Abstract
Background
Control of upper body motion deteriorates with ageing leading to impaired ability to preserve balance during gait, but little is known on the contribution of the upper body to preserve balance in response to unexpected perturbations during locomotor transitions, such as gait initiation.
Aim
To investigate differences between young and older adults in the ability to modify the trunk kinematics and muscle activity following unexpected waist lateral perturbations during gait initiation.
Methods
Ten young (25 ± 2 years) and ten older adults (73 ± 5 years) initiated locomotion from stance while a lateral pull was randomly applied to the pelvis. Two force plates were used to define the feet centre-of-pressure displacement. Angular displacement of the trunk in the frontal plane was obtained through motion analysis. Surface electromyography of cervical and thoracic erector spinae muscles was recorded bilaterally.
Results
A lower trunk lateral bending towards the stance leg side in the preparatory phase of gait initiation was observed in older participants following perturbation. Right thoracic muscle activity was increased in response to the perturbation during the initial phase of gait initiation in young (+ 68%) but not in older participants (+ 7%).
Conclusions
The age-related reduction in trunk movement could indicate a more rigid behaviour of the upper body employed by older compared to young individuals in response to unexpected perturbations preceding the initiation of stepping. Older adults’ delayed activation of thoracic muscles could suggest impaired reactive mechanisms that may potentially lead to a fall in the early stages of the gait initiation.
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References
Lepers R, Brenière Y (1995) The role of anticipatory postural adjustments and gravity in gait initiation. Exp Brain Res 107:118–124. https://doi.org/10.1007/BF00228023
Crenna P, Frigo C (1991) A motor programme for the initiation of forward-oriented movements in humans. J Physiol 437:635–653. https://doi.org/10.1113/jphysiol.1991.sp018616
Jian Y, Winter D, Ishac M, et al (1993) Trajectory of the body COG and COP during initiation and termination of gait. Gait Posture 1:9–22. https://doi.org/10.1016/0966-6362(93)90038-3
Mille M-L, Simoneau M, Rogers MW (2014) Postural dependence of human locomotion during gait initiation. J Neurophysiol 112:3095–3103. https://doi.org/10.1152/jn.00436.2014
Mizusawa H, Jono Y, Iwata Y et al (2017) Processes of anticipatory postural adjustment and step movement of gait initiation. Hum Mov Sci 52:1–16. https://doi.org/10.1016/j.humov.2017.01.003
Mickelborough J, Van Der Linden ML, Tallis RC, et al (2004) Muscle activity during gait initiation in normal elderly people. Gait Posture 19:50–57. https://doi.org/10.1016/S0966-6362(03)00016-X
Maslivec A, Bampouras TM, Dewhurst S et al (2018) Mechanisms of head stability during gait initiation in young and older women: a neuro-mechanical analysis. J Electromyogr Kinesiol 38:103–110. https://doi.org/10.1016/j.jelekin.2017.11.010
Laudani L, Casabona A, Perciavalle V, et al (2006) Control of head stability during gait initiation in young and older women. J Electromyogr Kinesiol 16:603–610. https://doi.org/10.1016/j.jelekin.2006.08.001
Ceccato J-C, de Sèze M, Azevedo C, et al (2009) Comparison of trunk activity during gait initiation and walking in humans. PLoS ONE 4:e8193. https://doi.org/10.1371/journal.pone.0008193
Summa A, Vannozzi G, Bergamini E et al (2016) Multilevel upper body movement control during gait in children with cerebral palsy. PLoS ONE 11:1–13. https://doi.org/10.1371/journal.pone.0151792
Aruin AS, Latash ML (1995) The role of motor action in anticipatory postural adjustments studied with self-induced and externally triggered perturbations. Exp brain Res 106:291–300. https://doi.org/10.1007/bf00241125
Falla D, Rainoldi A, Merletti R, et al (2004) Spatio-temporal evaluation of neck muscle activation during postural perturbations in healthy subjects. J Electromyogr Kinesiol 14:463–474. https://doi.org/10.1016/j.jelekin.2004.03.003
Danna-Dos-Santos A, Degani AM, Latash ML (2007) Anticipatory control of head posture. Clin Neurophysiol 118:1802–1814. https://doi.org/10.1016/j.clinph.2007.05.060
Rietdyk S, Patla AE, Winter DA et al (1999) Balance recovery from medio-lateral perturbations of the upper body during standing. J Biomech 32:1149–1158. https://doi.org/10.1016/S0021-9290(99)00116-5
Mouchnino L, Robert G, Ruget H et al (2012) Online control of anticipated postural adjustments in step initiation: evidence from behavioral and computational approaches. Gait Posture 35:616–620. https://doi.org/10.1016/j.gaitpost.2011.12.009
Grabiner MD, Donovan S, Lou BM et al (2008) Trunk kinematics and fall risk of older adults: translating biomechanical results to the clinic. J Electromyogr Kinesiol 18:197–204. https://doi.org/10.1016/j.jelekin.2007.06.009
Pavol MJ, Owings TM, Foley KT, et al (2001) Mechanisms leading to a fall from an induced trip in healthy older adults. J Gerontol A Biol Sci Med Sci 56:M428–M437. https://doi.org/10.1093/gerona/56.7.m428
Owings TM, Pavol MJ, Grabiner MD (2001) Mechanisms of failed recovery following postural perturbations on a motorized treadmill mimic those associated with an actual forward trip. Clin Biomech (Bristol, Avon) 16:813–819. https://doi.org/10.1097/00005537-200003002-00002
Greig CA, Young A, Skelton DA et al (1994) Exercise studies with elderly volunteers. Age Ageing 23:185–189. https://doi.org/10.1093/ageing/23.3.185
Berg KO, Wood-Dauphinee SL, Williams JI, et al (1992) Measuring balance in the elderly: validation of an instrument. Can J Public Health 83:S7–11. https://doi.org/10.1111/j.1532-950X.2008.00478.x
Yardley L, Beyer N, Hauer K et al (2005) Development and initial validation of the Falls Efficacy Scale-International (FES-I). Age Ageing 34:614–619. https://doi.org/10.1093/ageing/afi196
Gutierrez EM, Bartonek Å, Haglund-Åkerlind Y, et al (2003) Centre of mass motion during gait in persons with myelomeningocele. Gait Posture 18:37–46. https://doi.org/10.1016/S0966-6362(02)00192-3
Winter DA, Prince F, Frank JS et al (1996) Unified theory regarding A/P and M/L balance in quiet stance. J Neurophysiol 75:2334–2343. https://doi.org/10.1152/jn.1996.75.6.2334
MacKinnon CD, Bissig D, Chiusano J et al (2007) Preparation of anticipatory postural adjustments prior to stepping. J Neurophysiol 97:4368–4379. https://doi.org/10.1152/jn.01136.2006
Uemura K, Yamada M, Nagai K et al (2012) Fear of falling is associated with prolonged anticipatory postural adjustment during gait initiation under dual-task conditions in older adults. Gait Posture 35:282–286. https://doi.org/10.1016/j.gaitpost.2011.09.100
Drake JDM, Callaghan JP (2006) Elimination of electrocardiogram contamination from electromyogram signals: an evaluation of currently used removal techniques. J Electromyogr Kinesiol 16:175–187. https://doi.org/10.1016/j.jelekin.2005.07.003
Timmann D, Horak FB (2001) Perturbed step initiation in cerebellar subjects: 2. Modification of anticipatory postural adjustments. Exp Brain Res 141:110–120. https://doi.org/10.1007/s002210100858
Latash ML (2018) Muscle coactivation: definitions, mechanisms, and functions. J Neurophysiol 120:88–104. https://doi.org/10.1152/jn.00084.2018
Bland JM, Altman DG (1995) Calculating correlation coefficients with repeated observations: part 1 – Correlation within subjects. BMJ 310:446. https://doi.org/10.1136/bmj.310.6977.446
Richardson JTE (2011) Eta squared and partial eta squared as measures of effect size in educational research. Educ Res Rev 6:135–147. https://doi.org/10.1016/j.edurev.2010.12.001
Kavanagh JJ, Barrett RS, Morrison S (2004) Upper body accelerations during walking in healthy young and elderly men. Gait Posture 20:291–298. https://doi.org/10.1016/j.gaitpost.2003.10.004
Rum L, Laudani L, Macaluso A, et al (2017) Upper body accelerations during planned gait termination in young and older women. J Biomech 65:138–144. https://doi.org/10.1016/j.jbiomech.2017.10.019
Rogers MW, Mille M-L (2003) Lateral stability and falls in older people. Exerc Sport Sci Rev 31:182–187. https://doi.org/10.1097/00003677-200310000-00005
Kanekar N, Aruin AS (2014) The effect of aging on anticipatory postural control. Exp Brain Res 232:1127–1136. https://doi.org/10.1007/s00221-014-3822-3
Fujimoto M, Bair WN, Rogers MW (2015) Center of pressure control for balance maintenance during lateral waist-pull perturbations in older adults. J Biomech 48:963–968. https://doi.org/10.1016/j.jbiomech.2015.02.012
Hyodo M, Saito M, Ushiba J et al (2012) Anticipatory postural adjustments contribute to age-related changes in compensatory steps associated with unilateral perturbations. Gait Posture 36:625–630. https://doi.org/10.1016/j.gaitpost.2012.06.018
Khanmohammadi R, Talebian S, Hadian MR et al (2016) Characteristic muscle activity patterns during gait initiation in the healthy younger and older adults. Gait Posture 43:148–153. https://doi.org/10.1016/j.gaitpost.2015.09.014
Polcyn AF, Lipsitz LA, Kerrigan DC, et al (1998) Age-related changes in the initiation of gait: degradation of central mechanisms for momentum generation. Arch Phys Med Rehabil 79:1582–1589. https://doi.org/10.1016/S0003-9993(98)90425-7
Wang Y, Watanabe K, Asaka T (2017) Aging effect on muscle synergies in stepping forth during a forward perturbation. Eur J Appl Physiol 117:201–211. https://doi.org/10.1007/s00421-016-3514-8
Rogers MW, Hedman LD, Johnson ME et al (2003) Triggering of protective stepping for the control of human balance: age and contextual dependence. Cogn Brain Res 16:192–198. https://doi.org/10.1016/S0926-6410(02)00273-2
Pozzo T, Berthoz A, Lefort L (1990) Head stabilization during various locomotor tasks in humans. I. Normal subjects. Exp brain Res 82:97–106. https://doi.org/10.1007/bf00230842
Keshner EA, Chen KJ (1996) Mechanisms controlling head stabilization in the elderly during random rotations in the vertical plane. J Mot Behav 28:324–336. https://doi.org/10.1080/00222895.1996.10544602
Gerards MHG, McCrum C, Mansfield A, et al (2017) Perturbation-based balance training for falls reduction among older adults: current evidence and implications for clinical practice. Geriatr Gerontol Int 17:2294–2303. https://doi.org/10.1111/ggi.13082
Hilliard MJ, Martinez KM, Janssen I et al (2008) Lateral balance factors predict future falls in community-living older adults. Arch Phys Med Rehabil 89:1708–1713. https://doi.org/10.1016/j.apmr.2008.01.023
Claudino R, dos Santos ECC, Santos MJ (2013) Compensatory but not anticipatory adjustments are altered in older adults during lateral postural perturbations. Clin Neurophysiol 124:1628–1637. https://doi.org/10.1016/j.clinph.2013.02.111
Arvin M, Hoozemans MJM, Pijnappels M et al (2018) Where to step? Contributions of stance leg muscle spindle afference to planning of mediolateral foot placement for balance control in young and old adults. Front Physiol 9:1–10. https://doi.org/10.3389/fphys.2018.01134
Shulman D, Spencer A, Vallis LA (2018) Age-related alterations in reactive stepping following unexpected mediolateral perturbations during gait initiation. Gait Posture 64:130–134. https://doi.org/10.1016/j.gaitpost.2018.05.035
Sun R, Cui C, Shea JB (2017) Aging effect on step adjustments and stability control in visually perturbed gait initiation. Gait Posture 58:268–273. https://doi.org/10.1016/j.gaitpost.2017.08.013
Mille M-L, Rogers MW, Martinez K et al (2003) Thresholds for inducing protective stepping responses to external perturbations of human standing. J Neurophysiol 90:666–674. https://doi.org/10.1152/jn.00974.2002
Richards JG (1999) The measurement of human motion: a comparison of commercially available systems. Hum Mov Sci 18:589–602. https://doi.org/10.1016/S0167-9457(99)00023-8
Young WR, Mark Williams A (2015) How fear of falling can increase fall-risk in older adults: applying psychological theory to practical observations. Gait Posture 41:7–12. https://doi.org/10.1016/j.gaitpost.2014.09.006
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LR and LL conceived and designed the research. LR conducted the experiments under LL’s supervision. LR, GV and LL analysed data and all authors interpreted the experimental results. LR and LL wrote the manuscript. All authors edited, revised and approved the final version of the manuscript.
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Rum, L., Vannozzi, G., Macaluso, A. et al. Neuromechanical response of the upper body to unexpected perturbations during gait initiation in young and older adults. Aging Clin Exp Res 33, 909–919 (2021). https://doi.org/10.1007/s40520-020-01592-2
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DOI: https://doi.org/10.1007/s40520-020-01592-2