Abstract
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.
Similar content being viewed by others
References
Adamovich SV, Berkinblit MB, Fookson O, Poizner H (1998) Pointing in 3D space to remembered targets. I. Kinesthetic versus visual target presentation. J Neurophysiol 79:2833–2846
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 125:200–210
Almeida GL, Hong D, Corcos D, Gottlieb GL (1995) Organizing principles for voluntary movement: extending single-joint rules. J Neurophysiol 74(4):1374–1381
Annett M (1998) Handedness and cerebral dominance: the right shift theory. J Neuropsychiatry Clin Neurosci 10:459–469
Annett J, Annett M, Hudson PT, Turner A (1979) The control of movement in the preferred and non-preferred hands. Q J Exp Psychol 31:641–652
Bagesteiro LB, Sainburg RL (2002) Handedness: dominant arm advantages in control of limb dynamics. J Neurophysiol 88:2408–2421
Boulinguez P, Nougier V, Velay JL (2001) Manual asymmetries in reaching movement control. I: study of right-handers. Cortex 37:101–122
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 138:467–476
Brown SH, Cooke JD (1981) Amplitude- and instruction-dependent modulation of movement-related electromyogram activity in humans. J Physiol 316:97–107
Brown SH, Cooke JD (1984) Initial agonist burst duration depends on movement amplitude. Exp Brain Res 55:523–527
Brown SH, Cooke JD (1990) Movement-related phasic muscle activation. I. Relations with temporal profile of movement. J Neurophysiol 63:455–464
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 21:165–177
Carnahan H (1998) Manual asymmetries in response to rapid target movement. Brain Cogn 37:237–253
Chapman CD, Heath MD, Westwood DA, Roy EA (2001) Memory for kinesthetically defined target location: evidence for manual asymmetries. Brain Cogn 46:62–66
Chokron S, Colliot P, Atzeni T, Bartolomeo P, Ohlmann T (2004) Active versus passive proprioceptive straight-ahead pointing in normal subjects. Brain Cogn 55:290–294
Colley A (1984) Spatial location judgements by right and left-handers. Cortex 20:47–53
Coren S (1993) Measurement of handedness via self-report: the relationship between brief and extended inventories. Percept Mot Skills 76:1035–1042
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 83–98
Coren S, Porac C (1977) Fifty centuries of right-handedness: the historical record. Science 198:631–632
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 94:14015–14018
Elliott D, Weeks DJ, Jones R (1986) Lateral asymmetries in finger-tapping by adolescents and young adults with Down syndrome. Am J Ment Defic 90:472–475
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 31:309–324
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 13:1071–1079
Farthing JP, Chilibeck PD, Binsted G (2005) Cross-education of arm muscular strength is unidirectional in right-handed individuals. Med Sci Sports Exerc 37:1594–1600
Flash T, Hogan N (1985) The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci 5:1688–1703
Flash T, Inzelberg R, Schechtman E, Korczyn AD (1992) Kinematic analysis of upper limb trajectories in Parkinson’s disease. Exp Neurol 118:215–226
Flowers K (1975) Handedness and controlled movement. Br J Psychol 66:39–52
Gandevia SC, McCloskey DI, Burke D (1992) Kinaesthetic signals and muscle contraction. Trends Neurosci 15:62–65
Gilbert AN, Wysocki CJ (1992) Hand preference and age in the United States. Neuropsychologia 30:601–608
Goble DJ, Lewis CA, Hurvitz EA, Brown SH (2005) Development of upper limb proprioceptive accuracy in children and adolescents. Hum Mov Sci 24:155–170
Goble DJ, Lewis CA, Brown SH (2006) Upper limb asymmetries in the utilization of proprioceptive feedback. Exp Brain Res 168:307–311
Gordon J, Ghilardi MF, Ghez C (1994) Accuracy of planar reaching movements. I. Independence of direction and extent variability. Exp Brain Res 99(1):97–111
Granit R (1975) The functional role of the muscle spindles—facts and hypotheses. Brain 98:531–556
Gribble PL, Ostry DJ. (1999) Compensation for interaction torques during single- and multijoint limb movement. J Neurophysiol 82:2310–2326
Haaland KY, Harrington D (1989a) The role of the hemispheres in closed loop movements. Brain Cogn 9:158–180
Haaland KY, Harrington DL (1989b) Hemispheric control of the initial and corrective components of aiming movements. Neuropsychologia 27:961–969
Haaland KY, Harrington DL (1994) Limb-sequencing deficits after left but not right hemisphere damage. Brain Cogn 24:104–122
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 195
Heath M, Roy EA (2000) The expression of manual asymmetries following extensive training of the nondominant hand: a kinematic perspective. Brain Cogn 43:252–257
Honda H (1982) Rightward superiority of eye movements in a bimanual aiming task. Q J Exp Psychol A 34:499–513
Honda H (1984) Functional between-hand differences and outflow eye position information. Q J Exp Psychol A 36:75–88
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):423–34
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):274–280
Incel NA, Ceceli E, Durukan PB, Erdem HR, Yorgancioglu ZR (2002) Grip strength: effect of hand dominance. Singapore Med J 43:234–237
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 132:114–126
Jones B (1972) Outflow and inflow in movement duplication. Percept Pyschophys 12:95–96
Jones B (1974) Role of central monitoring of efference in short-term memory for movements. J Exp Psychol 102:37–43
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:P54–64
Lee D, Port NL, Georgopoulos AP (1997) Manual interception of moving targets. II. On-line control of overlapping submovements. Exp Brain Res 116:421–433
Leonard G, Milner B (1991a) Contribution of the right frontal lobe to the encoding and recall of kinesthetic distance information. Neuropsychologia 29:47–58
Leonard G, Milner B (1991b) Recall of the end-position of examiner-defined arm movements by patients with frontal- or temporal-lobe lesions. Neuropsychologia 29:629–640
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:629–647
Marteniuk RG (1973) Retention characteristics of motor short-term memory cues. J Mot Behavior 5:249–259
Marteniuk RG, Shields KW, Campbell S (1972) Amplitude, position, timing and velocity as cues in reproduction of movement. Perceptual Motor Skills 35:51–58
Marzi CA, Bisiacchi P, Nicoletti R (1991) Is interhemispheric transfer of visuomotor information asymmetric? Evidence from a meta-analysis. Neuropsychologia 29:1163–1177
McCloskey DI (1978) Kinesthetic sensibility. Physiol Rev 58:763–820
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 12:2823–2855
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 150:399–416
Milner TE (1992) A model for the generation of movements requiring endpoint precision. Neuroscience 49(2):487–496
Milner TE, Ijaz MM (1990) The effect of accuracy constraints on three-dimensional movement kinematics. Neuroscience 35(2):365–74
Morasso P (1981) Spatial control of arm movements. Exp Brain Res 42:223–227
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 93:1020–1034
Nishizawa S (1991) Different pattern of hemisphere specialization between identical kinesthetic spatial and weight discrimination tasks. Neuropsychologia 29:305–312
Novak KE, Miller LE, Houk JC (2002) The use of overlapping submovements in the control of rapid hand movements. Exp Brain Res 144:351–364
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Paillard J, Brouchon M (1968) Active and passive movement in the calibration of position sense. Neurophysiol Spatially Oriented Behavior, pp 37–55
Paillard J, Brouchon M (1974) A proprioceptive contribution to the spatial encoding of position cues for ballistic movements. Brain Res 71:273–284
Peters M (1976) Prolonged practice of a simple motor task by preferred and nonpreffered hands. Percept Motor Skills 42:447–450
Peters M, Durding B (1979) Left-handers and right-handers compared on a motor task. J Mot Behav 11:103–111
Petersen P, Petrick M, Connor H, Conklin D (1989) Grip strength and hand dominance: challenging the 10% rule. Am J Occup Ther 43:444–447
Provins KA (1967) Handedness and motor skill. Med J Aust 2:468–470
Provins KA (1997) The specificity of motor skill and manual asymmetry: a review of the evidence and its implications. J Mot Behav 29:183–192
Raymond M, Pontier D (2004) Is there geographical variation in human handedness? Laterality 9:35–51
Riolo-Quinn L (1991) Relationship of hand preference to accuracy on a thumb-positioning task. Percept Mot Skills 73:267–273
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 22:8297–8304
Rothwell JC, Traub MM, Day BL, Obeso JA, Thomas PK, Marsden CD (1982) Manual motor performance in a deafferented man. Brain 105(Pt 3):515–542
Roy EA (1978) Role of preselection in memory for movement extent. J Exp Psychol 4:397–408
Roy EA, Elliott D (1983) Manual performance asymmetries and motor control processess: Subject-generated changes in response parameters. Human Mov Sci 2:271–277
Roy EA, MacKenzie C (1978) Handedness effects in kinesthetic spatial location judgements. Cortex 14:250–258
Roy EA, Kalbfleisch L, Elliott D (1994) Kinematic analyses of manual asymmetries in visual aiming movements. Brain Cogn 24:289–295
Sainburg RL (2002) Evidence for a dynamic-dominance hypothesis of handedness. Exp Brain Res 142:241–258
Sainburg RL, Kalakanis D (2000) Differences in control of limb dynamics during dominant and nondominant arm reaching. J Neurophysiol 83:2661–2675
Sainburg RL, Schaefer SY (2004) Interlimb differences in control of movement extent. J Neurophysiol 92:1374–1383
Sainburg RL, Poizner H, Ghez C (1993) Loss of proprioception produces deficits in interjoint coordination. J Neurophysiol 70:2136–2147
Sainburg RL, Ghilardi MF, Poizner H, Ghez C (1995) Control of limb dynamics in normal subjects and patients without proprioception. J Neurophysiol 73:820–835
Schutz RW, Roy EA (1973) Absolute error: the devil in disguise. J Mot Behav 5(3):141–153
Seidler RD, Alberts JL, Stelmach GE (2002) Changes in multi-joint performance with age. Motor Control 6:19–31
Soechting JF (1984) Effect of target size on spatial and temporal characteristics of a pointing movement in man. Exp Brain Res 54:121–132
Soechting JF, Lacquaniti F (1981) Invariant characteristics of a pointing movement in man. J Neurosci 1:710–720
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 273–290
Teulings HL, Contreras-Vidal JL, Stelmach GE, Adler CH (1997) Parkinsonism reduces coordination of fingers, wrist, and arm in fine motor control. Exp Neurol 146:159–170
Todor JI, Cisneros J (1985) Accommodation to increased accuracy demands by the right and left hands. J Mot Behav 17:355–372
Todor JI, Kyprie PM (1980) Hand differences in the rate and variability of rapid tapping. J Mot Behav 12:57–62
Virji-Babul N, Cooke JD (1995) Influence of joint interactional effects on the coordination of planar two-joint arm movements. Exp Brain Res:103:451–459
Virji-Babul N, Cooke JD, Brown SH (1994) Effects of gravitational forces on single joint arm movements in humans. Exp Brain Res 99:338–346
Wang J, Sainburg RL (2004) Interlimb transfer of novel inertial dynamics is asymmetrical. J Neurophysiol 92:349–360
Winstein CJ, Pohl PS (1995) Effects of unilateral brain damage on the control of goal-directed hand movements. Exp Brain Res 105:163–174
Woodworth RS (1899) The accuracy of voluntary movement. Psychol Rev 3:1–119
Zia S, Cody F, O’Boyle D (2000) Joint position sense is impaired by Parkinson’s disease. Ann Neurol 47:218–228
Zia S, Cody FW, O’Boyle DJ (2002) Identification of unilateral elbow-joint position is impaired by Parkinson’s disease. Clin Anat 15:23–31
Acknowledgments
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Goble, D.J., Brown, S.H. Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement. Exp Brain Res 180, 693–704 (2007). https://doi.org/10.1007/s00221-007-0890-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-007-0890-7