Skip to main content

Proprioceptively guided reaching movements in 3D space: effects of age, task complexity and handedness

Experimental Brain Research volume 233, pages 631–639 (2015)Cite this article

Abstract

Aging is associated with impaired upper limb proprioceptive acuity, as reflected by decreased position matching accuracy with increasing task complexity and movement extent. Most studies have primarily used single-joint or planar paradigms to examine age-related changes in proprioception. It is unclear whether these changes can be generalized to more complex multi-joint movements, where additional sensory feedback may affect performance. Since age-related declines in cognitive function may impair the ability to integrate multiple sources of sensory feedback, deficits in position matching ability in older adults may persist when tasks are performed in three-dimensional space. The accuracy with which young and older participants reproduced remembered reference hand positions was assessed under different experimental conditions. Participants matched target locations located directly to the front or 45° to the side relative to the midline using the preferred and non-preferred arms. Either the same (i.e., ipsilateral matching) or the opposite (i.e., contralateral matching) arm was used to reproduce the target location. No differences in matching accuracy were found between young and older participants when matching ipsilaterally. When matching contralaterally, accuracy was worse in older participants for target locations located to the side, which may reflect age-related changes in the perception of peripersonal space. In contrast to previous studies, accuracy did not differ between the preferred and non-preferred arms in either group. These results extend previous findings demonstrating age-related impairments in proprioceptively guided arm movements when interhemispheric transfer is required.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Abe O, Aoki S, Hayashi N, Yamada H, Kunimatsu A, Mori H, Yoshikawa T, Okubo T, Ohtomo K (2002) Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol Aging 23(3):433–441

    PubMed  Article  Google Scholar 

  • Adamo DE, Martin BJ, Brown SH (2007) Age-related differences in upper limb proprioceptive acuity. Percept Mot Skills 104:1297–1309

    PubMed  Google Scholar 

  • Adamo DE, Alexander NB, Brown SH (2009) The influence of age and physical activity on upper limb proprioceptive ability. J Aging Phys Act 17:272–293

    PubMed  Google Scholar 

  • Adamovich SV, Berkinblit MB, Fookson O, Poizner H (1999) Pointing in 3D space to remembered targets I: kinesthetic versus visual target presentation. J Neurophysiol 79:2833–2846

    Google Scholar 

  • Bloesch EK, Davoli CC, Abrams RA (2013) Age-related changes in attentional reference frames for peripersonal space. Psychol Sci 24(4):557–561

    PubMed  Article  Google Scholar 

  • Bosco G, Poppele RE, Eian J (2000) Reference frames for spinal proprioception: limb endpoint based or joint-level based? J Neurophysiol 83(5):2931–2945

    CAS  PubMed  Google Scholar 

  • Brauer SG, Woollacott M, Shumway-Cook A (2001) The interacting effects of cognitive demand and recovery of postural stability in balance-impaired elderly persons. J Gerontol A Biol Sci Med Sci 56(8):M489–M496

    CAS  PubMed  Article  Google Scholar 

  • Brooks JL, Della Sala S, Darling S (2014) Representational pseudoneglect: a review. Neuropsychol Rev 24(2):148–165

    PubMed  Article  Google Scholar 

  • Carson RG, Elliott D, Goodman D, Dickinson J (1990) Manual asymmetries in the reproduction of a 3-dimensional spatial location. Neuropsychologia 28(1):99–103

    CAS  PubMed  Article  Google Scholar 

  • Chapman CD, Heath MD, Westwood DA, Roy EA (2001) Memory for kinesthetically defined target location: evidence for manual asymmetries. Brain Cogn 46(1–2):62–66

    CAS  PubMed  Article  Google Scholar 

  • Cordo PJ (1990) Kinesthetic control of a multijoint movement sequence. J Neurophysiol 63(1):161–172

    CAS  PubMed  Google Scholar 

  • Darling WG, Viaene AN, Peterson CR, Schmiedeler JP (2008) Perception of hand motion direction uses a gravitational reference. Exp Brain Res 186(2):237–248

    PubMed  Article  Google Scholar 

  • Fling BW, Peltier SJ, Bo J, Welsh RC, Seidler RD (2011) Age differences in interhemispheric interactions: callosal structure, physiological function, and behavior. Front Neurosci 5:38

  • Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”: a practical method for grading cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198

    CAS  PubMed  Article  Google Scholar 

  • Fuentes CT, Bastian AJ (2010) Where is your arm? Variations in proprioception across space and tasks. J Neurophysiol 103(1):164–171

    PubMed Central  PubMed  Article  Google Scholar 

  • Gandevia SC, Smith JL, Crawford M, Proske U, Taylor JL (2006) Motor commands contribute to human position sense. J Physiol 571(Pt 3):703–710

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Gentili R, Cahouet V, Papaxanthis C (2007) Motor planning of arm movements is direction-dependent in the gravity field. Neuroscience 145(1):20–32

    CAS  PubMed  Article  Google Scholar 

  • Ghafouri M, Lestienne FG (2000) Altered representation of peripersonal space in the elderly human subject: a sensorimotor approach. Neurosci Lett 289(3):193–196

    CAS  PubMed  Article  Google Scholar 

  • Goble DJ, Brown SH (2007) Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement. Exp Brain Res 180(4):693–704

    PubMed  Article  Google Scholar 

  • Goble DJ, Brown SH (2008) The biological and behavioral basis of upper limb asymmetries in sensorimotor performance. Neurosci Biobehav Rev 32(3):598–610

    PubMed  Article  Google Scholar 

  • Goble DJ, Brown SH (2009) Dynamic proprioceptive target matching behavior in the upper limb: effects of speed, task difficulty and arm/hemisphere asymmetries. Behav Brain Res 200(1):7–14

    PubMed  Article  Google Scholar 

  • Goble DJ, Lewis CA, Hurvitz EA, Brown SH (2005) Development of upper limb proprioceptive accuracy in children and adolescents. Hum Movement Sci 24(2):155-170

  • Goble DJ, Lewis CA, Brown SH (2006) Upper limb asymmetries in the utilization of proprioceptive feedback. Exp Brain Res 168(1–2):307–311

    PubMed  Article  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(3):271–278

    PubMed  Article  Google Scholar 

  • Gribble PL, Ostry DJ (1999) Compensation for interaction torques during single- and multijoint limb movement. J Neurophysiol 82(5):2310–2326

    CAS  PubMed  Google Scholar 

  • Haggard P, Wolpert DM (2005) Disorders of body scheme. In: Freund H, Jeannerod M, Hallett M, Leigaruda R (eds) Higher order motor disorders. Oxford University Press, Oxford, pp 261–271

    Google Scholar 

  • Haggard P, Newman C, Blundell J, Andrew H (2000) The perceived position of the hand in space. Percept Psychophys 62(2):363–377

    CAS  PubMed  Article  Google Scholar 

  • Haggard P, Taylor-Clarke M, Kennett S (2003) Tactile perception, cortical representation and the bodily self. Curr Biol 13(5):R170–R173

    CAS  PubMed  Article  Google Scholar 

  • Helms Tillery SI, Flanders M, Soechting JF (1994) Errors in kinesthetic transformations for hand apposition. NeuroReport 6(1):177–181

    Article  Google Scholar 

  • Helms Tillery SI, Soechting JF, Ebner TJ (1996) Somatosensory cortical activity in relation to arm posture: nonuniform spatial tuning. J Neurophysiol 76(4):2423–2438

    Google Scholar 

  • Herter TM, Scott SH, Dukelow SP (2014) Systematic changes in position sense accompany normal aging across adulthood. J Neuroeng Rehabil 11:43. doi:10.1186/1743-0003-11-43

    PubMed Central  PubMed  Article  Google Scholar 

  • Horak FB (2006) Postural orientation and equilibrium: what do we need to know about neural control of balance to prevent falls? Age Ageing 35(Suppl 2):ii7–ii11

    PubMed  Google Scholar 

  • Hultsch DF, MacDonald SW, Dixon RA (2002) Variability in reaction time performance of younger and older adults. J Gerontol B Psychol Sci Soc Sci 57(2):P101–P115

    PubMed  Article  Google Scholar 

  • Jueptner M, Willer C (1998) A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain 121(8):1437–1449

    PubMed  Article  Google Scholar 

  • Karduna AR, Sainburg RL (2012) Similarities in the neural control of the shoulder and elbow joints belie their structural differences. PLoS ONE 7(10):e45837. doi:10.1371/journal.pone.0045837

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • King J, Karduna A (2014) Joint position sense during a reaching task improves at targets located closer to the head but is unaffected by instruction. Exp Brain Res 232(3):865–874

    PubMed  Article  Google Scholar 

  • King J, Harding E, Karduna A (2013) The shoulder and elbow joints and right and left sides demonstrate similar joint position sense. J Mot Behav 45(6):479–486

    PubMed  Article  Google Scholar 

  • Kokmen E, Bossemeyer RW Jr, Williams WJ (1978) Quantitative evaluation of joint motion sensation in an aging population. J Gerontol 33(1):62–67

    CAS  PubMed  Article  Google Scholar 

  • Kuo AD (2005) An optimal state estimation model of sensory integration in human postural balance. J Neural Eng 2(3):S235–S249

    PubMed  Article  Google Scholar 

  • Langan J (2014) Older adults demonstrate greater accuracy in joint position matching using self-guided movements. Hum Mov Sci 36C:97–106

    Article  Google Scholar 

  • Li K, Lindenberger U (2002) Relations between aging sensorimotor and cognitive functions. Neurosci Biobehav Rev 26(7):777–783

    PubMed  Article  Google Scholar 

  • Lin CH, Lien YH, Wang SF, Tsauo JY (2006) Hip and knee proprioception in elite, amateur, and novice tennis players. Am J Phys Med Rehabil 85(3):216–221

    PubMed  Article  Google Scholar 

  • Lovelace EA, Aikens JE (1990) Vision, kinesthesis, and control of hand movement by young and old adults. Percept Mot Skills 70(3 Pt 2):1131–1137

    CAS  PubMed  Article  Google Scholar 

  • McGuire LM, Sabes PN (2009) Sensory transformations and the use of multiple reference frames for reach planning. Nat Neuroscience 12(8):1056–1063

    CAS  Article  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

  • Papaxanthis C, Pozzo T, McIntyre J (2005) Kinematic and dynamic processes for the control of pointing movements in humans revealed by short-term exposure to microgravity. Neuroscience 135(2):371–383

    CAS  PubMed  Article  Google Scholar 

  • Pijnappels M, Kingma I, Wezenberg D, Reurink G, van Dieën JH (2010) Armed against falls: the contribution of arm movements to balance recovery after tripping. Exp Brain Res 201(4):689–699

    PubMed  Article  Google Scholar 

  • Proske U, Gandevia SC (2009) The kinaesthetic senses. J Physiol 587(17):4139–4146

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Przybyla A, Haaland KY, Bagesteiro LB, Sainburg RL (2011) Motor asymmetry reduction in older adults. Neurosci Lett 489(2):99–104

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Rincon-Gonzalez L, Buneo CA, Helms Tillery SI (2011) The proprioceptive map of the arm is systematic and stable, but idiosyncratic. PLoS ONE 6(11):e25214. doi:10.1371/journal.pone.0025214

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Roos PE, McGuigan MP, Kerwin DG, Trewartha G (2008) The role of arm movement in early trip recovery in younger and older adults. Gait Posture 27(2):352–356

    PubMed  Article  Google Scholar 

  • Sainburg RL (2002) Evidence for a dynamic-dominance hypothesis of handedness. Exp Brain Res 142(2):241–258

    PubMed  Article  Google Scholar 

  • Sainburg RL, Poizner H, Ghez C (1993) Loss of proprioception produces deficits in interjoint coordination. J Neurophysiol 70(5):2136–2147

    CAS  PubMed  Google Scholar 

  • Sainburg RL, Ghilardi MF, Poizner H, Ghez C (1995) Control of limb dynamics in normal subjects and patients without proprioception. J Neurophysiol 73(20):820–835

    CAS  PubMed  Google Scholar 

  • Sattin RW (1992) Falls among older persons: a public health perspective. Annu Rev Public Health 13:489–508

    CAS  PubMed  Article  Google Scholar 

  • Shaffer SW, Harrison AL (2007) Aging of the somatosensory system: a translational perspective. Phys Ther 87(2):193–207

    PubMed  Article  Google Scholar 

  • Shetty AK, Shankar MS, Annamalai N (2014) Bimanual coordination: influence of age and gender. J Clin Diagn Res 8(2):15–16

    PubMed Central  PubMed  Google Scholar 

  • Soechting JF, Flanders M (1989) Errors in pointing are due to approximations in sensorimotor transformations. J Neurophysiol 62(2):595–608

    CAS  PubMed  Google Scholar 

  • Sorock GS, Labiner DM (1992) Peripheral neuromuscular dysfunction and falls in an elderly cohort. Am J Epidemiol 136(5):584–591

    CAS  PubMed  Google Scholar 

  • Suganthy J, Raghuram L, Antonisamy B, Vettivel S, Madhavi C, Koshi R (2003) Gender- and age-related differences in the morphology of the corpus callosum. Clin Anat 16(5):396–403

    CAS  PubMed  Article  Google Scholar 

  • van Beers RJ, Sittig AC, van der Gon JJD (1998) The precision of proprioceptive position sense. Exp Brain Res 122(4):367–377

    PubMed  Article  Google Scholar 

  • Verschueren SM, Swinnen SP, Cordo PJ, Dounskaia NV (1999) Proprioceptive control of multijoint movement: bimanual circle drawing. Exp Brain Res 127(2):182–192

    CAS  PubMed  Article  Google Scholar 

  • Vetter P, Goodbody SJ, Wolpert DM (1999) Evidence for an eye-centered spherical representation of the visuomotor map. J Neurophysiol 81(2):935–939

    CAS  PubMed  Google Scholar 

  • Wilson ET, Wong J, Gribble PL (2010) Mapping Proprioception across a 2D horizontal workspace. PLoS ONE 5(7):e11851. doi:10.1371/journal.pone.0011851

    PubMed Central  PubMed  Article  Google Scholar 

  • Winter JA, Allen TJ, Proske U (2005) Muscle spindle signals combine with the sense of effort to indicate limb position. J Physiol 568(3):1035–1046

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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

    CAS  PubMed  Article  Google Scholar 

  • Wright ML, Adamo DE, Brown SH (2011) Age-related declines in the detection of passive wrist movement. Neurosci Lett 500(2):108–112

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Zhang C, Zhu Q, Hua T (2010) Aging of cerebellar Purkinje cells. Cell Tissue Res 341(3):341–347

    PubMed  Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Human Movement Sciences, MOVE Research Institute Amsterdam, VU University, Amsterdam, The Netherlands

    T. S. Schaap & T. W. J. Janssen

  2. Motor Control Laboratory, School of Kinesiology, University of Michigan, Ann Arbor, MI, 48103, USA

    T. I. Gonzales & S. H. Brown

  3. Amsterdam Rehabilitation Research Institute, Reade, The Netherlands

    T. W. J. Janssen

Authors
  1. T. S. Schaap
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. I. Gonzales
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. W. J. Janssen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. H. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. H. Brown.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schaap, T.S., Gonzales, T.I., Janssen, T.W.J. et al. Proprioceptively guided reaching movements in 3D space: effects of age, task complexity and handedness. Exp Brain Res 233, 631–639 (2015). https://doi.org/10.1007/s00221-014-4142-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-014-4142-3

Keywords

  • Aging
  • Proprioception
  • Upper limb
  • Reaching
  • Multi-joint reaching