Vision, cognition, and walking stability in young adults.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
11 01 2022
11 01 2022
Historique:
received:
12
07
2021
accepted:
23
12
2021
entrez:
12
1
2022
pubmed:
13
1
2022
medline:
1
3
2022
Statut:
epublish
Résumé
Downward gazing is often observed when walking requires guidance. This gaze behavior is thought to promote walking stability through anticipatory stepping control. This study is part of an ongoing effort to investigate whether downward gazing also serves to enhance postural control, which can promote walking stability through a feedback/reactive mechanism. Since gaze behavior alone gives no indication as to what information is gathered and the functions it serves, we aimed to investigate the cognitive demands associated with downward gazing, as they are likely to differ between anticipatory and feedback use of visual input. To do so, we used a novel methodology to compromise walking stability in a manner that could not be resolved through modulation of stepping. Then, using interference methodology and neuroimaging, we tested for (1) interference related to dual tasking, and (2) changes in prefrontal activity. The novel methodology resulted in an increase in the time spent looking at the walking surface. Further, while some dual-task interference was observed, indicating that this gaze behavior is cognitively demanding, several gaze parameters pertaining to downward gazing and prefrontal activity correlated. These correlations revealed that a greater tendency to gaze onto the walking surface was associated with lower PFC activity, as is expected when sensory information is used through highly automatic, and useful, neural circuitry. These results, while not conclusive, do suggest that gazing onto the walking surface can be used for purposes other than anticipatory stepping control, bearing important motor-control and clinical implications.
Identifiants
pubmed: 35017580
doi: 10.1038/s41598-021-04540-w
pii: 10.1038/s41598-021-04540-w
pmc: PMC8752684
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
513Informations de copyright
© 2022. The Author(s).
Références
Armstrong, D. M. The supraspinal control of mammalian locomotion. J. Physiol. 405, 1–37 (1988).
pubmed: 3076600
pmcid: 1190962
doi: 10.1113/jphysiol.1988.sp017319
Clark, D. J. Automaticity of walking: functional significance, mechanisms, measurement and rehabilitation strategies. Front. Hum. Neurosci. 9, 246 (2015).
pubmed: 25999838
pmcid: 4419715
doi: 10.3389/fnhum.2015.00246
Yogev-Seligmann, G., Hausdorff, J. M. & Giladi, N. The role of executive function and attention in gait. Mov. Disord. 23, 329–342 (2008).
pubmed: 18058946
doi: 10.1002/mds.21720
Hamacher, D., Herold, F., Wiegel, P., Hamacher, D. & Schega, L. Brain activity during walking: a systematic review. Neurosci. Biobehav. Rev. 57, 310–327 (2015).
pubmed: 26306029
doi: 10.1016/j.neubiorev.2015.08.002
Vitorio, R., Stuart, S., Rochester, L., Alcock, L. & Pantall, A. fNIRS response during walking - Artefact or cortical activity? A Systematic review. Neurosci. Biobehav. Rev. 83, 160–172 (2017).
pubmed: 29017917
doi: 10.1016/j.neubiorev.2017.10.002
Herold, F. et al. Functional near-infrared spectroscopy in movement science: a systematic review on cortical activity in postural and walking tasks. Neurophotonics 4, 041403 (2017).
pubmed: 28924563
pmcid: 5538329
doi: 10.1117/1.NPh.4.4.041403
Miller, E. K. & Cohen, J. D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).
pubmed: 11283309
doi: 10.1146/annurev.neuro.24.1.167
Suzuki, M. et al. Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage 23, 1020–1026 (2004).
pubmed: 15528102
doi: 10.1016/j.neuroimage.2004.07.002
Harada, T., Miyai, I., Suzuki, M. & Kubota, K. Gait capacity affects cortical activation patterns related to speed control in the elderly. Exp. Brain Res. 193, 445–454 (2009).
pubmed: 19030850
doi: 10.1007/s00221-008-1643-y
Koenraadt, K. L., Roelofsen, E. G., Duysens, J. & Keijsers, N. L. Cortical control of normal gait and precision stepping: an fNIRS study. Neuroimage 85(Pt 1), 415–422 (2014).
pubmed: 23631980
doi: 10.1016/j.neuroimage.2013.04.070
Clark, D. J., Rose, D. K., Ring, S. A. & Porges, E. C. Utilization of central nervous system resources for preparation and performance of complex walking tasks in older adults. Front. Aging Neurosci. 6, 217 (2014).
pubmed: 25202270
pmcid: 4142860
doi: 10.3389/fnagi.2014.00217
Mirelman, A. et al. Effects of aging on prefrontal brain activation during challenging walking conditions. Brain Cogn. 115, 41–46 (2017).
pubmed: 28433922
doi: 10.1016/j.bandc.2017.04.002
Patla, A. E. Understanding the roles of vision in the control of human locomotion. Gait Posture 5, 54–69 (1997).
doi: 10.1016/S0966-6362(96)01109-5
Patla, A. E. & Vickers, J. N. Where and when do we look as we approach and step over an obstacle in the travel path?. NeuroRep. 8, 3661–3665 (1997).
doi: 10.1097/00001756-199712010-00002
Patla, A. E. & Vickers, J. N. How far ahead do we look when required to step on specific locations in the travel path during locomotion?. Exp. Brain Res. 148, 133–138 (2003).
pubmed: 12478404
doi: 10.1007/s00221-002-1246-y
Matthis, J. S., Yates, J. L. & Hayhoe, M. M. Gaze and the control of foot placement when walking in natural terrain. Curr. Biol. 28, 1224-1233.e5 (2018).
pubmed: 29657116
pmcid: 5937949
doi: 10.1016/j.cub.2018.03.008
Higuchi, T. Visuomotor control of human adaptive locomotion: understanding the anticipatory nature. Front. Psychol. 4, 277 (2013).
pubmed: 23720647
pmcid: 3655271
doi: 10.3389/fpsyg.2013.00277
Marigold, D. S. & Patla, A. E. Visual information from the lower visual field is important for walking across multi-surface terrain. Exp. Brain Res. 188, 23–31 (2008).
pubmed: 18322679
doi: 10.1007/s00221-008-1335-7
Yamada, M. et al. Fallers choose an early transfer gaze strategy during obstacle avoidance in dual-task condition. Aging Clin. Exp. Res. 23, 316–319 (2011).
pubmed: 20834203
doi: 10.1007/BF03337757
Ellmers, T. J., Cocks, A. J., Doumas, M., Williams, A. M. & Young, W. R. Gazing into thin air: the dual-task costs of movement planning and execution during adaptive gait. PLoS ONE 11, e0166063 (2016).
pubmed: 27824937
pmcid: 5100909
doi: 10.1371/journal.pone.0166063
Feld, J. A. & Plummer, P. Visual scanning behavior during distracted walking in healthy young adults. Gait Posture 67, 219–223 (2019).
pubmed: 30380505
doi: 10.1016/j.gaitpost.2018.10.017
Miller, A. B., Lajoie, K., Strath, R. A., Neima, D. R. & Marigold, D. S. Coordination of gaze behavior and foot placement during walking in persons with glaucoma. J. Glaucoma 27, 55–63 (2018).
pubmed: 29117005
doi: 10.1097/IJG.0000000000000819
Zukowski, L. A., Tennant, J. E., Iyigun, G., Giuliani, C. A. & Plummer, P. Dual-tasking impacts gait, cognitive performance, and gaze behavior during walking in a real-world environment in older adult fallers and non-fallers. Exp. Gerontol. 150, 111342 (2021).
pubmed: 33838215
doi: 10.1016/j.exger.2021.111342
Woollacott, M. & Shumway-Cook, A. Attention and the control of posture and gait: a review of an emerging area of research. Gait Posture 16, 1–14 (2002).
pubmed: 12127181
doi: 10.1016/S0966-6362(01)00156-4
Wittenberg, E., Thompson, J., Nam, C. S. & Franz, J. R. Neuroimaging of human balance control: a systematic review. Front. Hum. Neurosci. 11, 170 (2017).
pubmed: 28443007
pmcid: 5385364
doi: 10.3389/fnhum.2017.00170
Lajoie, Y., Teasdale, N., Bard, C. & Fleury, M. Attentional demands for static and dynamic equilibrium. Exp. Brain Res. 97, 139–144 (1993).
pubmed: 8131825
doi: 10.1007/BF00228824
Lee, D. N. & Lishman, J. Visual proprioceptive control of stance. Journal of human movement studies (1975).
Stoffregen, T. A. Flow structure versus retinal location in the optical control of stance. J. Exp. Psychol. Hum. Percept. Perform. 11, 554–565 (1985).
pubmed: 2932530
doi: 10.1037/0096-1523.11.5.554
Bardy, B. G., Warren, W. H. & Kay, B. A. Motion parallax is used to control postural sway during walking. Exp. Brain Res. 111, 271–282 (1996).
pubmed: 8891657
doi: 10.1007/BF00227304
Guerraz, M., Sakellari, V., Burchill, P. & Bronstein, A. M. Influence of motion parallax in the control of spontaneous body sway. Exp. Brain Res. 131, 244–252 (2000).
pubmed: 10766276
doi: 10.1007/s002219900307
Warren, W. H., Kay, B. A. & Yilmaz, E. H. Visual control of posture during walking: functional specificity. J. Exp. Psychol. Hum. Percept. Perform. 22, 818–838 (1996).
pubmed: 8756954
doi: 10.1037/0096-1523.22.4.818
Stins, J., Michielsen, M., Roerdink, M. & Beek, P. J. Sway regularity reflects attentional involvement in postural control: Effects of expertise, vision and cognition. Gait Posture 30, 106–109 (2009).
pubmed: 19411174
doi: 10.1016/j.gaitpost.2009.04.001
Teo, W., Goodwill, A. M., Hendy, A. M., Muthalib, M. & Macpherson, H. Sensory manipulation results in increased dorsolateral prefrontal cortex activation during static postural balance in sedentary older adults: An fNIRS study. Brain and behavior 8, e01109 (2018).
pubmed: 30230687
pmcid: 6192391
doi: 10.1002/brb3.1109
Koren, Y. et al. Gazing down increases standing and walking postural steadiness. Royal Society Open Science 8, 201556 (2021).
Koren, Y. et al. Downward Gazing for Steadiness. preprint at https://www.biorxiv.org/content/ https://doi.org/10.1101/2020.02.28.969162v1 (2020).
Ellmers, T. J. & Young, W. R. Conscious motor control impairs attentional processing efficiency during precision stepping. Gait Posture 63, 58–62 (2018).
pubmed: 29715607
doi: 10.1016/j.gaitpost.2018.04.033
Koren, Y., Parmet, Y. & Bar-Haim, S. Treading on the unknown increases prefrontal activity: A pilot fNIRS study. Gait Posture 69, 96–100 (2019).
pubmed: 30690327
doi: 10.1016/j.gaitpost.2019.01.026
Bar-Haim, S., Harries, N., Hutzler, Y., Belokopytov, M. & Dobrov, I. Training to walk amid uncertainty with Re-Step: measurements and changes with perturbation training for hemiparesis and cerebral palsy. Disabil. Rehabil. Assist. Technol. 8, 417–425 (2013).
pubmed: 23324031
doi: 10.3109/17483107.2012.754954
Huppert, T. J., Diamond, S. G., Franceschini, M. A. & Boas, D. A. HomER: a review of time-series analysis methods for near-infrared spectroscopy of the brain. Appl. Opt. 48, D280–D298 (2009).
pubmed: 19340120
pmcid: 2761652
doi: 10.1364/AO.48.00D280
Scholkmann, F. et al. A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology. Neuroimage 85(Pt 1), 6–27 (2014).
pubmed: 23684868
doi: 10.1016/j.neuroimage.2013.05.004
Marigold, D. S. & Patla, A. E. Gaze fixation patterns for negotiating complex ground terrain. Neuroscience 144, 302–313 (2007).
pubmed: 17055177
doi: 10.1016/j.neuroscience.2006.09.006
Marigold, D. S. Role of peripheral visual cues in online visual guidance of locomotion. Exerc. Sport Sci. Rev. 36, 145–151 (2008).
pubmed: 18580295
doi: 10.1097/JES.0b013e31817bff72
Al-Yahya, E. et al. Cognitive motor interference while walking: a systematic review and meta-analysis. Neurosci. Biobehav. Rev. 35, 715–728 (2011).
pubmed: 20833198
doi: 10.1016/j.neubiorev.2010.08.008
Hayhoe, M. M. & Matthis, J. S. Control of gaze in natural environments: effects of rewards and costs, uncertainty and memory in target selection. Interface Focus 8, 20180009 (2018).
pubmed: 29951189
pmcid: 6015808
doi: 10.1098/rsfs.2018.0009
Delafontaine, A., Hansen, C., Marolleau, I., Kratzenstein, S. & Gouelle, A. Effect of a concurrent cognitive task, with stabilizing visual information and withdrawal, on body sway adaptation of parkinsonian’s patients in an off-medication state: a controlled study. Sensors 20, 5059 (2020).
pmcid: 7571225
doi: 10.3390/s20185059
Iara de, A. I., Jörn M Horschig, Gerakaki, S., Wanrooij, M. M. v. & Willy, N J M Colier. Cerebral oxygenation responses to head movement measured with near-infrared spectroscopy Ser. 11638, March 05 2021).