Skip to main content
Top
Published in: BMC Geriatrics 1/2019

Open Access 01-12-2019 | Research article

Age-related deficits in bilateral motor synergies and force coordination

Authors: Nyeonju Kang, Lisa M. Roberts, Clara Aziz, James H. Cauraugh

Published in: BMC Geriatrics | Issue 1/2019

Login to get access

Abstract

Background

Ageing may cause impairments in executing bilateral movement control. This study investigated age-related changes in interlimb force coordination across multiple trials by quantifying bilateral motor synergies based on the uncontrolled manifold hypothesis. Participants completed the trials with and without visual feedback.

Methods

Twenty healthy individuals (10 older adults and 10 young adults) performed 12 isometric force control trials for the two vision conditions at 5% of maximal voluntary contraction. All dependent variables were analyzed in two-way mixed model (Group × Vision Condition; 2 × 2) ANOVAs with repeated measures on the last factor.

Results

The analyses revealed that older adults had greater mean force produced by two hands in both vision conditions (i.e., yes and no visual feedback). Across both vision conditions, the older adult group showed greater asymmetrical force variability (i.e., standard deviation of non-dominant hand > standard deviation of dominant hand) and revealed more positive correlation coefficients between forces produced by two hands as compared with the young adult group. Finally, an index of bilateral motor synergies was significantly greater in young adults than older adults when visual feedback was available.

Conclusion

The current findings indicate that deficits in interlimb force coordination across multiple trials appeared in older adults.
Literature
1.
go back to reference Bowden JL, McNulty PA. The magnitude and rate of reduction in strength, dexterity and sensation in the human hand vary with ageing. Exp Gerontol. 2013;48(8):756–65.CrossRef Bowden JL, McNulty PA. The magnitude and rate of reduction in strength, dexterity and sensation in the human hand vary with ageing. Exp Gerontol. 2013;48(8):756–65.CrossRef
2.
go back to reference Hunter SK, Pereira HM, Keenan KG. The aging neuromuscular system and motor performance. J Appl Physiol. 2016;121(4):982–95.CrossRef Hunter SK, Pereira HM, Keenan KG. The aging neuromuscular system and motor performance. J Appl Physiol. 2016;121(4):982–95.CrossRef
3.
go back to reference Gale CR, Martyn CN, Cooper C, Sayer AA. Grip strength, body composition, and mortality. Int J Epidemiol. 2007;36(1):228–35.CrossRef Gale CR, Martyn CN, Cooper C, Sayer AA. Grip strength, body composition, and mortality. Int J Epidemiol. 2007;36(1):228–35.CrossRef
4.
go back to reference Hortobagyi T, Mizelle C, Beam S, DeVita P. Old adults perform activities of daily living near their maximal capabilities. J Gerontol A Biol Sci Med Sci. 2003;58(5):M453–60.CrossRef Hortobagyi T, Mizelle C, Beam S, DeVita P. Old adults perform activities of daily living near their maximal capabilities. J Gerontol A Biol Sci Med Sci. 2003;58(5):M453–60.CrossRef
5.
go back to reference Scherder E, Dekker W, Eggermont L. Higher-level hand motor function in aging and (preclinical) dementia: its relationship with (instrumental) activities of daily life - a mini-review. Gerontology. 2008;54(6):333–41.CrossRef Scherder E, Dekker W, Eggermont L. Higher-level hand motor function in aging and (preclinical) dementia: its relationship with (instrumental) activities of daily life - a mini-review. Gerontology. 2008;54(6):333–41.CrossRef
6.
go back to reference Kilbreath SL, Heard RC. Frequency of hand use in healthy older persons. Aust J Physiother. 2005;51(2):119–22.CrossRef Kilbreath SL, Heard RC. Frequency of hand use in healthy older persons. Aust J Physiother. 2005;51(2):119–22.CrossRef
7.
go back to reference Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, et al. Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev. 2010;34(5):721–33.CrossRef Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, et al. Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev. 2010;34(5):721–33.CrossRef
8.
go back to reference Verheij S, Muilwijk D, Pel JJ, Van der Cammen TJ, Mattace-Raso FU, Van der Steen J. Visuomotor impairment in early-stage Alzheimer's disease: changes in relative timing of eye and hand movements. J Alzheimers Dis. 2012;30(1):131–43.CrossRef Verheij S, Muilwijk D, Pel JJ, Van der Cammen TJ, Mattace-Raso FU, Van der Steen J. Visuomotor impairment in early-stage Alzheimer's disease: changes in relative timing of eye and hand movements. J Alzheimers Dis. 2012;30(1):131–43.CrossRef
9.
go back to reference Hu XG, Loncharich M, Newell KM. Visual information interacts with neuromuscular factors in the coordination of bimanual isometric force. Exp Brain Res. 2011;209(1):129–38.CrossRef Hu XG, Loncharich M, Newell KM. Visual information interacts with neuromuscular factors in the coordination of bimanual isometric force. Exp Brain Res. 2011;209(1):129–38.CrossRef
10.
go back to reference Kang N, Cauraugh JH. Bilateral synergy as an index of force coordination in chronic stroke. Exp Brain Res. 2017;235(5):1501–9.CrossRef Kang N, Cauraugh JH. Bilateral synergy as an index of force coordination in chronic stroke. Exp Brain Res. 2017;235(5):1501–9.CrossRef
11.
go back to reference Kang N, Cauraugh JH. Coherence and interlimb force control: effects of visual gain. Neurosci Lett. 2018;668:86–91.CrossRef Kang N, Cauraugh JH. Coherence and interlimb force control: effects of visual gain. Neurosci Lett. 2018;668:86–91.CrossRef
12.
go back to reference Hu X, Newell KM. Aging, visual information, and adaptation to task asymmetry in bimanual force coordination. J Appl Physiol. 2011;111(6):1671–80.CrossRef Hu X, Newell KM. Aging, visual information, and adaptation to task asymmetry in bimanual force coordination. J Appl Physiol. 2011;111(6):1671–80.CrossRef
13.
go back to reference Lin CH, Chou LW, Wei SH, Lieu FK, Chiang SL, Sung WH. Influence of aging on bimanual coordination control. Exp Gerontol. 2014;53:40–7.CrossRef Lin CH, Chou LW, Wei SH, Lieu FK, Chiang SL, Sung WH. Influence of aging on bimanual coordination control. Exp Gerontol. 2014;53:40–7.CrossRef
14.
go back to reference Krehbiel LM, Kang N, Cauraugh JH. Age-related differences in bimanual movements: a systematic review and meta-analysis. Exp Gerontol. 2017;98:199–206.CrossRef Krehbiel LM, Kang N, Cauraugh JH. Age-related differences in bimanual movements: a systematic review and meta-analysis. Exp Gerontol. 2017;98:199–206.CrossRef
15.
go back to reference Ranganathan R, Newell KM. Motor synergies: feedback and error compensation within and between trials. Exp Brain Res. 2008;186(4):561–70.CrossRef Ranganathan R, Newell KM. Motor synergies: feedback and error compensation within and between trials. Exp Brain Res. 2008;186(4):561–70.CrossRef
16.
go back to reference Ram N, Rabbitt P, Stollery B, Nesselroade JR. Cognitive performance inconsistency: intraindividual change and variability. Psychol Aging. 2005;20(4):623–33.CrossRef Ram N, Rabbitt P, Stollery B, Nesselroade JR. Cognitive performance inconsistency: intraindividual change and variability. Psychol Aging. 2005;20(4):623–33.CrossRef
17.
go back to reference Latash ML. The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res. 2012;217(1):1–5.CrossRef Latash ML. The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res. 2012;217(1):1–5.CrossRef
18.
go back to reference Sarabon N, Markovic G, Mikulic P, Latash ML. Bilateral synergies in foot force production tasks. Exp Brain Res. 2013;227(1):121–30.CrossRef Sarabon N, Markovic G, Mikulic P, Latash ML. Bilateral synergies in foot force production tasks. Exp Brain Res. 2013;227(1):121–30.CrossRef
19.
go back to reference Latash ML. Motor synergies and the equilibrium-point hypothesis. Mot Control. 2010;14(3):294–322.CrossRef Latash ML. Motor synergies and the equilibrium-point hypothesis. Mot Control. 2010;14(3):294–322.CrossRef
20.
go back to reference Sainburg R, Good D, Przybyla A. Bilateral synergy: a framework for post-stroke rehabilitation. J Neurol Transl Neurosci. 2013;1(3). Sainburg R, Good D, Przybyla A. Bilateral synergy: a framework for post-stroke rehabilitation. J Neurol Transl Neurosci. 2013;1(3).
21.
go back to reference Marchini A, Pereira R, Pedroso W, Christou E, Neto OP. Age-associated differences in motor output variability and coordination during the simultaneous dorsiflexion of both feet. Somatosens Mot Res. 2017;34(2):96–101.CrossRef Marchini A, Pereira R, Pedroso W, Christou E, Neto OP. Age-associated differences in motor output variability and coordination during the simultaneous dorsiflexion of both feet. Somatosens Mot Res. 2017;34(2):96–101.CrossRef
22.
go back to reference Kennedy DM, Christou EA. Greater amount of visual information exacerbates force control in older adults during constant isometric contractions. Exp Brain Res. 2011;213(4):351–61.CrossRef Kennedy DM, Christou EA. Greater amount of visual information exacerbates force control in older adults during constant isometric contractions. Exp Brain Res. 2011;213(4):351–61.CrossRef
23.
go back to reference Tracy BL, Dinenno DV, Jorgensen B, Welsh SJ. Aging, visuomotor correction, and force fluctuations in large muscles. Med Sci Sports Exerc. 2007;39(3):469–79.CrossRef Tracy BL, Dinenno DV, Jorgensen B, Welsh SJ. Aging, visuomotor correction, and force fluctuations in large muscles. Med Sci Sports Exerc. 2007;39(3):469–79.CrossRef
24.
go back to reference Tracy BL, Hitchcock LN, Welsh SJ, Paxton RJ, Feldman-Kothe CE. Visuomotor correction is a robust contributor to force variability during index finger abduction by older adults. Front Aging Neurosci. 2015;7. Tracy BL, Hitchcock LN, Welsh SJ, Paxton RJ, Feldman-Kothe CE. Visuomotor correction is a robust contributor to force variability during index finger abduction by older adults. Front Aging Neurosci. 2015;7.
25.
go back to reference Kang N, Cauraugh JH. Force control improvements in chronic stroke: bimanual coordination and motor synergy evidence after coupled bimanual movement training. Exp Brain Res. 2014;232(2):503–13.CrossRef Kang N, Cauraugh JH. Force control improvements in chronic stroke: bimanual coordination and motor synergy evidence after coupled bimanual movement training. Exp Brain Res. 2014;232(2):503–13.CrossRef
26.
go back to reference Kang N, Cauraugh JH. Bimanual force variability in chronic stroke: with and without visual information. Neurosci Lett. 2015;587:41–5.CrossRef Kang N, Cauraugh JH. Bimanual force variability in chronic stroke: with and without visual information. Neurosci Lett. 2015;587:41–5.CrossRef
27.
go back to reference Agresti A, Finlay B. Statistical methods for the social sciences. New Jersey: Pearson; 2009. Agresti A, Finlay B. Statistical methods for the social sciences. New Jersey: Pearson; 2009.
28.
go back to reference Field A. Discovering statistics using IBM SPSS statistics. Thousand Oaks: SAGE Publications; 2017. Field A. Discovering statistics using IBM SPSS statistics. Thousand Oaks: SAGE Publications; 2017.
29.
go back to reference Parsa B, O'Shea DJ, Zatsiorsky VM, Latash ML. On the nature of unintentional action: a study of force/moment drifts during multifinger tasks. J Neurophysiol. 2016;116(2):698–708.CrossRef Parsa B, O'Shea DJ, Zatsiorsky VM, Latash ML. On the nature of unintentional action: a study of force/moment drifts during multifinger tasks. J Neurophysiol. 2016;116(2):698–708.CrossRef
30.
go back to reference Massie CL, Tracy BL, Malcolm MP. Functional repetitive transcranial magnetic stimulation increases motor cortex excitability in survivors of stroke. Clin Neurophysiol. 2013;124(2):371–8.CrossRef Massie CL, Tracy BL, Malcolm MP. Functional repetitive transcranial magnetic stimulation increases motor cortex excitability in survivors of stroke. Clin Neurophysiol. 2013;124(2):371–8.CrossRef
31.
go back to reference Chen YC, Lin LL, Lin YT, Hu CL, Hwang IS. Variations in static force control and motor unit behavior with error amplification feedback in the elderly. Front Hum Neurosci. 2017;11:538.CrossRef Chen YC, Lin LL, Lin YT, Hu CL, Hwang IS. Variations in static force control and motor unit behavior with error amplification feedback in the elderly. Front Hum Neurosci. 2017;11:538.CrossRef
32.
go back to reference Sainburg RL. Convergent models of handedness and brain lateralization. Front Psychol. 2014;5:1092.CrossRef Sainburg RL. Convergent models of handedness and brain lateralization. Front Psychol. 2014;5:1092.CrossRef
33.
go back to reference Dolcos F, Rice HJ, Cabeza R. Hemispheric asymmetry and aging: right hemisphere decline or asymmetry reduction. Neurosci Biobehav Rev. 2002;26(7):819–25.CrossRef Dolcos F, Rice HJ, Cabeza R. Hemispheric asymmetry and aging: right hemisphere decline or asymmetry reduction. Neurosci Biobehav Rev. 2002;26(7):819–25.CrossRef
34.
go back to reference Kelso JA. Phase transitions and critical behavior in human bimanual coordination. Am J Phys. 1984;246(6 Pt 2):R1000–4. Kelso JA. Phase transitions and critical behavior in human bimanual coordination. Am J Phys. 1984;246(6 Pt 2):R1000–4.
35.
go back to reference Woytowicz E, Whitall J, Westlake KP. Age-related changes in bilateral upper extremity coordination. Curr Geriatr Rep. 2016;5(3):191–9.CrossRef Woytowicz E, Whitall J, Westlake KP. Age-related changes in bilateral upper extremity coordination. Curr Geriatr Rep. 2016;5(3):191–9.CrossRef
36.
go back to reference Fling BW, Walsh CM, Bangert AS, Reuter-Lorenz PA, Welsh RC, Seidler RD. Differential callosal contributions to bimanual control in young and older adults. J Cognitive Neurosci. 2011;23(9):2171–85.CrossRef Fling BW, Walsh CM, Bangert AS, Reuter-Lorenz PA, Welsh RC, Seidler RD. Differential callosal contributions to bimanual control in young and older adults. J Cognitive Neurosci. 2011;23(9):2171–85.CrossRef
37.
go back to reference Fujiyama H, Van Soom J, Rens G, Gooijers J, Leunissen I, Levin O, et al. Age-related changes in frontal network structural and functional connectivity in relation to bimanual movement control. J Neurosci. 2016;36(6):1808–22.CrossRef Fujiyama H, Van Soom J, Rens G, Gooijers J, Leunissen I, Levin O, et al. Age-related changes in frontal network structural and functional connectivity in relation to bimanual movement control. J Neurosci. 2016;36(6):1808–22.CrossRef
38.
go back to reference Seidler RD, Kwak Y, Fling BW, Bernard JA. Neurocognitive mechanisms of error-based motor learning. Adv Exp Med Biol. 2013;782:39–60.CrossRef Seidler RD, Kwak Y, Fling BW, Bernard JA. Neurocognitive mechanisms of error-based motor learning. Adv Exp Med Biol. 2013;782:39–60.CrossRef
39.
go back to reference Boisgontier MP, Cheval B, van Ruitenbeek P, Cuypers K, Leunissen I, Sunaert S, et al. Cerebellar gray matter explains bimanual coordination performance in children and older adults. Neurobiol Aging. 2018;65:109–20.CrossRef Boisgontier MP, Cheval B, van Ruitenbeek P, Cuypers K, Leunissen I, Sunaert S, et al. Cerebellar gray matter explains bimanual coordination performance in children and older adults. Neurobiol Aging. 2018;65:109–20.CrossRef
40.
go back to reference Bernard JA, Seidler RD. Moving forward: age effects on the cerebellum underlie cognitive and motor declines. Neurosci Biobehav Rev. 2014;42:193–207.CrossRef Bernard JA, Seidler RD. Moving forward: age effects on the cerebellum underlie cognitive and motor declines. Neurosci Biobehav Rev. 2014;42:193–207.CrossRef
Metadata
Title
Age-related deficits in bilateral motor synergies and force coordination
Authors
Nyeonju Kang
Lisa M. Roberts
Clara Aziz
James H. Cauraugh
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Geriatrics / Issue 1/2019
Electronic ISSN: 1471-2318
DOI
https://doi.org/10.1186/s12877-019-1285-x

Other articles of this Issue 1/2019

BMC Geriatrics 1/2019 Go to the issue