Skip to main content

The effect of proprioceptive acuity variability on motor adaptation in older adults

Experimental Brain Research volume 236, pages 599–608 (2018)Cite this article

Abstract

Motor adaptation requires efficient integration of sensory information with predicted sensory consequences of one’s own action. However, the effect of reduced sensory acuity on motor adaptation in humans remains to be further investigated. Here, we examined the variability of proprioceptive acuity during an arm-position matching task and the pattern of visuomotor adaptation in older and young adults, and determined the relationship between the two variables. The older adults, a known example of impaired proprioceptive acuity, exhibited greater trial-to-trial variability during the arm-position matching task as compared with the young adults. Furthermore, the older adults showed a slower rate of adaptation to a 30° visuomotor rotation during targeted reaching movements, as well as larger movement errors in the later phase of adaptation, than the young adults. Our correlation analyses indicated a negative association between the variability in proprioceptive acuity and the rate of visuomotor adaptation in the older adults; and no association was observed in the young adults. These findings point to a possibility that an increase in the variability of proprioceptive acuity due to aging may weaken the integration of predicted and actual sensory feedback, which in turn may result in poor visuomotor adaptation in older adults.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Allison T, Hume AL, Wood CC, Goff WR (1984) Developmental and aging changes in somatosensory, auditory and visual evoked potentials. Electroencephalogr Clin Neurophysiol 58:14–24

    CAS  Article  PubMed  Google Scholar 

  • Aydog ST, Korkusuz P, Doral MN, Tetik O, Demirel HA (2006) Decrease in the numbers of mechanoreceptors in rabbit ACL: the effects of ageing. Knee Surg Sports Traumatol Arthrosc 14:325–329

    Article  PubMed  Google Scholar 

  • Bastian AJ (2008) Understanding sensorimotor adaptation and learning for rehabilitation. Curr Opin Neurol 21:628

    Article  PubMed  PubMed Central  Google Scholar 

  • Burge J, Ernst MO, Banks MS (2008) The statistical determinants of adaptation rate in human reaching. J Vis 8:20–20

    Article  PubMed  PubMed Central  Google Scholar 

  • Burke JR, Schutten MC, Koceja DM, Kamen G (1996) Age-dependent effects of muscle vibration and the Jendrassik maneuver on the patellar tendon reflex response. Arch Phys Med Rehabil 77:600–604

    CAS  Article  PubMed  Google Scholar 

  • Clamann HP (1969) Statistical analysis of motor unit firing patterns in a human skeletal muscle. Biophys J 9:1233–1251

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Coq J, Xerri C (2000) Age-related alteration of the forepaw representation in the rat primary somatosensory cortex. Neuroscience 99:403–411

    CAS  Article  PubMed  Google Scholar 

  • Coq J, Xerri C (2001) Sensorimotor experience modulates age-dependent alterations of the forepaw representation in the rat primary somatosensory cortex. Neuroscience 104:705–715

    CAS  Article  PubMed  Google Scholar 

  • Cressman EK, Salomonczyk D, Henriques DY (2010) Visuomotor adaptation and proprioceptive recalibration in older adults. Exp Brain Res 205:533–544

    Article  PubMed  Google Scholar 

  • Darling WG, Cooke JD, Brown SH (1989) Control of simple arm movements in elderly humans. Neurobiol Aging 10:149–157

    CAS  Article  PubMed  Google Scholar 

  • Diedrichsen J, Verstynen T, Lehman SL, Ivry RB (2005) Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. J Neurophysiol 93:801–812

    Article  PubMed  Google Scholar 

  • Donchin O, Francis JT, Shadmehr R (2003) Quantifying generalization from trial-by-trial behavior of adaptive systems that learn with basis functions: theory and experiments in human motor control. J Neurosci 23:9032–9045

    CAS  PubMed  Google Scholar 

  • Faulkner JA, Larkin LM, Claflin DR, Brooks SV (2007) Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharmacol Physiol 34:1091–1096

    CAS  Article  PubMed  Google Scholar 

  • Fernandez-Ruiz J, Hall C, Vergara P, Diaz R (2000) Prism adaptation in normal aging: slower adaptation rate and larger aftereffect. Brain Res Cogn Brain Res 9:223–226

    CAS  Article  PubMed  Google Scholar 

  • Fernandez-Ruiz J, Wong W, Armstrong IT, Flanagan JR (2011) Relation between reaction time and reach errors during visuomotor adaptation. Behav Brain Res 219:8–14

    Article  PubMed  Google Scholar 

  • Ferrell WR, Crighton A, Sturrock RD (1992a) Position sense at the proximal interphalangeal joint is distorted in patients with rheumatoid arthritis of finger joints. Exp Physiol 77:675–680

    CAS  Article  PubMed  Google Scholar 

  • Ferrell WR, Crighton A, Sturrock RD (1992b) Age-dependent changes in position sense in human proximal interphalangeal joints. Neuroreport 3:259–261

    CAS  Article  PubMed  Google Scholar 

  • Galea JM, Vazquez A, Pasricha N, de Xivry JJ, Celnik P (2011) Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb Cortex 21:1761–1770

    Article  PubMed  Google Scholar 

  • Gibo TL, Criscimagna-Hemminger SE, Okamura AM, Bastian AJ (2013) Cerebellar motor learning: are environment dynamics more important than error size? J Neurophysiol 110:322–333

    Article  PubMed  PubMed Central  Google Scholar 

  • Goble DJ, Coxon JP, Van Impe A, Geurts M, Van Hecke W, Sunaert S, Wenderoth N, Swinnen SP (2012) The neural basis of central proprioceptive processing in older versus younger adults: an important sensory role for right putamen. Hum Brain Mapp 33:895–908

    Article  PubMed  Google Scholar 

  • Goble DJ, Coxon JP, Wenderoth N, Van Impe A, Swinnen SP (2009) Proprioceptive sensibility in the elderly: degeneration, functional consequences and plastic-adaptive processes. Neurosci Biobehav Rev 33:271–278

    Article  PubMed  Google Scholar 

  • Godde B, Berkefeld T, David-Jürgens M, Dinse H (2002) Age-related changes in primary somatosensory cortex of rats: evidence for parallel degenerative and plastic-adaptive processes. Neurosci Biobehav Rev 26:743–752

    Article  PubMed  Google Scholar 

  • Good C, Johnsrude I, Ashburner J, Henson R, Friston K, Frackowiak R (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21–36

    CAS  Article  PubMed  Google Scholar 

  • Haith AM, Krakauer JW (2013) Model-based and model-free mechanisms of human motor learning. Adv Exp Med Biol 782:1–21

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamzey RJ, Kirk EM, Vasudevan EV (2016) Gait speed influences aftereffect size following locomotor adaptation, but only in certain environments. Exp Brain Res 234:1479–1490

    Article  PubMed  Google Scholar 

  • Harrington DL, Haaland KY (1992) Skill learning in the elderly: diminished implicit and explicit memory for a motor sequence. Psychol Aging 7:425

    CAS  Article  PubMed  Google Scholar 

  • Heuer H, Hegele M (2014) Age-related variations of visuo-motor adaptation beyond explicit knowledge. Front Aging Neurosci 6:152

    Article  PubMed  PubMed Central  Google Scholar 

  • Heuninckx S, Wenderoth N, Debaere F, Peeters R, Swinnen SP (2005) Neural basis of aging: the penetration of cognition into action control. J Neurosci 25:6787–6796

    CAS  Article  PubMed  Google Scholar 

  • Heuninckx S, Wenderoth N, Swinnen SP (2008a) Age-related reduction in the differential pathways involved in internal and external movement generation. Neurobiol Aging 31:301–314

    Article  Google Scholar 

  • Heuninckx S, Wenderoth N, Swinnen SP (2008b) Systems neuroplasticity in the aging brain: recruiting additional neural resources for successful motor performance in elderly persons. J Neurosci 28:91–99

    CAS  Article  PubMed  Google Scholar 

  • Howard JH, Howard DV (1997) Age differences in implicit learning of higher order dependencies in serial patterns. Psychol Aging 12:634–656

    Article  PubMed  Google Scholar 

  • Huang VS, Haith A, Mazzoni P, Krakauer JW (2011) Rethinking motor learning and savings in adaptation paradigms: model-free memory for successful actions combines with internal models. Neuron 70:787–801

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hurley MV, Rees J, Newham DJ (1998) Quadriceps function, proprioceptive acuity and functional performance in healthy young, middle-aged and elderly subjects. Age Ageing 27:55–62

    CAS  Article  PubMed  Google Scholar 

  • Izawa J, Shadmehr R (2008) On-line processing of uncertain information in visuomotor control. J Neurosci 28:11360–11368

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Izawa J, Criscimagna-Hemminger SE, Shadmehr R (2012) Cerebellar contributions to reach adaptation and learning sensory consequences of action. J Neurosci 32:4230–4239

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kaasinen V, Rinne JO (2002) Functional imaging studies of dopamine system and cognition in normal aging and Parkinson’s disease. Neurosci Biobehav Rev 26:785–793

    CAS  Article  PubMed  Google Scholar 

  • Kalisch T, Kattenstroth JC, Kowalewski R, Tegenthoff M, Dinse HR (2012) Age-related changes in the joint position sense of the human hand. Clin Interv Aging 7:499–507

    Article  PubMed  PubMed Central  Google Scholar 

  • Kararizou E, Manta P, Kalfakis N, Vassilopoulos D (2005) Morphometric study of the human muscle spindle. Anal Quant Cytol Histol 27:1–4

    PubMed  Google Scholar 

  • Kim GH, Suzuki S, Kanda K (2007) Age-related physiological and morphological changes of muscle spindles in rats. J Physiol 582:525–538

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Körding KP, Wolpert DM (2004) Bayesian integration in sensorimotor learning. Nature 427:244–247

    Article  PubMed  Google Scholar 

  • Körding KP, Wolpert DM (2006) Bayesian decision theory in sensorimotor control. Trends Cogn Sci 10:319–326

    Article  PubMed  Google Scholar 

  • Körding KP, Tenenbaum JB, Shadmehr R (2007) The dynamics of memory as a consequence of optimal adaptation to a changing body. Nat neurosci 10:779–786

    Article  PubMed  PubMed Central  Google Scholar 

  • Korenberg AT, Ghahramani Z (2002) A Bayesian view of motor adaptation. Curr Psychol Cogn 21:537–564

    Google Scholar 

  • Lei Y, Bao S, Wang J (2016) The combined effects of action observation and passive proprioceptive training on adaptive motor learning. Neuroscience 331:91–98

    CAS  Article  PubMed  Google Scholar 

  • Liu J, Eriksson P, Thornell L, Pedrosa-Domellöf F (2005) Fiber content and myosin heavy chain composition of muscle spindles in aged human biceps brachii. J Histochem Cytochem 53:445–454

    CAS  Article  PubMed  Google Scholar 

  • Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT (1996) Throwing while looking through prisms. Brain 119:1183–1198

    Article  PubMed  Google Scholar 

  • Maschke M, Gomez CM, Ebner TJ, Konczak J (2004) Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J Neurophysiol 91:230–238

    Article  PubMed  Google Scholar 

  • Mawase F, Bar-Haim S, Joubran K, Rubin L, Karniel A, Shmuelof L (2016) Increased adaptation rates and reduction in trial-by-trial variability in subjects with cerebral palsy following a multi-session locomotor adaptation training. Front Hum Neurosci 10:203

    Article  PubMed  PubMed Central  Google Scholar 

  • Morton SM, Bastian AJ (2006) Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci 26:9107–9116

    CAS  Article  PubMed  Google Scholar 

  • Pratt J, Chasteen AL, Abrams RA (1994) Rapid aimed limb movements: age differences and practice effects in component submovements. Psychol Aging 9:325

    CAS  Article  PubMed  Google Scholar 

  • Quiton R, Roys S, Zhuo J, Keaser M, Gullapalli R, Greenspan J (2007) Age related changes in nociceptive processing in the human brain. Ann N Y Acad Sci 1097:175–178

    Article  PubMed  Google Scholar 

  • Raz N, Rodrigue K (2006) Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev 30:730–748

    Article  PubMed  Google Scholar 

  • Ruch FL (1934) The differentiative effects of age upon human learning. J Gen Psychol 11:261–286

    Article  Google Scholar 

  • Sanes JN, Dimitrov B, Hallett M (1990) Motor learning in patients with cerebellar dysfunction. Brain 113:103–120

    Article  PubMed  Google Scholar 

  • Schutz RW, Roy EA (1973) Absolute error: The devil in disguise. J Mot Behav 5:141–153

    CAS  Article  PubMed  Google Scholar 

  • Seidler RD (2006) Differential effects of age on sequence learning and sensorimotor adaptation. Brain Res Bull 70:337–346

    Article  PubMed  Google Scholar 

  • Seidler RD (2007) Aging affects motor learning but not savings at transfer of learning. Learn Mem 14:17

    Article  PubMed  Google Scholar 

  • Seidler RD, Alberts JL, Stelmach GE (2002) Changes in multi-joint performance with age. Mot Control 6:19–31

    Article  Google Scholar 

  • Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB (2010) Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev 34:721–733

    CAS  Article  PubMed  Google Scholar 

  • Seidler-Dobrin RD, Stelmach GE (1998) Persistence in visual feedback control by the elderly. Exp Brain Res 119:467–474

    CAS  Article  PubMed  Google Scholar 

  • Shadmehr R, Smith MA, Krakauer JW (2010) Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci 33:89–108

    CAS  Article  PubMed  Google Scholar 

  • Shaffer S, Harrison A (2007) Aging of the somatosensory system: a translational perspective. Phys Ther 87:193–207

    Article  PubMed  Google Scholar 

  • Singh P, Jana S, Ghosal A, Murthy A (2016) Exploration of joint redundancy but not task space 13 variability facilitates supervised motor learning. Proc Natl Acad Sci USA 113:14414–14419

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Smith MA, Shadmehr R (2005) Intact ability to learn internal models of arm dynamics in Huntington’s disease but not cerebellar degeneration. J Neurophysiol 93:2809–2821

    Article  PubMed  Google Scholar 

  • Spengler F, Godde B, Dinse H (1995) Effects of ageing on topographic organization of somatosensory cortex. Neuroreport 6:469–473

    CAS  Article  PubMed  Google Scholar 

  • Spirduso W (1975) Reaction and movement time as a function of age and physical activity level. J Gerontol 30:435–440

    CAS  Article  PubMed  Google Scholar 

  • 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 16:417–432

    CAS  Article  PubMed  Google Scholar 

  • Thoroughman KA, Shadmehr R (2000) Learning of action through adaptive combination of motor primitives. Nature 407:742–747

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Trojaborg W (1976) Motor and sensory conduction in the musculocutaneous nerve. J Neurol Neurosurg Psychiatry 39:890–899

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Tseng YW, Diedrichsen J, Krakauer JW, Shadmehr R, Bastian AJ (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98:54–62

    Article  PubMed  Google Scholar 

  • Vaziri S, Diedrichsen J, Shadmehr R (2006) Why does the brain predict sensory consequences of oculomotor commands? Optimal integration of the predicted and the actual sensory feedback. J Neurosci 26:4188–4197

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Verhaeghen P, Salthouse T (1997) Meta-analyses of age-cognition relations in adulthood: estimates of linear and nonlinear age effects and structural models. Psychol Bull 122:231–249

    CAS  Article  PubMed  Google Scholar 

  • Verschueren SM, Brumagne S, Swinnen SP, Cordo PJ (2002) The effect of aging on dynamic position sense at the ankle. Behav Brain Res 136:593–603

    CAS  Article  PubMed  Google Scholar 

  • Wang J, Sainburg RL (2006) Interlimb transfer of visuomotor rotations depends on handedness. Exp Brain Res 175:223–230

    Article  PubMed  Google Scholar 

  • Wang J, Przybyla A, Wuebbenhorst K, Haaland KY, Sainburg RL (2011) Aging reduces asymmetries in interlimb transfer of visuomotor adaptation. Exp Brain Res 210:283–290

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang J, Lei Y, Binder JR (2015) Performing a reaching task with one arm while adapting to a visuomotor rotation with the other can lead to complete transfer of motor learning across the arms. J Neurophysiol 113:2302–2308

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang J, D’Amato A, Bambrough J, Swartz AM, Miller NE (2016) A positive association between active lifestyle and hemispheric lateralization for motor control and learning in older adults. Exp Brain Res 314:38–44

    Article  Google Scholar 

  • Warabi T, Noda H, Kato T (1986) Effect of aging on sensorimotor functions of eye and hand movements. Exp Neurol 92:686–697

    CAS  Article  PubMed  Google Scholar 

  • Wei K, Körding K (2010) Uncertainty of feedback and state estimation determines the speed of motor adaptation. Front Comput Neurosci 4:11

    PubMed  PubMed Central  Google Scholar 

  • Wishart LR, Lee TD (1997) Effects of aging and reduced relative frequency of knowledge of results on learning a motor skill. Percept Mot Skills 84:1107–1122

    CAS  Article  PubMed  Google Scholar 

  • Wolpe N, Ingram JN, Tsvetanov KA, Geerligs L, Kievit RA, Henson RN, Wolpert DM, Rowe JB (2016) Ageing increases reliance on sensorimotor prediction through structural and functional differences in frontostriatal circuits. Nat Commun 7: 13034

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1880

    CAS  Article  PubMed  Google Scholar 

  • Wolpert DM, Diedrichsen J, Flanagan JR (2011) Principles of sensorimotor learning. Nat Rev Neurosci 12:739–751

    CAS  Article  PubMed  Google Scholar 

  • Wong JD, Kistemaker DA, Chin A, Gribble PL (2012) Can proprioceptive training improve motor learning? J Neurophysiol 108:3313–3321

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu HG, Miyamoto YR, Castro LN, Ölveczky BP, Smith MA (2014) Temporal structure of motor variability is dynamically regulated and predicts motor learning ability. Nat Neurosci 17:312–321

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurological Surgery, The Miami Project to Cure Paralysis, University of Miami, Miami, FL, 33136, USA

    Yuming Lei

  2. Department of Kinesiology, University of Wisconsin-Milwaukee, Milwaukee, WI, 53201, USA

    Jinsung Wang

Authors
  1. Yuming Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jinsung Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuming Lei.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lei, Y., Wang, J. The effect of proprioceptive acuity variability on motor adaptation in older adults. Exp Brain Res 236, 599–608 (2018). https://doi.org/10.1007/s00221-017-5150-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-017-5150-x

Keywords

  • Aging
  • Motor learning
  • Visuomotor rotation
  • Proprioception
  • Trial-to-trial variability