking [12] and cause many accidents in older adults [13, 14]. Recently, studies have shown that peripheral vision is needed to stabilize anteriorposterior sway while standing [15, 16] as well as to establish an accurate representation of spatial structure while walking [9]. Glaucoma, one of the most common causes of irreversible blindness worldwide in older adults due to ARD (age-related-decline) causes a reduction in the peripheral field of view [1, 15] and problems with peripheral vision affect the stability of walking [9, 10]. Many studies have used dual-task paradigms to investigate postural control under impaired vision [17, 18]. In a study with healthy older adults, an addition of a cognitive secondary task combined with an artificially induced blurred vision produced an imbalance while standing [18]. However, it is still unknown how such visual impairment may affect CMI associated with dual-task during walking, especially in older adults. For example, walking-and-talking while road-crossing involves processing multiple types of information that requires greater cognitive resources than walking or talking alone and thus will be greatly affected by visual impairment. Thus, the purpose of this study is to investigate the effect of concurrent visual impairment like blurred vision and peripheral-vision-loss on CMI during dual-task walking in young and older adults. We hypothesized that a greater walking cost would be associated with vision and age (Hypothesis 1). 3
Specifically, in blurred vision and peripheral-vision-loss and in older adults, the walking cost would be increased. We also hypothesized that a greater cognitive cost would be associated with impaired vision and age (Hypothesis 2). METHODS Nineteen healthy young adults (Mean ± SD = 22.25 ± 0.68 years, 4 males) and nineteen healthy older adults (Mean ± SD = 71.45 ± 1.25 years, 6 males) participated in the study. Young participants were recruited from the California State University, Long Beach, while the older adults were recruited from a senior center in Long Beach. All the older adults lived independently in the community. Participants were excluded from this study if they had one or more of the following: uncorrected secondary eye pathologies, history of neurological disorders, orthopedic deficits of the lower extremity, depression, assistance with activities of daily living (ADL), morbidly obese, hip or knee replacements, and auditory or vestibular pathologies. We also excluded the participants with cognitive impairment (evidenced by a score of less than 26 on the mini‐cog) [19]. We obtained informed consent forms and the experiment was conducted according to the Declaration of Helsinki [20]. Equipment Temporal and spatial parameters of gait were recorded using the ZenoMat ‘Platinum’ 16-ft electronic walkway and the Protokinetics Movement Analysis Software (PKMAS - ProtoKinetics, Havertown, PA) that has sensors embedded into a 16*2 feet mat. The following gait characteristics were assessed: step length, stride length, stride width, gait velocity, double limb support time, gait cycle time, gait cycle time coefficient of variation (CV), gait velocity and cadence. The three vision conditions were simulated using customized laboratory googles (See Fig.1): normal vision (NV – participants wore a plain laboratory goggle), blurred vision (BV - participants wore a laboratory goggle blurred by frosted glass paint) and peripheral-vision-loss (PVL - participants wore a laboratory google with peripheral vision occluded by black tape). < Figure 1 is about here> A cognitive challenge targeting working memory was introduced by asking the subjects to subtract 3 from a 3-digit number. A different 3-digit number was used as a starting point whenever the cognitive task was administered across different conditions. The number of correct responses in 20 s was recorded using the Audacity sound recording software (version 2.1.2) [21]. Experimental Procedure 4
Participants performed both single and dual-tasks (see Fig.2). Block A consisted of a cognitive single task – serial subtraction by 3, (i.e., performing a cognitive task while sitting) that was performed three times in all three visual conditions in a random order. Block B consisted of walking single task, i.e., walking on the ZenoMat at normal speed without performing any cognitive challenge. The participants walked across the mat, turned and walked back to the starting position, starting and ending the walk 1.5m away from the edge of the mat. The walking singletask was also performed three times, one in each vision condition. Both block A and B were counterbalanced across the participants. Block C consisted of dual-tasking (i.e., walking while performing a cognitive task), also under three visual conditions in a random order. Participants first received standardized instructions on how to perform the cognitive task followed by one familiarization trial. An interval of 15 minutes was provided between single-task and dual-task conditions. The experiment took about 35-55 minutes. < Figure 2 is about here> Data Analysis We computed the dual-task cost, which is the change in dual-task compared to the same singletask performance separately using the following formula [22]. Dual-task cost = 100* (single task-dual task)/single task The formula shows that the difference between single task and dual task is normalized by the single task performance. Specifically, walking cost was computed using the gait parameters between STwalking and DT-walking on the following gait variables: step length, stride length, velocity, cadence, step width, double support time, gait cycle time, and coefficient of variation of gait cycle time. Cognitive cost was computed using the number of correct responses between ST-cognitive and DT-cognitive. Statistical Analysis Two-way mixed MANOVA was used to compare the effects of age (young vs older) and vision (NV vs BV vs PVL) and their interaction on walking cost for the following gait parameters (Hypothesis #1): step length, stride length, velocity, cadence, step width, double support time, gait cycle time, and coefficient of variation of gait cycle time. A significant result was followed by univariate ANOVAs with correction for Type I error. A parallel two-way mixed ANOVA was used to compare the age and vision and their interactive effects on cognitive cost (Hypothesis #2). 5
For a baseline cognition comparison, we also performed a two-way mixed ANOVA to understand the main effect of age and vision and their interaction effects on the number of correct responses during the single task cognitive performance. For vision, whenever the Mauchly’s test of sphericity was not met, Green-House-Geiser correction was made. Post-hoc analysis with Bonferroni correction was used for further comparisons within the three visual conditions. The statistical significance was set at p < 0.05 in all the other tests, and for the univariate ANOVAs with Type I error correction, the significance was set at p < 0.025. Statistical analysis was performed in SPSS version 24.0, Chicago, IL. RESULTS Our first hypothesis was partially supported: there was a greater walking cost associated with impaired vision and older age, but not a significant interaction. A mixed 2-way MANOVA on the gait variables revealed a significant main effect of vision [Wilk’s λ = 0.38, F(16,21) = 2.17, p = .05, η2 = 0.62] and a significant main effect of age [Wilk’s λ = 0.59, F(8,29) = 2.54, p = .03, η2 = 0.41], without any interaction (p = .07). To control for the inflation of Type I error for the follow-up Univariate ANOVAs, we created two groups of gait variables, one for the family of four spatial gait variables and the other for the family of four temporal gait variables. We set the alpha level of each family-wise analysis to be .10, and applied Bonferroni correction to set the alpha level of each Univariate ANOVA to be .10/4 = .025 [23]. The results of the univariate ANOVA for the vision did not show any significance. The results of the univariate ANOVA for the age (young vs. old) were as follows: step length (p = .03), stride length (p = .025), cycle time (p = .01), velocity (p = .02), cadence (p = .01). Figure 3 shows the walking cost of the gait parameters for the young and older adults. < Figure 3 is about here> Our second hypothesis that a greater cognitive cost would be associated with impaired vision and age, was also partially supported. Both impaired vision conditions compared to the normal vision showed a greater cognitive cost, but surprisingly there were no age-related differences. A mixed 2-way ANOVA revealed a significant main effect of vision alone [F(2,60) = 5.76, p = .01] and did not show any effect of age or interaction (Fig.4A). The post-hoc analysis on vision using Bonferroni correction showed the NV condition significantly different from the BV (p = .01) and from the PVL conditions (p = .03). There was no difference between BV and PVL conditions, 6
suggesting that the cognitive cost increased with impaired vision in both young and older adults. To demonstrate that impaired vison did not affect the cognitive ST performance, but affected the cognitive performance while walking, we analyzed the effects of vision (and age) on the cognitive ST performance. The number of correct responses during ST cognitive for the young and older adults is shown in Fig 4B. A mixed 2-way ANOVA revealed a significant main effect of age [F(1,31) = 7.03, p = .01], but did not show any effect of either vision or interaction on the number of correct responses. Specifically, older adults had reduced number of correct responses when compared to young adults in all the vision conditions during the serial subtraction tests conducted during sitting. Taken together, these results seem to suggest that both groups have prioritized walking compared to cognition during DT under impaired vision, resulting in increased cognitive cost with impaired vison which did not exist in the cognitive ST. To gauge the potential practice effect in performing serial subtraction task multiple times across different vision conditions, we focused on the serial subtraction responses under the single task and rearranged them in the order of performance regardless of vision condition (which was possible because the vision condition was counterbalanced). Then we applied a paired samples ttest to compare the cognitive performance between trial 1 and trial 2 and the one between trial 2 and trial 3 for all subjects (young and older adults combined). The results did not show a significant difference between trial 1 and trial 2 [t(39) = .31, p = .76], and between trial 2 and trial 3 [t(40) = .32, p = .75]. Figure 4B also shows that we did not see any practice effect between single task and dual task, as both groups did not improve their cognitive performance in the dual task. < Figure 4 is about here> DISCUSSION This study investigated the effects of concurrent visual impairment like blurred vision and peripheral-vision-loss on CMI during dual-task walking in young and older adults. The results showed that while impaired vision and older age increased the walking cost, surprisingly only impaired vision increased the cognitive cost. During dual-task walking, when interrupted with vision, both young and older adults let cognition suffer, thus prioritizing walking. Walking Cost As expected, DT was harder compared to ST, and the walking cost increased with aging and with visual impairment. ARD increases gait and balance disorders from around 10% between the ages 7
of 60 and 69 years to more than 60% in those over 80 years [24]. The existence of walking cost in older adults from our study is consistent with the findings of previous studies [4, 5, 21]. It corroborates the common consensus that ARD makes it difficult for older adults to share attention in dual-task conditions [17, 25]. With an addition of visual impairment, sharing of attention becomes even more difficult, resulting in increased CMI. Our study, for the first time, found a greater decline in walking performance in DT with an additional visual challenge in older adults, and further underscore the importance of impaired vision as an added risk factor on walking while performing another task. Cognitive Cost In the single-cognitive task, our results showed large age differences in the raw cognitive performance (the number of correct responses). However, the cognitive cost (that captures the cost in cognition with added walking) did not change with age, but with impaired vision. The increased cognitive cost in impaired vision conditions in both groups may be linked to a reliance on the use of vision to guide walking in DT, in general. For example, to move safely we require visual identification of where we walk and to place our foot. Therefore, it is possible that when faced with blurred and peripheral-vision-loss, both young and older adults appear to allocate less attention to cognition, while prioritizing walking over cognition to overcome the difficulties associated with walking and foot placement. This confirms that impaired vision places greater demand on the available processing resources, thus forcing both young and older adults to concentrate on ‘posture-first’ strategy [22]. In a study by Oh-Park et al., older adults, when walking while carrying a tray, paid more attention to walking than to the tray, even when asked to pay attention to the tray, supporting the ‘posture-first’ strategy, as compared to the young adults [26]. In our study, under impaired vision conditions, both older and young adults allocated more attention to walking than to cognition. However, the cognitive cost (with impaired vision and during DT) did not show any age effect. The lack of age effect on cognitive cost in our study is in line with a previous study, though they employed stroop task while walking, while we employed serial subtraction task while walking [3]. Loss of Vision Impaired vision may pose significant challenges to an individual who is walking with a simultaneous cognitive challenge. While we found that both blurred vision and peripheral-visionloss caused greater walking cost as well as cognitive cost, we did not see any specific differences 8
between the two artificially imposing impaired conditions. Very few experimental studies have assessed the role of impaired vision such as blurred or peripheral vision loss while walking [9, 27]. When young healthy adults with simulated cataracts walked across a curved pathway, gait speed decreased in dim light but not in full light [27]. Another study showed that low light vision resulted in increased variability in gait performance and a reduced walking speed [28]. Few other studies have shown that peripheral-vision-loss may be predominant in the anterior-posterior balance control, providing support to the ‘peripheral dominance theory’ during standing [16, 29]. One study related to walking suggested that peripheral vision is important for establishing and/or updating an accurate representation of spatial structure for navigation [9]. In their study, participants drifted off course while walking when they had a peripheral visual field loss. Our study extends the evidence of the importance of peripheral vision in walking performance itself, rather than the walking course, especially when challenged by a simultaneous cognition task. Limitation In our study, participants performed the single tasks first and performed each ST and DT tasks across different visual conditions. The repetition might induce practice effect, which is particularly important for a cognitive task. However, we did not see any statistically significant practice effect enough to improve performance in the DT cognitive tasks with impaired vision. We also did not assess single task performance of the visual task because of the complexity involved working with the vision charts and computing the vision cost. It could definitely be a future work. One more limitation is that the results of this study cannot be transferable to older populations with actual visual impairments, who might have developed alternative strategies to overcome their visual impairments [30]. Conclusion This study examined CMI (as assessed separately by walking and cognitive costs) during dualtask walking in young and older adults, under normal, blurred and peripheral-vision-loss conditions. Higher walking performance cost was seen in older adults and with impaired vision. In contrast, both young and older adults exhibited prioritization of walking over cognitive performance during blurred vision and peripheral-vision-loss. These results provide new information on how young and older adults distribute their attention to cope with the increased motor and cognitive challenges associated with DT under impaired sensory information. Future
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work should explore whether dual-task training under visual challenge could reduce cognitivemotor interference and reduce fall risks in older adults.
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FIGURE CAPTIONS Fig.1. The letters provide a simulation of the three visual conditions received by the participants. NV is the normal vision, BV is the blurred vision and PVL is the peripheral-vision-loss conditions. Fig. 2. Single Task (ST) and Dual Task (DT) conditions. (A) ST cognitive serial subtraction task was performed in sitting under normal, blurred and peripheral-vision-loss conditions. (B) ST walking was performed under normal, blurred and peripheral-vision-loss conditions. (C) DT cognitive serial subtraction task was performed while walking under normal, blurred and peripheral-vision-loss conditions. Fig. 3. Dual-task walking cost for all the gait parameters. A positive walking cost in the spatial parameters (step length, stride length, velocity, cadence) and a negative walking cost in the temporal parameters (double support time, gait cycle time, gait cycle time CV) of gait indicate reduced performance in the dual tasks compared to single tasks. Error bars indicate standard deviations (SDs) of the mean. The figure shows an increased walking cost for the older adults. Significance level was set at p < 0.025 (indicated by *). Fig. 4. Cognitive performance: (A) Figure shows a decline in the performance of number of correct responses during cognitive single task in older adults. (B) Dual-task cognitive cost (indicating reduced performance in dual task compared to cognitive single task) is increased with impaired vision (BV and PVL) in both the groups. Error bars indicate standard deviations (SDs) of the mean. Significance level was set at p < 0.05 (indicated by *). Acknowledgement This study was supported in part by HOGAR grant from CSU, Long Beach to Dr. Krishnan in 2015. The authors thank Meagan Suen, Trong Pham, Alica Pech Corrales, Babken Sarkissian, Emily Nichols and Daniela Gonzalez for their help in data collection and analysis.
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REFERENCES [1] Kotecha A, Chopra R, Fahy RT, Rubin GS. Dual tasking and balance in those with central and peripheral vision loss. Invest Ophthalmol Vis Sci. 2013;54:5408-15. [2] Patel P, Lamar M, Bhatt T. Effect of type of cognitive task and walking speed on cognitive-motor interference during dual-task walking. Neuroscience. 2014;260:140-8. [3] Plummer-D'Amato P, Brancato B, Dantowitz M, Birken S, Bonke C, Furey E. Effects of gait and cognitive task difficulty on cognitive-motor interference in aging. J Aging Res. 2012;2012:583894. [4] Theill N, Martin M, Schumacher V, Bridenbaugh SA, Kressig RW. Simultaneously measuring gait and cognitive performance in cognitively healthy and cognitively impaired older adults: the Basel motorcognition dual-task paradigm. J Am Geriatr Soc. 2011;59:1012-8. [5] Hausdorff JM, Schweiger A, Herman T, Yogev-Seligmann G, Giladi N. Dual-task decrements in gait: contributing factors among healthy older adults. J Gerontol A Biol Sci Med Sci. 2008;63:1335-43. [6] Verghese J, Buschke H, Viola L, Katz M, Hall C, Kuslansky G, et al. Validity of divided attention tasks in predicting falls in older individuals: a preliminary study. J Am Geriatr Soc. 2002;50:1572-6. [7] Tinetti ME, Speechley M, Ginter SF. Risk factors for falls among elderly persons living in the community. N Engl J Med. 1988;319:1701-7. [8] Mohapatra S, Krishnan V, Aruin AS. The effect of decreased visual acuity on control of posture. Clinical Neurophysiology. 2012;123:173-82. [9] Turano KA, Yu D, Hao L, Hicks JC. Optic-flow and egocentric-direction strategies in walking: central vs peripheral visual field. Vision Res. 2005;45:3117-32. [10] Turano KA, Rubin GS, Quigley HA. Mobility performance in glaucoma. Invest Ophthalmol Vis Sci. 1999;40:2803-9. [11] Kuyk T, Elliott JL, Fuhr PS. Visual correlates of obstacle avoidance in adults with low vision. Optom Vis Sci. 1998;75:174-82. [12] Winter DA. Biomechanics and motor control of human movement: John Wiley & Sons; 2009. [13] Miyasike-daSilva V, McIlroy WE. Does it really matter where you look when walking on stairs? Insights from a dual-task study. PLoS One. 2012;7:e44722. [14] Young WR, Hollands MA. Can telling older adults where to look reduce falls? Evidence for a causal link between inappropriate visual sampling and suboptimal stepping performance. Exp Brain Res. 2010;204:103-13. [15] Nougier V, Bard C, Fleury M, Teasdale N. Contribution of central and peripheral vision to the regulation of stance: developmental aspects. J Exp Child Psychol. 1998;68:202-15. [16] Lestienne F, Soechting J, Berthoz A. Postural readjustments induced by linear motion of visual scenes. Exp Brain Res. 1977;28:363-84. [17] Yeh TT, Cluff T, Balasubramaniam R. Visual reliance for balance control in older adults persists when visual information is disrupted by artificial feedback delays. PLoS One. 2014;9:e91554. [18] Anand V, Buckley JG, Scally A, Elliott DB. Postural stability in the elderly during sensory perturbations and dual tasking: the influence of refractive blur. Invest Ophthalmol Vis Sci. 2003;44:288591. [19] Borson S, Scanlan JM, Watanabe J, Tu SP, Lessig M. Simplifying detection of cognitive impairment: comparison of the Mini-Cog and Mini-Mental State Examination in a multiethnic sample. J Am Geriatr Soc. 2005;53:871-4. [20] World Medical A. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310:2191-4. [21] Beauchet O, Dubost V, Herrmann FR, Kressig RW. Stride-to-stride variability while backward counting among healthy young adults. J Neuroeng Rehabil. 2005;2:26.
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[22] Kelly VE, Janke AA, Shumway-Cook A. Effects of instructed focus and task difficulty on concurrent walking and cognitive task performance in healthy young adults. Exp Brain Res. 2010;207:65-73. [23] Keppel G. Design and analysis: A researcher's handbook: Prentice-Hall, Inc; 1991. [24] Mahlknecht P, Kiechl S, Bloem BR, Willeit J, Scherfler C, Gasperi A, et al. Prevalence and burden of gait disorders in elderly men and women aged 60-97 years: a population-based study. PLoS One. 2013;8:e69627. [25] Lacour M, Bernard-Demanze L, Dumitrescu M. Posture control, aging, and attention resources: models and posture-analysis methods. Neurophysiol Clin. 2008;38:411-21. [26] Oh-Park M, Holtzer R, Mahoney J, Wang C, Raghavan P, Verghese J. Motor dual-task effect on gait and task of upper limbs in older adults under specific task prioritization: pilot study. Aging Clin Exp Res. 2013;25:99-106. [27] Elliott DB, Bullimore MA, Patla AE, Whitaker D. Effect of a cataract simulation on clinical and real world vision. Br J Ophthalmol. 1996;80:799-804. [28] Moe-Nilssen R, Helbostad JL, Akra T, Birdedal L, Nygaard HA. Modulation of gait during visual adaptation to dark. J Mot Behav. 2006;38:118-25. [29] Amblard B, Carblanc A. Role of foveal and peripheral visual information in maintenance of postural equilibrium in man. Perceptual and Motor Skills. 1980;51:903-12. [30] Edwards AS. Body sway and vision. J Exp Psychol. 1946;36:526-35. Figure Caption
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S0966-6362(17)30229-1 http://dx.doi.org/doi:10.1016/j.gaitpost.2017.06.006 GAIPOS 5452
To appear in:
Gait & Posture
Received date: Revised date: Accepted date:
19-8-2016 18-5-2017 9-6-2017
Please cite this article as: Krishnan V, Cho Y, Mohamed O.ROLE OF IMPAIRED VISION DURING DUAL-TASK WALKING IN YOUNG AND OLDER ADULTS.Gait and Posture http://dx.doi.org/10.1016/j.gaitpost.2017.06.006 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ROLE OF IMPAIRED VISION DURING DUAL-TASK WALKING IN YOUNG AND OLDER ADULTS Krishnan V1*, Cho Y2*, and Mohamed O1 1 2
Department of Physical Therapy, California State University Long Beach, CA, 90840 United States Department of Psychology, California State University Long Beach, CA, 90840 United States
*
Both authors contributed equally to the manuscript
Corresponding Author Vennila Krishnan, PT, PhD Associate Professor Director, Clinical Rehabilitation And Biomechanics (CRAB) Laboratory Department of Physical Therapy, ET 118 1250 Bellflower Blvd California State University Long Beach, CA 90840 Phone: 562-985-4155 Fax: 562-985-4069 Email: [email protected] Conflict of interest statement The authors do not have any financial or personal relationships with other people or organizations that could inappropriately influence their work. HIGHLIGHTS
Higher dual-task walking cost was seen with simulated impaired vision and in older adults Higher dual-task cognitive cost was seen with simulated impaired vision, but not with aging When faced with simulated impaired vision, both young and older adults prioritize walking over cognition Future work should aim to evaluate this finding in adults with real visual impairment
ABSTRACT While cognitive-motor interference in dual-task activities is well established, it is still unknown how such interference is influenced by concurrent visual challenges. Nineteen communitydwelling healthy, cognitively intact, older adults (Mean ± SD = 71.45 ± 1.25 years, 6 males) and nineteen young adults (Mean ± SD = 22.25 ± 0.68 years, 4 males) performed a cognitive-singletask (serial subtraction by 3), a walking-single-task and a cognitive-walking-dual-task under normal, blurred and peripheral-vision-loss conditions (artificially imposed using goggles). Gait parameters and the number of correct responses were measured. Dual task costs for both walking 1
and cognition were computed. Results showed that higher walking cost was seen with impaired vision (p = .05) and with older adults (p = .03); greater cognitive cost was seen with impaired vision (p = .01), but no difference in cognitive cost was seen between young and older adults. Thus, when faced with impaired vision, both young and older adults appear to allocate less attention to cognition than to walking, and thus prioritize walking. Future work should explore whether dual-task training under visual challenge could reduce cognitive-motor interference and reduce fall risks in older adults. Keywords: dual-task cost; vision; cognitive-motor interference; prioritization; elderly
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INTRODUCTION Dual-tasking is the ability of the brain to perform tasks that have different attentional demands and to perform two tasks at once [1]. For example, walking (motor challenge) and simultaneously thinking (cognitive challenge) could cause a cognitive-motor interference (CMI) that might affect performance in either of the tasks or both tasks [2]. CMI could be determined by the reduced dualtask (DT) performance compared to the single-task (ST) performance, represented as a cost for walking (walking cost) and as a cost for cognition (cognitive cost) [2, 3]. For example, CMI in walking performance could be reflected by a slow gait speed, shorter stride length, reduced cadence, increased stride duration, and longer double limb support phases. When older adults perform a simultaneous cognitive task, they exhibit both increased walking and cognitive costs [46], which were associated with increased risk of falling [6, 7]. Several studies have shown that impaired vision such as blurred vision and peripheral-vision-loss causes deterioration in postural control [8] and in walking [9-11]. Other studies have shown that blurred vision that reduces visual acuity, edge contrast sensitivity, and depth perception tends to result in greater risk for loss of balance while walking [12] and cause many accidents in older adults [13, 14]. Recently, studies have shown that peripheral vision is needed to stabilize anteriorposterior sway while standing [15, 16] as well as to establish an accurate representation of spatial structure while walking [9]. Glaucoma, one of the most common causes of irreversible blindness worldwide in older adults due to ARD (age-related-decline) causes a reduction in the peripheral field of view [1, 15] and problems with peripheral vision affect the stability of walking [9, 10]. Many studies have used dual-task paradigms to investigate postural control under impaired vision [17, 18]. In a study with healthy older adults, an addition of a cognitive secondary task combined with an artificially induced blurred vision produced an imbalance while standing [18]. However, it is still unknown how such visual impairment may affect CMI associated with dual-task during walking, especially in older adults. For example, walking-and-talking while road-crossing involves processing multiple types of information that requires greater cognitive resources than walking or talking alone and thus will be greatly affected by visual impairment. Thus, the purpose of this study is to investigate the effect of concurrent visual impairment like blurred vision and peripheral-vision-loss on CMI during dual-task walking in young and older adults. We hypothesized that a greater walking cost would be associated with vision and age (Hypothesis 1). 3
Specifically, in blurred vision and peripheral-vision-loss and in older adults, the walking cost would be increased. We also hypothesized that a greater cognitive cost would be associated with impaired vision and age (Hypothesis 2). METHODS Nineteen healthy young adults (Mean ± SD = 22.25 ± 0.68 years, 4 males) and nineteen healthy older adults (Mean ± SD = 71.45 ± 1.25 years, 6 males) participated in the study. Young participants were recruited from the California State University, Long Beach, while the older adults were recruited from a senior center in Long Beach. All the older adults lived independently in the community. Participants were excluded from this study if they had one or more of the following: uncorrected secondary eye pathologies, history of neurological disorders, orthopedic deficits of the lower extremity, depression, assistance with activities of daily living (ADL), morbidly obese, hip or knee replacements, and auditory or vestibular pathologies. We also excluded the participants with cognitive impairment (evidenced by a score of less than 26 on the mini‐cog) [19]. We obtained informed consent forms and the experiment was conducted according to the Declaration of Helsinki [20]. Equipment Temporal and spatial parameters of gait were recorded using the ZenoMat ‘Platinum’ 16-ft electronic walkway and the Protokinetics Movement Analysis Software (PKMAS - ProtoKinetics, Havertown, PA) that has sensors embedded into a 16*2 feet mat. The following gait characteristics were assessed: step length, stride length, stride width, gait velocity, double limb support time, gait cycle time, gait cycle time coefficient of variation (CV), gait velocity and cadence. The three vision conditions were simulated using customized laboratory googles (See Fig.1): normal vision (NV – participants wore a plain laboratory goggle), blurred vision (BV - participants wore a laboratory goggle blurred by frosted glass paint) and peripheral-vision-loss (PVL - participants wore a laboratory google with peripheral vision occluded by black tape). < Figure 1 is about here> A cognitive challenge targeting working memory was introduced by asking the subjects to subtract 3 from a 3-digit number. A different 3-digit number was used as a starting point whenever the cognitive task was administered across different conditions. The number of correct responses in 20 s was recorded using the Audacity sound recording software (version 2.1.2) [21]. Experimental Procedure 4
Participants performed both single and dual-tasks (see Fig.2). Block A consisted of a cognitive single task – serial subtraction by 3, (i.e., performing a cognitive task while sitting) that was performed three times in all three visual conditions in a random order. Block B consisted of walking single task, i.e., walking on the ZenoMat at normal speed without performing any cognitive challenge. The participants walked across the mat, turned and walked back to the starting position, starting and ending the walk 1.5m away from the edge of the mat. The walking singletask was also performed three times, one in each vision condition. Both block A and B were counterbalanced across the participants. Block C consisted of dual-tasking (i.e., walking while performing a cognitive task), also under three visual conditions in a random order. Participants first received standardized instructions on how to perform the cognitive task followed by one familiarization trial. An interval of 15 minutes was provided between single-task and dual-task conditions. The experiment took about 35-55 minutes. < Figure 2 is about here> Data Analysis We computed the dual-task cost, which is the change in dual-task compared to the same singletask performance separately using the following formula [22]. Dual-task cost = 100* (single task-dual task)/single task The formula shows that the difference between single task and dual task is normalized by the single task performance. Specifically, walking cost was computed using the gait parameters between STwalking and DT-walking on the following gait variables: step length, stride length, velocity, cadence, step width, double support time, gait cycle time, and coefficient of variation of gait cycle time. Cognitive cost was computed using the number of correct responses between ST-cognitive and DT-cognitive. Statistical Analysis Two-way mixed MANOVA was used to compare the effects of age (young vs older) and vision (NV vs BV vs PVL) and their interaction on walking cost for the following gait parameters (Hypothesis #1): step length, stride length, velocity, cadence, step width, double support time, gait cycle time, and coefficient of variation of gait cycle time. A significant result was followed by univariate ANOVAs with correction for Type I error. A parallel two-way mixed ANOVA was used to compare the age and vision and their interactive effects on cognitive cost (Hypothesis #2). 5
For a baseline cognition comparison, we also performed a two-way mixed ANOVA to understand the main effect of age and vision and their interaction effects on the number of correct responses during the single task cognitive performance. For vision, whenever the Mauchly’s test of sphericity was not met, Green-House-Geiser correction was made. Post-hoc analysis with Bonferroni correction was used for further comparisons within the three visual conditions. The statistical significance was set at p < 0.05 in all the other tests, and for the univariate ANOVAs with Type I error correction, the significance was set at p < 0.025. Statistical analysis was performed in SPSS version 24.0, Chicago, IL. RESULTS Our first hypothesis was partially supported: there was a greater walking cost associated with impaired vision and older age, but not a significant interaction. A mixed 2-way MANOVA on the gait variables revealed a significant main effect of vision [Wilk’s λ = 0.38, F(16,21) = 2.17, p = .05, η2 = 0.62] and a significant main effect of age [Wilk’s λ = 0.59, F(8,29) = 2.54, p = .03, η2 = 0.41], without any interaction (p = .07). To control for the inflation of Type I error for the follow-up Univariate ANOVAs, we created two groups of gait variables, one for the family of four spatial gait variables and the other for the family of four temporal gait variables. We set the alpha level of each family-wise analysis to be .10, and applied Bonferroni correction to set the alpha level of each Univariate ANOVA to be .10/4 = .025 [23]. The results of the univariate ANOVA for the vision did not show any significance. The results of the univariate ANOVA for the age (young vs. old) were as follows: step length (p = .03), stride length (p = .025), cycle time (p = .01), velocity (p = .02), cadence (p = .01). Figure 3 shows the walking cost of the gait parameters for the young and older adults. < Figure 3 is about here> Our second hypothesis that a greater cognitive cost would be associated with impaired vision and age, was also partially supported. Both impaired vision conditions compared to the normal vision showed a greater cognitive cost, but surprisingly there were no age-related differences. A mixed 2-way ANOVA revealed a significant main effect of vision alone [F(2,60) = 5.76, p = .01] and did not show any effect of age or interaction (Fig.4A). The post-hoc analysis on vision using Bonferroni correction showed the NV condition significantly different from the BV (p = .01) and from the PVL conditions (p = .03). There was no difference between BV and PVL conditions, 6
suggesting that the cognitive cost increased with impaired vision in both young and older adults. To demonstrate that impaired vison did not affect the cognitive ST performance, but affected the cognitive performance while walking, we analyzed the effects of vision (and age) on the cognitive ST performance. The number of correct responses during ST cognitive for the young and older adults is shown in Fig 4B. A mixed 2-way ANOVA revealed a significant main effect of age [F(1,31) = 7.03, p = .01], but did not show any effect of either vision or interaction on the number of correct responses. Specifically, older adults had reduced number of correct responses when compared to young adults in all the vision conditions during the serial subtraction tests conducted during sitting. Taken together, these results seem to suggest that both groups have prioritized walking compared to cognition during DT under impaired vision, resulting in increased cognitive cost with impaired vison which did not exist in the cognitive ST. To gauge the potential practice effect in performing serial subtraction task multiple times across different vision conditions, we focused on the serial subtraction responses under the single task and rearranged them in the order of performance regardless of vision condition (which was possible because the vision condition was counterbalanced). Then we applied a paired samples ttest to compare the cognitive performance between trial 1 and trial 2 and the one between trial 2 and trial 3 for all subjects (young and older adults combined). The results did not show a significant difference between trial 1 and trial 2 [t(39) = .31, p = .76], and between trial 2 and trial 3 [t(40) = .32, p = .75]. Figure 4B also shows that we did not see any practice effect between single task and dual task, as both groups did not improve their cognitive performance in the dual task. < Figure 4 is about here> DISCUSSION This study investigated the effects of concurrent visual impairment like blurred vision and peripheral-vision-loss on CMI during dual-task walking in young and older adults. The results showed that while impaired vision and older age increased the walking cost, surprisingly only impaired vision increased the cognitive cost. During dual-task walking, when interrupted with vision, both young and older adults let cognition suffer, thus prioritizing walking. Walking Cost As expected, DT was harder compared to ST, and the walking cost increased with aging and with visual impairment. ARD increases gait and balance disorders from around 10% between the ages 7
of 60 and 69 years to more than 60% in those over 80 years [24]. The existence of walking cost in older adults from our study is consistent with the findings of previous studies [4, 5, 21]. It corroborates the common consensus that ARD makes it difficult for older adults to share attention in dual-task conditions [17, 25]. With an addition of visual impairment, sharing of attention becomes even more difficult, resulting in increased CMI. Our study, for the first time, found a greater decline in walking performance in DT with an additional visual challenge in older adults, and further underscore the importance of impaired vision as an added risk factor on walking while performing another task. Cognitive Cost In the single-cognitive task, our results showed large age differences in the raw cognitive performance (the number of correct responses). However, the cognitive cost (that captures the cost in cognition with added walking) did not change with age, but with impaired vision. The increased cognitive cost in impaired vision conditions in both groups may be linked to a reliance on the use of vision to guide walking in DT, in general. For example, to move safely we require visual identification of where we walk and to place our foot. Therefore, it is possible that when faced with blurred and peripheral-vision-loss, both young and older adults appear to allocate less attention to cognition, while prioritizing walking over cognition to overcome the difficulties associated with walking and foot placement. This confirms that impaired vision places greater demand on the available processing resources, thus forcing both young and older adults to concentrate on ‘posture-first’ strategy [22]. In a study by Oh-Park et al., older adults, when walking while carrying a tray, paid more attention to walking than to the tray, even when asked to pay attention to the tray, supporting the ‘posture-first’ strategy, as compared to the young adults [26]. In our study, under impaired vision conditions, both older and young adults allocated more attention to walking than to cognition. However, the cognitive cost (with impaired vision and during DT) did not show any age effect. The lack of age effect on cognitive cost in our study is in line with a previous study, though they employed stroop task while walking, while we employed serial subtraction task while walking [3]. Loss of Vision Impaired vision may pose significant challenges to an individual who is walking with a simultaneous cognitive challenge. While we found that both blurred vision and peripheral-visionloss caused greater walking cost as well as cognitive cost, we did not see any specific differences 8
between the two artificially imposing impaired conditions. Very few experimental studies have assessed the role of impaired vision such as blurred or peripheral vision loss while walking [9, 27]. When young healthy adults with simulated cataracts walked across a curved pathway, gait speed decreased in dim light but not in full light [27]. Another study showed that low light vision resulted in increased variability in gait performance and a reduced walking speed [28]. Few other studies have shown that peripheral-vision-loss may be predominant in the anterior-posterior balance control, providing support to the ‘peripheral dominance theory’ during standing [16, 29]. One study related to walking suggested that peripheral vision is important for establishing and/or updating an accurate representation of spatial structure for navigation [9]. In their study, participants drifted off course while walking when they had a peripheral visual field loss. Our study extends the evidence of the importance of peripheral vision in walking performance itself, rather than the walking course, especially when challenged by a simultaneous cognition task. Limitation In our study, participants performed the single tasks first and performed each ST and DT tasks across different visual conditions. The repetition might induce practice effect, which is particularly important for a cognitive task. However, we did not see any statistically significant practice effect enough to improve performance in the DT cognitive tasks with impaired vision. We also did not assess single task performance of the visual task because of the complexity involved working with the vision charts and computing the vision cost. It could definitely be a future work. One more limitation is that the results of this study cannot be transferable to older populations with actual visual impairments, who might have developed alternative strategies to overcome their visual impairments [30]. Conclusion This study examined CMI (as assessed separately by walking and cognitive costs) during dualtask walking in young and older adults, under normal, blurred and peripheral-vision-loss conditions. Higher walking performance cost was seen in older adults and with impaired vision. In contrast, both young and older adults exhibited prioritization of walking over cognitive performance during blurred vision and peripheral-vision-loss. These results provide new information on how young and older adults distribute their attention to cope with the increased motor and cognitive challenges associated with DT under impaired sensory information. Future
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work should explore whether dual-task training under visual challenge could reduce cognitivemotor interference and reduce fall risks in older adults.
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FIGURE CAPTIONS Fig.1. The letters provide a simulation of the three visual conditions received by the participants. NV is the normal vision, BV is the blurred vision and PVL is the peripheral-vision-loss conditions. Fig. 2. Single Task (ST) and Dual Task (DT) conditions. (A) ST cognitive serial subtraction task was performed in sitting under normal, blurred and peripheral-vision-loss conditions. (B) ST walking was performed under normal, blurred and peripheral-vision-loss conditions. (C) DT cognitive serial subtraction task was performed while walking under normal, blurred and peripheral-vision-loss conditions. Fig. 3. Dual-task walking cost for all the gait parameters. A positive walking cost in the spatial parameters (step length, stride length, velocity, cadence) and a negative walking cost in the temporal parameters (double support time, gait cycle time, gait cycle time CV) of gait indicate reduced performance in the dual tasks compared to single tasks. Error bars indicate standard deviations (SDs) of the mean. The figure shows an increased walking cost for the older adults. Significance level was set at p < 0.025 (indicated by *). Fig. 4. Cognitive performance: (A) Figure shows a decline in the performance of number of correct responses during cognitive single task in older adults. (B) Dual-task cognitive cost (indicating reduced performance in dual task compared to cognitive single task) is increased with impaired vision (BV and PVL) in both the groups. Error bars indicate standard deviations (SDs) of the mean. Significance level was set at p < 0.05 (indicated by *). Acknowledgement This study was supported in part by HOGAR grant from CSU, Long Beach to Dr. Krishnan in 2015. The authors thank Meagan Suen, Trong Pham, Alica Pech Corrales, Babken Sarkissian, Emily Nichols and Daniela Gonzalez for their help in data collection and analysis.
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