Abstract
This study aimed to investigate age-related differences in electromyographic (EMG) responses to unexpected Achilles tendon vibration (ATV) perturbations while standing blindfold. ATV with variable and random duration (12–15 s) and rest periods (20–24 s) was applied on 18 young and 16 older volunteers. The anterior/posterior center of pressure (CoP) and the soleus (SOL) and tibialis anterior (TA) EMG were analyzed for 1 s before and 8 s after the ATV onset and offset. ATV induced a posterior shift of CoP in both groups, with more pronounced shift in the older group. During ATV onset, the older group demonstrated less SOL and more TA EMG increase compared to the young group. During the first 0.5 s of ATV offset, SOL EMG was decreased in both age groups, while TA showed a burst of EMG activity that was greater in the older group. No difference in the latencies of EMG peaks or valleys was observed between the groups. It is concluded that ATV induces greater posterior CoP shift in older adults, and they adopt a recovery strategy, characterized by a decreased SOL activation and an increased TA activation. These differences are possibly attributed to the increased fear of falling, decreased limits of stability and reduced capacity of older people to reweight their sensory inflow when proprioception is distorted.
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References
Abrahámová D, Mancini M, Hlavačka F, Chiari L (2009) The age-related changes of trunk responses to Achilles tendon vibration. Neurosci Lett 467(3):220–224. https://doi.org/10.1016/j.neulet.2009.10.041
Barbieri G, Gissot A, Nougier V, Pérennou D (2013) Achilles tendon vibration shifts the center of pressure backward in standing and forward in sitting in young subjects. Clin Neurophysiol 43(4):237–242. https://doi.org/10.1016/j.neucli.2013.06.001
Baudry S (2016) Aging changes the contribution of spinal and corticospinal pathways to control balance. Exerc Sport Sci Rev 44(3):104–109. https://doi.org/10.1249/JES.0000000000000080
Baudry S, Duchateau J (2012) Age-related influence of vision and proprioception on Ia presynaptic inhibition in soleus muscle during upright stance. J Physiol 590(21):5541–5554. https://doi.org/10.1113/jphysiol.2012.228932
Baudry S, Collignon S, Duchateau J (2015) Influence of age and posture on spinal and corticospinal excitability. Exp Gerontol 69:62–69. https://doi.org/10.1016/j.exger.2015.06.006
Benjuya N, Melzer I, Kaplanski J (2004) Aging-induced shifts from a reliance on sensory input to muscle cocontraction during balanced standing. J Gerontol 59A(2):166–171. https://doi.org/10.1093/gerona/59.2.M166
Billot M, Handrigan GA, Simoneau M, Teasdale N (2015) Reduced plantar sole sensitivity induces balance control modifications to compensate ankle tendon vibration and vision deprivation. J Electromyogr Kinesiol 25(1):155–160. https://doi.org/10.1016/j.jelekin.2014.06.003
Carpenter MG, Frank JS, Silcher CP, Peysar GW (2001) The influence of postural threat on the control of upright stance. Exp Brain Res 138(2):210–218. https://doi.org/10.1007/s002210100681
Dalton BH, Blouin JS, Allen MD, Rice CL, Inglis JT (2014) The altered vestibular-evoked myogenic and whole-body postural responses in old men during standing. Exp Gerontol 60:120–128. https://doi.org/10.1016/j.exger.2014.09.020
Day BL, Séverac Cauquil A, Bartolomei L, Pastor MA, Lyon IN (1997) Human body-segment tilts induced by galvanic stimulation: a vestibularly driven balance protection mechanism. J Physiol 500(3):661–672. https://doi.org/10.1113/jphysiol.1997.sp022051
Duclos NC, Maynard L, Barthelemy J, Mesure S (2014) Postural stabilization during bilateral and unilateral vibration of ankle muscles in the sagittal and frontal planes. J Neuroeng Rehabil 11(1):130. https://doi.org/10.1186/1743-0003-11-130
Ehsani H, Mohler J, Marlinski V, Rashedi E, Toosizadeh N (2018) The influence of mechanical vibration on local and central balance control. J Biomech 71:59–66. https://doi.org/10.1016/J.JBIOMECH.2018.01.027
Eikema DJ, Hatzitaki V, Tzovaras D, Papaxanthis C (2014) Application of intermittent galvanic vestibular stimulation reveals age-related constraints in the multisensory reweighting of posture. Neurosci Lett 561:112–117
Eklund G (1972) General features of vibration-induced effects on balance. Upsala J Med Sci 77(2):112–124. https://doi.org/10.1517/03009734000000016
Fallon JB, Macefield VG (2007) Vibration sensitivity of human muscle spindles and golgi tendon organs. Muscle Nerve 36(1):21–29. https://doi.org/10.1002/mus.20796
Fountoulakis KN, Tsolaki M, Chantzi H, Kazis A (2000) Mini mental state examination (MMSE): a validation study in Greece. Am J Alzheimer’s Dis Other Dementias 15(6):342–345. https://doi.org/10.1177/153331750001500604
Freyler K, Gollhofer A, Colin R, Brüderlin U, Ritzmann R (2015) Reactive balance control in response to perturbation in unilateral stance: interaction effects of direction, displacement and velocity on compensatory neuromuscular and kinematic responses. PLoS ONE 10(12):e0144529. https://doi.org/10.1371/journal.pone.0144529
García-Piqueras J, García-Mesa Y, Cárcaba L, Feito J, Torres-Parejo I, Martín-Biedma B, Cobo J, García-Suárez O, Vega JA (2019) Ageing of the somatosensory system at the periphery: age-related changes in cutaneous mechanoreceptors. J Anat 234(6):839–852. https://doi.org/10.1111/joa.12983
Girardi M, Konrad HR, Amin M, Hughes LF (2001) Predicting Fall risks in an elderly population : computer dynamic posturography versus electronystagmography test results. September, 1528–1532.
Gouglidis V, Nikodelis T, Hatzitaki V, Amiridis IG (2011) Changes in the limits of stability induced by weight-shifting training in elderly women. Exp Aging Res 37(1):46–62. https://doi.org/10.1080/0361073X.2010.507431
Hatzitaki V, Pavlou M, Bronstein AM (2004) The integration of multiple proprioceptive information: effect of ankle tendon vibration on postural responses to platform tilt. Exp Brain Res 154:345–354. https://doi.org/10.1007/s00221-003-1661-8
Hay L, Bard C, Fleury M, Teasdale N (1996) Availability of visual and proprioceptive afferent messages and postural control in elderly adults. Exp Brain Res 108(1):129–139. https://doi.org/10.1007/BF00242910
Hermens HJ, Freriks B, Merletti R, Hagg G, Stegeman D, Blok J, Rau G, Disselhorst K, Roessingh G (1999) Seniam 8: European recommendations for surface electromyography. In Research and Development.
Horak FB, Nashner LM (1986) Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol 55(6): 1369–1381. 3734861
Ivanenko YP, Talis VL, Kazennikov OV (1999) Support stability influences postural responses to muscle vibration in humans. Euro J Neurosci 11(September 1998), 647–654.
Ivanenko YP, Gurfinkel VS (2018) Human postural control. Front Neurosci 12:171. https://doi.org/10.3389/fnins.2018.00171
Kanakis I, Hatzitaki V, Patikas DA, Amiridis IG (2014) Postural leaning direction challenges the manifestation of tendon vibration responses. Hum Mov Sci 33:251–262. https://doi.org/10.1016/j.humov.2013.09.005
Karamanidis K, Arampatzis A, Mademli L (2008) Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol 18:980–989
Kasahara S, Saito H, Anjiki T, Osanai H (2015) The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture 42(4):448–454. https://doi.org/10.1016/j.gaitpost.2015.07.056
Kim GH, Suzuki S, Kanda K (2007) Age-related physiological and morphological changes of muscle spindles in rats. J Physiol (london) 582(2):525–538. https://doi.org/10.1113/jphysiol.2007.130120
Lach HW, Parsons JL (2013) Impact of fear of falling in long term care: An integrative review. J Am Med Dir Assoc 14(8):573–577. https://doi.org/10.1016/j.jamda.2013.02.019
Lindemann I, Coombes BK, Tucker K, Hug F, Dick TJM (2020) Age-related differences in gastrocnemii muscles and Achilles tendon mechanical properties in vivo. J Biomech 112:110067. https://doi.org/10.1016/j.jbiomech.2020.110067
Maitre J, Jully JL, Gasnier Y, Paillard T (2013) Chronic physical activity preserves efficiency of proprioception in postural control in older women. J Rehabil Res Dev 50(6):811–819. https://doi.org/10.1682/JRRD.2012.08.0141
Masani K, Popovic MR, Nakazawa K, Kouzaki M, Nozaki D (2003) Importance of body sway velocity information in controlling ankle extensor activities during quiet stance. J Neurophysiol 90:3774–3782
Massion J (1992) Movement, posture and equilibrium: interaction and coordination. Prog Neurobiol 38(1):35–56
Masud T, Morris RO (2001) Epidemiology of falls. Age Ageing 30(suppl. 4):3–7. https://doi.org/10.1093/ageing/30.suppl_4.3
Mildren RL, Peters RM, Hill AJ, Blouin J-S, Carpenter MG, Inglis JT (2017) Frequency characteristics of human muscle and cortical responses evoked by noisy Achilles tendon vibration. J Appl Physiol 122(5):1134–1144. https://doi.org/10.1152/japplphysiol.00908.2016
Mildren RL, Schmidt ME, Eschelmuller G, Carpenter MG, Blouin J, Inglis JT (2020) Influence of age on the frequency characteristics of the soleus muscle response to Achilles tendon vibration during standing. J Physiol 1–28. https://doi.org/10.1113/jp280324
Nagai K, Yamada M, Uemura K, Yamada Y, Ichihashi N, Tsuboyama T (2011) Differences in muscle coactivation during postural control between healthy older and young adults. Arch Gerontol Geriatr 53(3):338–343. https://doi.org/10.1016/j.archger.2011.01.003
Nashner LM (1976) Adapting reflexes controlling the human posture. Exp Brain Res 26(1):59–72. https://doi.org/10.1007/BF00235249
Nielsen JB, Kagamihara Y (1993) The regulation of presynaptic inhibition during co-contraction of antagonistic muscles in man. J Physiol (london) 464:575–593
Ozdemir RA, Contreras-Vidal JL, Paloski WH (2018) Cortical control of upright stance in elderly. Mech Ageing Dev 169(October 2017): 19–31. https://doi.org/10.1016/j.mad.2017.12.004
Pai YC, Yang F, Bhatt T, Wang E (2014) Learning from laboratory-induced falling: Long-term motor retention among older adults. Age 36(3):1367–1376. https://doi.org/10.1007/s11357-014-9640-5
Papegaaij S, Taube W, Baudry S, Otten E, Hortobágyi T (2014) Aging causes a reorganization of cortical and spinal control of posture. Frontiers in Aging Neuroscience 6(March):1–15. https://doi.org/10.3389/fnagi.2014.00028
Pedalini MEB, Cruz OLM, Bittar RSM, Lorenzi MC, Grasel SS (2009) Sensory organization test in elderly patients with and without vestibular dysfunction. Acta Otolaryngol 129(9):962–965. https://doi.org/10.1080/00016480802468930
Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88(3):1097–1118
Peterka RJ, Benolken MS (1995) Role of somatosensory and vestibular cues in attenuating visually induced human postural sway. Exp Brain Res 105(1):101–110. https://doi.org/10.1007/BF00242186
Piirainen JM, Linnamo V, Cronin NJ, Avela J (2013) Age-related neuromuscular function and dynamic balance control during slow and fast balance perturbations. J Neurophysiol 110(11):2557–2562. https://doi.org/10.1152/jn.00476.2013
Piitulainen H, Seipäjärvi S, Avela J, Parviainen T, Walker S (2018) Cortical proprioceptive processing is altered by aging. Front Aging Neurosci 10(JUN): 1–13. https://doi.org/10.3389/fnagi.2018.00147
Pyykkö I, Jäntti P, Aalto H (1990) Postural control in elderly subjects. Age Ageing 19(3):215–221. https://doi.org/10.1093/ageing/19.3.215
Quoniam C, Hay L, Roll JPP, Harlay F (1995) Age effects on reflex and postural responses to propriomuscular inputs generated by tendon vibration. J Gerontol Ser A Biol Sci Med Sci 50(3):155–165. https://doi.org/10.1093/gerona/50A.3.B155
Roll JP, Vedel J-P, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res 76(1):213–222. https://doi.org/10.1007/BF00253639
Spiliopoulou SI, Amiridis IG, Hatzitaki V, Patikas DA, Kellis E (2012) Tendon vibration during submaximal isometric strength and postural tasks. Eur J Appl Physiol 112(11):3807–3817. https://doi.org/10.1007/s00421-012-2319-7
Swash M, Fox KP (1972) The effect of age on human skeletal muscle studies of the morphology and innervation of muscle spindles. J Neurol Sci 16(4):417–432. https://doi.org/10.1016/0022-510X(72)90048-2
Takakusaki K (2017) Functional neuroanatomy for posture and gait control. J Movement Dis 10(1): 1–17. https://doi.org/10.14802/jmd.16062
Taylor MW, Taylor JL, Seizova-Cajic T (2017) Muscle vibration-induced illusions: review of contributing factors, taxonomy of illusions and user’s guide. Multisensory Research 30(1):25–63. https://doi.org/10.1163/22134808-00002544
Thompson C, Fung J, Be M (2007) Effects of bilateral Achilles tendon vibration on postural orientation and balance during standing. Clin Neurophysiol 118:2456–2467. https://doi.org/10.1016/j.clinph.2007.08.013
Toosizadeh N, Ehsani H, Miramonte M, Mohler J (2018) Proprioceptive impairments in high fall risk older adults: the effect of mechanical calf vibration on postural balance. Biomed Eng Online 17(1):51. https://doi.org/10.1186/s12938-018-0482-8
Tsai YC, Hsieh LF, Yang S (2014) Age-related changes in posture response under a continuous and unexpected perturbation. J Biomech 47(2):482–490. https://doi.org/10.1016/j.jbiomech.2013.10.047
Turano K, Rubin GS, Herdman SJ, Chee E, Fried LP (1994) Visual stabilization of posture in the elderly: fallers vs. nonfallers. Opt Vis Sci 71(12): 761–769. https://doi.org/10.1097/00006324-199412000-00006
Vaughan SK, Stanley OL, Valdez G (2017) Impact of aging on proprioceptive sensory neurons and intrafusal muscle fibers in mice. J Gerontol Ser A Biol Sci Med Sci 72(6): 771–779. https://doi.org/10.1093/gerona/glw175
Wang Y, Asaka T, Zatsiorsky VM, Latash ML (2006) Muscle synergies during voluntary body sway: Combining across-trials and within-a-trial analyses. Exp Brain Res 174(4):679–693. https://doi.org/10.1007/s00221-006-0513-8
Winter DA (1995) Human balance and posture standing and walking control during.
Woollacott MH, Shumway-Cook A, Nashner LM (1986) Aging and posture control: changes in sensory organization and muscular coordination. Int J Aging Hum Dev 23(2):97–114
Zatsiorsky VM, Duarte M (1999) Instant equilibrium point and its migration in standing tasks: rambling and trembling components of the stabilogram. Mot Control 3(1):28–38. https://doi.org/10.1123/mcj.3.1.28
Acknowledgements
This work was supported by a grant from the State Scholarships Foundation of Greece. The authors are grateful to Dimitris Petrakis for his contribution to the measurements of this study and all the volunteers who kindly participated.
Funding
This study was supported by a grant from the State Scholarships Foundation of Greece (Grant number: MIS 5000432/11405. Grand Recipient: Anastasia Papavasileiou).
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AP carried out the experiment and wrote the first draft. AP and DP conceived the main idea, designed research protocol, assessed the data analysis. DP, VH and LM supervised the experiment. VH contributed to the materials required to assess the experiment. All authors revised / edited the manuscript and approved its final version.
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The experiment was performed in accordance with the Declaration of Helsinki and was approved from the ethics committee of the Aristotle University of Thessaloniki (approval code: 18424/2019).
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Communicated by John G. Semmler.
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Papavasileiou, A., Mademli, L., Hatzitaki, V. et al. Electromyographic responses to unexpected Achilles tendon vibration-induced perturbations during standing in young and older people. Exp Brain Res 240, 1017–1027 (2022). https://doi.org/10.1007/s00221-022-06309-7
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DOI: https://doi.org/10.1007/s00221-022-06309-7