The acute effects of action observation on muscle strength/weakness and corticospinal excitability in older adults

Kylie K Harmon, Ryan M Girts, Jason I Pagan, Gabriela Rodriguez, Matt S Stock, Kylie K Harmon, Ryan M Girts, Jason I Pagan, Gabriela Rodriguez, Matt S Stock

Abstract

Muscle weakness is a critical problem facing many older adults. Interventions targeting nervous system plasticity may show promise in enhancing strength. The purpose of this study was to examine the acute effects of action observation on muscular strength characteristics and corticospinal excitability in older adults. Isometric wrist flexion strength characteristics and corticospinal excitability of the first dorsal interosseous (FDI) were measured in 14 older adults (mean age = 73 years) in response to observation of (1) STRONG contractions of the hand/wrist, (2) WEAK contractions of the hand/wrist, and (3) a CONTROL condition. Results from repeated measures analyses of variance (ANOVAs) indicated that rate of torque development at 200 ms (RTD200) significantly decreased from PRE to POST observation for CONTROL and WEAK, but not STRONG. No other ANOVAs were significant. However, effect sizes indicated that maximal voluntary contraction (MVC) peak torque showed moderate declines following WEAK (d = - 0.571) and CONTROL (d = - 0.636), but not STRONG (d = 0.024). Similarly, rate of torque development at 30 (RTD30), 50 (RTD50), and 200 (RTD200) ms showed large declines from PRE to POST after WEAK and CONTROL, but small changes following STRONG. FDI motor-evoked potential (MEP) amplitude tended to increase over time, but these results were variable. There was a pronounced effect from PRE to 8MIN (d = 0.954) during all conditions. Action observation of strong contractions may exert a preservatory effect on muscular strength. More work is needed to determine whether this is modulated by increased corticospinal excitability. The study was prospectively registered (ClinicalTrials.gov Identifier: NCT03946709).

Keywords: Mirror neuron system; Muscular weakness; Neuromuscular system; Transcranial magnetic stimulation.

Conflict of interest statement

The authors declare no conflicts of interests or competing interests.

© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Figures

Fig. 1
Fig. 1
Action observation setup (a). Actions observed included using scissors (b), squeezing a clip (c), crushing cans (d), and squeezing a stress ball (e)
Fig. 2
Fig. 2
PRE to POST test results. a MVC peak torque, b RTD30, c RTD50, d RTD200. All data points represent mean ± SD
Fig. 3
Fig. 3
FDI MEP amplitude throughout action observation conditions. All data points represent mean ± SD

References

    1. Andersen LL, Aagaard P. Influence of maximal muscle strength and intrinsic muscle contractile properties on contractile rate of force development. Eur J Appl Physiol. 2006;96(1):46–52. doi: 10.1007/s00421-005-0070-z.
    1. Avesani M, Formaggio E, Fuggetta G, Fiaschi A, Manganotti P. Corticospinal excitability in human subjects during nonrapid eye movement sleep: single and paired-pulse transcranial magnetic stimulation study. Exp Brain Res. 2008;187(1):17–23. doi: 10.1007/s00221-008-1274-3.
    1. Bastani A, Jaberzadeh S. A higher number of TMS-elicited MEP from a combined hotspot improves intra- and inter-session reliability of the upper limb muscles in healthy individuals. PLoS One. 2012;7(10):e47582. doi: 10.1371/journal.pone.0047582.
    1. Bellelli G, Buccino G, Bernardini B, Padovani A, Trabucchi M. Action observation treatment improves recovery of postsurgical orthopedic patients: evidence for a top-down effect? Arch Phys Med Rehabil. 2010;91(10):1489–1494. doi: 10.1016/j.apmr.2010.07.013.
    1. Briggs AM, Cross MJ, Hoy DG, Sànchez-Riera L, Blyth FM, Woolf AD, March L. Musculoskeletal health conditions represent a global threat to healthy aging: a report for the 2015 World Health Organization world report on ageing and health. Gerontologist. 2016;56(Suppl 2):S243–S255. doi: 10.1093/geront/gnw002.
    1. Carrillo-Garcia P, Garmendia-Prieto B, Cristofori G, Montoya IL, Hidalgo JJ, Feijoo MQ, Cortés JJB, Gómez-Pavón J. Health status in survivors older than 70 years after hospitalization with COVID-19: observational follow-up study at 3 months. Eur Geriatr Med. 2021 doi: 10.1007/s41999-021-00516-1.
    1. Caspers S, Zilles K, Laird AR, Eickhoff SB. ALE meta-analysis of action observation and imitation in the human brain. NeuroImage. 2010;50(3):1148–1167. doi: 10.1016/j.neuroimage.2009.12.112.
    1. Chang K-V, Hsu T-H, Wu W-T, Huang K-C, Han D-S. Is sarcopenia associated with depression? A systematic review and meta-analysis of observational studies. Age Ageing. 2017;46(5):738–746. doi: 10.1093/ageing/afx094.
    1. Christie A, Fling B, Crews RT, Mulwitz LA, Kamen G. Reliability of motor-evoked potentials in the ADM muscle of older adults. J Neurosci Methods. 2007;164(2):320–324. doi: 10.1016/j.jneumeth.2007.05.011.
    1. Clark BC, Manini TM. Sarcopenia ≠ dynapenia. J Gerontol A. 2008;63(8):829–834. doi: 10.1093/gerona/63.8.829.
    1. Clark BC, Manini TM. What is dynapenia? Nutrition. 2012;28(5):495–503. doi: 10.1016/j.nut.2011.12.002.
    1. Clark BC, Taylor JL. Age-related changes in motor cortical properties and voluntary activation of skeletal muscle. Curr Aging Sci. 2011;4(3):192–199. doi: 10.2174/1874609811104030192.
    1. Clark S, Tremblay F, Ste-Marie D. Differential modulation of corticospinal excitability during observation, mental imagery and imitation of hand actions. Neuropsychologia. 2004;42(1):105–112. doi: 10.1016/s0028-3932(03)00144-1.
    1. Clark BC, Mahato NK, Nakazawa M, Law TD, Thomas JS. The power of the mind: the cortex as a critical determinant of muscle strength/weakness. J Neurophysiol. 2014;112(12):3219–3226. doi: 10.1152/jn.00386.2014.
    1. Cohen J. Statistical power analysis for the behavioral sciences. 2. New York: L. Erlbaum Associates; 1988.
    1. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, Boudreau R, Manini TM, Nevitt M, Newman AB, Goodpaster BH, Health, Aging, and Body Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579–1585. doi: 10.3945/ajcn.2009.28047.
    1. Derosiere G, Vassiliadis P, Duque J. Advanced TMS approaches to probe corticospinal excitability during action preparation. Neuroimage. 2020;213:116746. doi: 10.1016/j.neuroimage.2020.116746.
    1. di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G. Understanding motor events: a neurophysiological study. Exp Brain Res. 1992;91(1):176–180. doi: 10.1007/BF00230027.
    1. Di Rienzo F, Joassy P, Kanthack T, MacIntyre TE, Debarnot U, Blache Y, Hautier C, Collet C, Guillot A. Effects of action observation and action observation combined with motor imagery on maximal isometric strength. Neuroscience. 2019;418:82–95. doi: 10.1016/j.neuroscience.2019.08.025.
    1. Doeltgen SH, Ridding MC. Behavioural exposure and sleep do not modify corticospinal and intracortical excitability in the human motor system. Clin Neurophysiol. 2010;121(3):448–452. doi: 10.1016/j.clinph.2009.11.085.
    1. Erim Z, Beg MF, Burke DT, de Luca CJ. Effects of aging on motor-unit control properties. J Neurophysiol. 1999;82(5):2081–2091. doi: 10.1152/jn.1999.82.5.2081.
    1. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol. 1995;73(6):2608–2611. doi: 10.1152/jn.1995.73.6.2608.
    1. Fekih S, Zguira MS, Koubaa A, Masmoudi L, Bragazzi NL, Jarraya M. Effects of motor mental imagery training on tennis service performance during the ramadan fasting: a randomized. Controlled Trial Nutr. 2020;12(4):1035. doi: 10.3390/nu12041035.
    1. Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol. 2000;88(4):1321–1326. doi: 10.1152/jappl.2000.88.4.1321.
    1. Galganski ME, Fuglevand AJ, Enoka RM. Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. J Neurophysiol. 1993;69(6):2108–2115. doi: 10.1152/jn.1993.69.6.2108.
    1. Gerstner GR, Thompson BJ, Rosenberg JG, Sobolewski EJ, Scharville MJ, Ryan ED. Neural and muscular contributions to the age-related reductions in rapid strength. Med Sci Sports Exerc. 2017;49(7):1331–1339. doi: 10.1249/MSS.0000000000001231.
    1. Girts RM, Mota JA, Harmon KK, MacLennan RJ, Stock MS. Vastus lateralis motor unit recruitment thresholds are compressed towards lower forces in older men. J Frailty Aging. 2020;9(4):191–196. doi: 10.14283/jfa.2020.19.
    1. Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61(10):1059–1064. doi: 10.1093/gerona/61.10.1059.
    1. Grosse P, Khatami R, Salih F, Kühn A, Meyer B-U. Corticospinal excitability in human sleep as assessed by transcranial magnetic stimulation. Neurology. 2002;59(12):1988–1991. doi: 10.1212/01.wnl.0000038762.11894.da.
    1. Helm F, Marinovic W, Krüger B, Munzert J, Riek S. Corticospinal excitability during imagined and observed dynamic force production tasks: effortfulness matters. Neuroscience. 2015;290:398–405. doi: 10.1016/j.neuroscience.2015.01.050.
    1. Hétu S, Grégoire M, Saimpont A, Coll M-P, Eugène F, Michon P-E, Jackson PL. The neural network of motor imagery: an ALE meta-analysis. Neurosci Biobehav Rev. 2013;37(5):930–949. doi: 10.1016/j.neubiorev.2013.03.017.
    1. Kamen G, De Luca CJ. Unusual motor unit firing behavior in older adults. Brain Res. 1989;482(1):136–140. doi: 10.1016/0006-8993(89)90550-7.
    1. Kamen G, Sison SV, Du CC, Patten C. Motor unit discharge behavior in older adults during maximal-effort contractions. J Appl Physiol. 1995;79(6):1908–1913. doi: 10.1152/jappl.1995.79.6.1908.
    1. Klass M, Baudry S, Duchateau J. Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions. J Appl Physiol. 2008;104(3):739–746. doi: 10.1152/japplphysiol.00550.2007.
    1. Loporto M, McAllister CJ, Edwards MG, Wright DJ, Holmes PS. Prior action execution has no effect on corticospinal facilitation during action observation. Behav Brain Res. 2012;231(1):124–129. doi: 10.1016/j.bbr.2012.03.009.
    1. Louie GH, Ward MM. Sex disparities in self-reported physical functioning: true differences, reporting bias, or incomplete adjustment for confounding? J Am Geriatr Soc. 2010;58(6):1117–1122. doi: 10.1111/j.1532-5415.2010.02858.x.
    1. Malmstrom TK, Morley JE. SARC-F: a simple questionnaire to rapidly diagnose sarcopenia. J Am Med Dir Assoc. 2013;14(8):531–532. doi: 10.1016/j.jamda.2013.05.018.
    1. Mizuguchi N, Umehara I, Nakata H, Kanosue K. Modulation of corticospinal excitability dependent upon imagined force level. Exp Brain Res. 2013;230(2):243–249. doi: 10.1007/s00221-013-3649-3.
    1. Moritani T, deVries HA. Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med. 1979;58(3):115–130.
    1. Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB. Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol A Biol Sci Med Sci. 2006;61(1):72–77. doi: 10.1093/gerona/61.1.72.
    1. NHIS—National Health Interview Survey (2021). . Accessed 27 Apr 2021
    1. Nojima I, Mima T, Koganemaru S, Thabit MN, Fukuyama H, Kawamata T. Human motor plasticity induced by mirror visual feedback. J Neurosci. 2012;32(4):1293–1300. doi: 10.1523/JNEUROSCI.5364-11.2012.
    1. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113. doi: 10.1016/0028-3932(71)90067-4.
    1. Olmos AA, Stratton MT, Ha PL, Dalton BE, VanDusseldorp TA, Mangine GT, Feito Y, Poisal MJ, Jones JA, Smith TM, Hester GM. Early and late rapid torque characteristics and select physiological correlates in middle-aged and older males. PLoS One. 2020;15(4):e0231907. doi: 10.1371/journal.pone.0231907.
    1. Pasco JA, Williams LJ, Jacka FN, Stupka N, Brennan-Olsen SL, Holloway KL, Berk M. Sarcopenia and the common mental disorders: a potential regulatory role of Skeletal muscle on brain function? Curr Osteoporos Rep. 2015;13(5):351–357. doi: 10.1007/s11914-015-0279-7.
    1. Porro CA, Facchin P, Fusi S, Dri G, Fadiga L. Enhancement of force after action observation: behavioural and neurophysiological studies. Neuropsychologia. 2007;45(13):3114–3121. doi: 10.1016/j.neuropsychologia.2007.06.016.
    1. Ranganathan VK, Siemionow V, Liu JZ, Sahgal V, Yue GH. From mental power to muscle power—gaining strength by using the mind. Neuropsychologia. 2004;42(7):944–956. doi: 10.1016/j.neuropsychologia.2003.11.018.
    1. Rizzolatti G, Fadiga L, Gallese V, Fogassi L. Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res. 1996;3(2):131–141. doi: 10.1016/0926-6410(95)00038-0.
    1. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, Safety of TMS Consensus Group Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol off J Int Fed Clin Neurophysiol. 2009;120(12):2008–2039. doi: 10.1016/j.clinph.2009.08.016.
    1. Salama IM, Turner S, Edwards MG. Automatic priming of grip force following action observation. Q J Exp Psychol. 2011;64(5):833–838. doi: 10.1080/17470218.2011.572172.
    1. Sartori L, Bucchioni G, Castiello U. Motor cortex excitability is tightly coupled to observed movements. Neuropsychologia. 2012;50(9):2341–2347. doi: 10.1016/j.neuropsychologia.2012.06.002.
    1. Sartori L, Xompero F, Bucchioni G, Castiello U. The transfer of motor functional strategies via action observation. Biol Let. 2012;8(2):193–196. doi: 10.1098/rsbl.2011.0759.
    1. Scott M, Taylor S, Chesterton P, Vogt S, Eaves DL. Motor imagery during action observation increases eccentric hamstring force: an acute non-physical intervention. Disabil Rehabil. 2018;40(12):1443–1451. doi: 10.1080/09638288.2017.1300333.
    1. Strafella AP, Paus T. Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. NeuroReport. 2000;11(10):2289–2292. doi: 10.1097/00001756-200007140-00044.
    1. Wong AL, Haith AM, Krakauer JW. Motor planning. Neuroscientist. 2015;21(4):385–398. doi: 10.1177/1073858414541484.
    1. Wrightson JG, Twomey R, Smeeton NJ. Exercise performance and corticospinal excitability during action observation. Front Hum Neurosci. 2016;10:106. doi: 10.3389/fnhum.2016.00106.
    1. Yasui T, Yamaguchi T, Tanabe S, Tatemoto T, Takahashi Y, Kondo K, Kawakami M. Time course of changes in corticospinal excitability induced by motor imagery during action observation combined with peripheral nerve electrical stimulation. Exp Brain Res. 2019;237(3):637–645. doi: 10.1007/s00221-018-5454-5.
    1. Zijdewind I, Toering ST, Bessem B, Van Der Laan O, Diercks RL. Effects of imagery motor training on torque production of ankle plantar flexor muscles. Muscle Nerve. 2003;28(2):168–173. doi: 10.1002/mus.10406.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever