Experimental Brain Research

, Volume 180, Issue 4, pp 693–704 | Cite as

Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement

  • Daniel J. Goble
  • Susan H. BrownEmail author
Research Article


Whereas the majority of studies regarding upper limb asymmetries in motor performance have focused on preferred arm dominance for producing motor output, studies exploring the role of sensory feedback have suggested that the preferred and non-preferred arms are specialized for different aspects of movement. A recent study by Goble et al. (2006) found evidence of a non-preferred left arm (and presumably right hemisphere) proprioceptive dominance for a target matching task that required subjects to both memorize and transfer across hemispheres proprioceptive target information. This paradigm contrasted previous studies of proprioceptive matching asymmetry that explored only memory-based matching and produced equivocal results. The purpose of the present study, therefore, was to examine task-dependent asymmetries in proprioceptive matching performance, including differences related to active versus passive presentation of the matching target. It was found that the non-preferred left arm of right handers matched target elbow angles more accurately than the preferred arm, but only in the matching condition that required both memory and interhemispheric transfer. Task-dependent asymmetries were not affected by the mode of target presentation and assessment of matching kinematics revealed differences in strategy for both the speed and smoothness of targeted movements. Taken together, these results suggest that the non-preferred arm/hemisphere system is specialized for the processing of movement-related proprioceptive feedback.


Handedness Kinematics Hemispheric specialization Human movement 



Special thanks to A Downing for assistance with data collection and analysis aspects of this project, and B Skvarla for the graphic design of Fig. 1.


  1. Adamovich SV, Berkinblit MB, Fookson O, Poizner H (1998) Pointing in 3D space to remembered targets. I. Kinesthetic versus visual target presentation. J Neurophysiol 79:2833–2846PubMedGoogle Scholar
  2. Adamovich SV, Berkinblit MB, Fookson O, Poizner H (1999) Pointing in 3D space to remembered targets. II. Effects of movement speed toward kinesthetically defined targets. Exp Brain Res 125:200–210PubMedCrossRefGoogle Scholar
  3. Almeida GL, Hong D, Corcos D, Gottlieb GL (1995) Organizing principles for voluntary movement: extending single-joint rules. J Neurophysiol 74(4):1374–1381PubMedGoogle Scholar
  4. Annett M (1998) Handedness and cerebral dominance: the right shift theory. J Neuropsychiatry Clin Neurosci 10:459–469PubMedGoogle Scholar
  5. Annett J, Annett M, Hudson PT, Turner A (1979) The control of movement in the preferred and non-preferred hands. Q J Exp Psychol 31:641–652PubMedGoogle Scholar
  6. Bagesteiro LB, Sainburg RL (2002) Handedness: dominant arm advantages in control of limb dynamics. J Neurophysiol 88:2408–2421PubMedCrossRefGoogle Scholar
  7. Boulinguez P, Nougier V, Velay JL (2001) Manual asymmetries in reaching movement control. I: study of right-handers. Cortex 37:101–122PubMedGoogle Scholar
  8. Brouwer B, Sale MV, Nordstrom MA (2001) Asymmetry of motor cortex excitability during a simple motor task: relationships with handedness and manual performance. Exp Brain Res 138:467–476PubMedCrossRefGoogle Scholar
  9. Brown SH, Cooke JD (1981) Amplitude- and instruction-dependent modulation of movement-related electromyogram activity in humans. J Physiol 316:97–107PubMedGoogle Scholar
  10. Brown SH, Cooke JD (1984) Initial agonist burst duration depends on movement amplitude. Exp Brain Res 55:523–527PubMedCrossRefGoogle Scholar
  11. Brown SH, Cooke JD (1990) Movement-related phasic muscle activation. I. Relations with temporal profile of movement. J Neurophysiol 63:455–464PubMedGoogle Scholar
  12. Butler AJ, Fink GR, Dohle C, Wunderlich G, Tellmann L, Seitz RJ, Zilles K, Freund HJ (2004) Neural mechanisms underlying reaching for remembered targets cued kinesthetically or visually in left or right hemispace. Hum Brain Mapp 21:165–177PubMedCrossRefGoogle Scholar
  13. Carnahan H (1998) Manual asymmetries in response to rapid target movement. Brain Cogn 37:237–253PubMedCrossRefGoogle Scholar
  14. Chapman CD, Heath MD, Westwood DA, Roy EA (2001) Memory for kinesthetically defined target location: evidence for manual asymmetries. Brain Cogn 46:62–66PubMedCrossRefGoogle Scholar
  15. Chokron S, Colliot P, Atzeni T, Bartolomeo P, Ohlmann T (2004) Active versus passive proprioceptive straight-ahead pointing in normal subjects. Brain Cogn 55:290–294PubMedCrossRefGoogle Scholar
  16. Colley A (1984) Spatial location judgements by right and left-handers. Cortex 20:47–53PubMedGoogle Scholar
  17. Coren S (1993) Measurement of handedness via self-report: the relationship between brief and extended inventories. Percept Mot Skills 76:1035–1042PubMedGoogle Scholar
  18. Coren S (1996) Pathological causes and consequences of left-handedness. In: Elliott D, Roy EA (eds) Manual asymmetries in motor performance. CRC, Boca Raton, pp 83–98Google Scholar
  19. Coren S, Porac C (1977) Fifty centuries of right-handedness: the historical record. Science 198:631–632PubMedCrossRefGoogle Scholar
  20. Dassonville P, Zhu XH, Uurbil K, Kim SG, Ashe J (1997) Functional activation in motor cortex reflects the direction and the degree of handedness. Proc Natl Acad Sci USA 94:14015–14018PubMedCrossRefGoogle Scholar
  21. Elliott D, Weeks DJ, Jones R (1986) Lateral asymmetries in finger-tapping by adolescents and young adults with Down syndrome. Am J Ment Defic 90:472–475PubMedGoogle Scholar
  22. Elliott D, Heath M, Binsted G, Ricker KL, Roy EA, Chua R (1999) Goal-directed aiming: correcting a force-specification error with the right and left hands. J Mot Behav 31:309–324PubMedGoogle Scholar
  23. Fabri M, Polonara G, Del Pesce M, Quattrini A, Salvolini U, Manzoni T (2001) Posterior corpus callosum and interhemispheric transfer of somatosensory information: an fMRI and neuropsychological study of a partially callosotomized patient. J Cogn Neurosci 13:1071–1079PubMedCrossRefGoogle Scholar
  24. Farthing JP, Chilibeck PD, Binsted G (2005) Cross-education of arm muscular strength is unidirectional in right-handed individuals. Med Sci Sports Exerc 37:1594–1600PubMedCrossRefGoogle Scholar
  25. Flash T, Hogan N (1985) The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci 5:1688–1703PubMedGoogle Scholar
  26. Flash T, Inzelberg R, Schechtman E, Korczyn AD (1992) Kinematic analysis of upper limb trajectories in Parkinson’s disease. Exp Neurol 118:215–226PubMedCrossRefGoogle Scholar
  27. Flowers K (1975) Handedness and controlled movement. Br J Psychol 66:39–52PubMedGoogle Scholar
  28. Gandevia SC, McCloskey DI, Burke D (1992) Kinaesthetic signals and muscle contraction. Trends Neurosci 15:62–65PubMedCrossRefGoogle Scholar
  29. Gilbert AN, Wysocki CJ (1992) Hand preference and age in the United States. Neuropsychologia 30:601–608PubMedCrossRefGoogle Scholar
  30. Goble DJ, Lewis CA, Hurvitz EA, Brown SH (2005) Development of upper limb proprioceptive accuracy in children and adolescents. Hum Mov Sci 24:155–170PubMedCrossRefGoogle Scholar
  31. Goble DJ, Lewis CA, Brown SH (2006) Upper limb asymmetries in the utilization of proprioceptive feedback. Exp Brain Res 168:307–311PubMedCrossRefGoogle Scholar
  32. Gordon J, Ghilardi MF, Ghez C (1994) Accuracy of planar reaching movements. I. Independence of direction and extent variability. Exp Brain Res 99(1):97–111PubMedCrossRefGoogle Scholar
  33. Granit R (1975) The functional role of the muscle spindles—facts and hypotheses. Brain 98:531–556PubMedCrossRefGoogle Scholar
  34. Gribble PL, Ostry DJ. (1999) Compensation for interaction torques during single- and multijoint limb movement. J Neurophysiol 82:2310–2326PubMedGoogle Scholar
  35. Haaland KY, Harrington D (1989a) The role of the hemispheres in closed loop movements. Brain Cogn 9:158–180CrossRefGoogle Scholar
  36. Haaland KY, Harrington DL (1989b) Hemispheric control of the initial and corrective components of aiming movements. Neuropsychologia 27:961–969CrossRefGoogle Scholar
  37. Haaland KY, Harrington DL (1994) Limb-sequencing deficits after left but not right hemisphere damage. Brain Cogn 24:104–122PubMedCrossRefGoogle Scholar
  38. Harris LJ (1990) Cultural influences on handedness: historical and contemporary theory and evidence. In: Coren S (ed) Left-handedness: behavioral Implications and anomalies. Advances in psychology, vol 67. North-Holland, Amsterdam, p 195Google Scholar
  39. Heath M, Roy EA (2000) The expression of manual asymmetries following extensive training of the nondominant hand: a kinematic perspective. Brain Cogn 43:252–257PubMedGoogle Scholar
  40. Honda H (1982) Rightward superiority of eye movements in a bimanual aiming task. Q J Exp Psychol A 34:499–513PubMedGoogle Scholar
  41. Honda H (1984) Functional between-hand differences and outflow eye position information. Q J Exp Psychol A 36:75–88PubMedGoogle Scholar
  42. Imanaka K (1989) Effect of starting position on reproduction of movement: further evidence of interference between location and distance information. Percept Mot Skills 68(2):423–34PubMedGoogle Scholar
  43. Imanaka K Abernethy B (1992) Interference between location and distance information in motor short-term memory: the respective roles of direct kinesthetic signals and abstract codes. J Mot Behav 24(3):274–280CrossRefGoogle Scholar
  44. Incel NA, Ceceli E, Durukan PB, Erdem HR, Yorgancioglu ZR (2002) Grip strength: effect of hand dominance. Singapore Med J 43:234–237PubMedGoogle Scholar
  45. Ingram HA, van Donkelaar P, Cole J, Vercher JL, Gauthier GM, Miall RC (2000) The role of proprioception and attention in a visuomotor adaptation task. Exp Brain Res 132:114–126PubMedCrossRefGoogle Scholar
  46. Jones B (1972) Outflow and inflow in movement duplication. Percept Pyschophys 12:95–96Google Scholar
  47. Jones B (1974) Role of central monitoring of efference in short-term memory for movements. J Exp Psychol 102:37–43PubMedCrossRefGoogle Scholar
  48. Ketcham CJ, Seidler RD, Van Gemmert AW, Stelmach GE (2002) Age-related kinematic differences as influenced by task difficulty, target size, and movement amplitude. J Gerontol B Psychol Sci Soc Sci 57:P54–64PubMedGoogle Scholar
  49. Lee D, Port NL, Georgopoulos AP (1997) Manual interception of moving targets. II. On-line control of overlapping submovements. Exp Brain Res 116:421–433PubMedCrossRefGoogle Scholar
  50. Leonard G, Milner B (1991a) Contribution of the right frontal lobe to the encoding and recall of kinesthetic distance information. Neuropsychologia 29:47–58CrossRefGoogle Scholar
  51. Leonard G, Milner B (1991b) Recall of the end-position of examiner-defined arm movements by patients with frontal- or temporal-lobe lesions. Neuropsychologia 29:629–640CrossRefGoogle Scholar
  52. MacKenzie CL, Marteniuk RG, Dugas C, Liske D, Eickmeier B (1987) Three-dimensional movement trajectories in Fitts’ task: implications for control. Q J Exp Psychol Hum Percept 39A:629–647Google Scholar
  53. Marteniuk RG (1973) Retention characteristics of motor short-term memory cues. J Mot Behavior 5:249–259Google Scholar
  54. Marteniuk RG, Shields KW, Campbell S (1972) Amplitude, position, timing and velocity as cues in reproduction of movement. Perceptual Motor Skills 35:51–58Google Scholar
  55. Marzi CA, Bisiacchi P, Nicoletti R (1991) Is interhemispheric transfer of visuomotor information asymmetric? Evidence from a meta-analysis. Neuropsychologia 29:1163–1177PubMedCrossRefGoogle Scholar
  56. McCloskey DI (1978) Kinesthetic sensibility. Physiol Rev 58:763–820PubMedGoogle Scholar
  57. McIntyre J, Stratta F, Droulez J, Lacquaniti F (2000) Analysis of pointing errors reveals properties of data representations and coordinate transformations within the central nervous system. Neural Comput 12:2823–2855PubMedCrossRefGoogle Scholar
  58. Messier J, Adamovich S, Berkinblit M, Tunik E, Poizner H (2003) Influence of movement speed on accuracy and coordination of reaching movements to memorized targets in three-dimensional space in a deafferented subject. Exp Brain Res 150:399–416PubMedGoogle Scholar
  59. Milner TE (1992) A model for the generation of movements requiring endpoint precision. Neuroscience 49(2):487–496PubMedCrossRefGoogle Scholar
  60. Milner TE, Ijaz MM (1990) The effect of accuracy constraints on three-dimensional movement kinematics. Neuroscience 35(2):365–74PubMedCrossRefGoogle Scholar
  61. Morasso P (1981) Spatial control of arm movements. Exp Brain Res 42:223–227PubMedCrossRefGoogle Scholar
  62. Naito E, Roland PE, Grefkes C, Choi HJ, Eickhoff S, Geyer S, Zilles K, Ehrsson HH (2005) Dominance of the right hemisphere and role of area 2 in human kinesthesia. Neurophysiology 93:1020–1034PubMedGoogle Scholar
  63. Nishizawa S (1991) Different pattern of hemisphere specialization between identical kinesthetic spatial and weight discrimination tasks. Neuropsychologia 29:305–312PubMedCrossRefGoogle Scholar
  64. Novak KE, Miller LE, Houk JC (2002) The use of overlapping submovements in the control of rapid hand movements. Exp Brain Res 144:351–364PubMedCrossRefGoogle Scholar
  65. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRefGoogle Scholar
  66. Paillard J, Brouchon M (1968) Active and passive movement in the calibration of position sense. Neurophysiol Spatially Oriented Behavior, pp 37–55Google Scholar
  67. Paillard J, Brouchon M (1974) A proprioceptive contribution to the spatial encoding of position cues for ballistic movements. Brain Res 71:273–284PubMedCrossRefGoogle Scholar
  68. Peters M (1976) Prolonged practice of a simple motor task by preferred and nonpreffered hands. Percept Motor Skills 42:447–450PubMedGoogle Scholar
  69. Peters M, Durding B (1979) Left-handers and right-handers compared on a motor task. J Mot Behav 11:103–111PubMedGoogle Scholar
  70. Petersen P, Petrick M, Connor H, Conklin D (1989) Grip strength and hand dominance: challenging the 10% rule. Am J Occup Ther 43:444–447PubMedGoogle Scholar
  71. Provins KA (1967) Handedness and motor skill. Med J Aust 2:468–470PubMedGoogle Scholar
  72. Provins KA (1997) The specificity of motor skill and manual asymmetry: a review of the evidence and its implications. J Mot Behav 29:183–192PubMedCrossRefGoogle Scholar
  73. Raymond M, Pontier D (2004) Is there geographical variation in human handedness? Laterality 9:35–51PubMedGoogle Scholar
  74. Riolo-Quinn L (1991) Relationship of hand preference to accuracy on a thumb-positioning task. Percept Mot Skills 73:267–273PubMedGoogle Scholar
  75. Rohrer B, Fasoli S, Krebs HI, Hughes R, Volpe B, Frontera WR, Stein J, Hogan N (2002) Movement smoothness changes during stroke recovery. J Neurosci 22:8297–8304PubMedGoogle Scholar
  76. Rothwell JC, Traub MM, Day BL, Obeso JA, Thomas PK, Marsden CD (1982) Manual motor performance in a deafferented man. Brain 105(Pt 3):515–542PubMedCrossRefGoogle Scholar
  77. Roy EA (1978) Role of preselection in memory for movement extent. J Exp Psychol 4:397–408Google Scholar
  78. Roy EA, Elliott D (1983) Manual performance asymmetries and motor control processess: Subject-generated changes in response parameters. Human Mov Sci 2:271–277CrossRefGoogle Scholar
  79. Roy EA, MacKenzie C (1978) Handedness effects in kinesthetic spatial location judgements. Cortex 14:250–258PubMedGoogle Scholar
  80. Roy EA, Kalbfleisch L, Elliott D (1994) Kinematic analyses of manual asymmetries in visual aiming movements. Brain Cogn 24:289–295PubMedCrossRefGoogle Scholar
  81. Sainburg RL (2002) Evidence for a dynamic-dominance hypothesis of handedness. Exp Brain Res 142:241–258PubMedCrossRefGoogle Scholar
  82. Sainburg RL, Kalakanis D (2000) Differences in control of limb dynamics during dominant and nondominant arm reaching. J Neurophysiol 83:2661–2675PubMedGoogle Scholar
  83. Sainburg RL, Schaefer SY (2004) Interlimb differences in control of movement extent. J Neurophysiol 92:1374–1383PubMedCrossRefGoogle Scholar
  84. Sainburg RL, Poizner H, Ghez C (1993) Loss of proprioception produces deficits in interjoint coordination. J Neurophysiol 70:2136–2147PubMedGoogle Scholar
  85. Sainburg RL, Ghilardi MF, Poizner H, Ghez C (1995) Control of limb dynamics in normal subjects and patients without proprioception. J Neurophysiol 73:820–835PubMedGoogle Scholar
  86. Schutz RW, Roy EA (1973) Absolute error: the devil in disguise. J Mot Behav 5(3):141–153Google Scholar
  87. Seidler RD, Alberts JL, Stelmach GE (2002) Changes in multi-joint performance with age. Motor Control 6:19–31PubMedGoogle Scholar
  88. Soechting JF (1984) Effect of target size on spatial and temporal characteristics of a pointing movement in man. Exp Brain Res 54:121–132PubMedCrossRefGoogle Scholar
  89. Soechting JF, Lacquaniti F (1981) Invariant characteristics of a pointing movement in man. J Neurosci 1:710–720PubMedGoogle Scholar
  90. Sperry R, Gazzaniga MS, Bogen JE (1969) Interhemispheric relationships: the neocortical commissures; syndromes of hemisphere disconnection. In: Vinken PJ, Bruyn GW (eds) Handbook of clinical neurology, vol 4. North-Holland, Amsterdam, pp 273–290Google Scholar
  91. Teulings HL, Contreras-Vidal JL, Stelmach GE, Adler CH (1997) Parkinsonism reduces coordination of fingers, wrist, and arm in fine motor control. Exp Neurol 146:159–170PubMedCrossRefGoogle Scholar
  92. Todor JI, Cisneros J (1985) Accommodation to increased accuracy demands by the right and left hands. J Mot Behav 17:355–372PubMedGoogle Scholar
  93. Todor JI, Kyprie PM (1980) Hand differences in the rate and variability of rapid tapping. J Mot Behav 12:57–62PubMedGoogle Scholar
  94. Virji-Babul N, Cooke JD (1995) Influence of joint interactional effects on the coordination of planar two-joint arm movements. Exp Brain Res:103:451–459Google Scholar
  95. Virji-Babul N, Cooke JD, Brown SH (1994) Effects of gravitational forces on single joint arm movements in humans. Exp Brain Res 99:338–346PubMedCrossRefGoogle Scholar
  96. Wang J, Sainburg RL (2004) Interlimb transfer of novel inertial dynamics is asymmetrical. J Neurophysiol 92:349–360PubMedCrossRefGoogle Scholar
  97. Winstein CJ, Pohl PS (1995) Effects of unilateral brain damage on the control of goal-directed hand movements. Exp Brain Res 105:163–174PubMedCrossRefGoogle Scholar
  98. Woodworth RS (1899) The accuracy of voluntary movement. Psychol Rev 3:1–119Google Scholar
  99. Zia S, Cody F, O’Boyle D (2000) Joint position sense is impaired by Parkinson’s disease. Ann Neurol 47:218–228PubMedCrossRefGoogle Scholar
  100. Zia S, Cody FW, O’Boyle DJ (2002) Identification of unilateral elbow-joint position is impaired by Parkinson’s disease. Clin Anat 15:23–31PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Motor Control Laboratory, Division of KinesiologyUniversity of MichiganAnn ArborUSA

Personalised recommendations