Neural motor control differs between bimanual common-goal vs. bimanual dual-goal tasks

  • Wan-wen Liao
  • Jill Whitall
  • Joseph E. Barton
  • Sandy McCombe Waller
Research Article
  • 68 Downloads

Abstract

Coordinating bimanual movements is essential for everyday activities. Two common types of bimanual tasks are common goal, where two arms share a united goal, and dual goal, which involves independent goals for each arm. Here, we examine how the neural control mechanisms differ between these two types of bimanual tasks. Ten non-disabled individuals performed isometric force tasks of the elbow at 10% of their maximal voluntary force in both bimanual common and dual goals as well as unimanual conditions. Using transcranial magnetic stimulation, we concurrently examined the intracortical inhibitory modulation (short-interval intracortical inhibition, SICI) as well as the interlimb coordination strategies utilized between common- vs. dual-goal tasks. Results showed a reduction of SICI in both hemispheres during dual-goal compared to common-goal tasks (dominant hemisphere: P = 0.04, non-dominant hemisphere: P = 0.03) and unimanual tasks (dominant hemisphere: P = 0.001, non-dominant hemisphere: P = 0.001). For the common-goal task, a reduction of SICI was only seen in the dominant hemisphere compared to unimanual tasks (P = 0.03). Behaviorally, two interlimb coordination patterns were identified. For the common-goal task, both arms were organized into a cooperative “give and take” movement pattern. Control of the non-dominant arm affected stabilization of bimanual force (R2 = 0.74, P = 0.001). In contrast, for the dual-goal task, both arms were coupled together in a positive fashion and neither arm affected stabilization of bimanual force (R2 = 0.31, P = 0.1). The finding that intracortical inhibition and interlimb coordination patterns were different based on the goal conceptualization of bimanual tasks has implications for future research.

Keywords

Bimanual coordination Task goal Short-interval intracortical inhibition (SICI) Interlimb force coordination Motor control 

Notes

Acknowledgements

We thank study participants who devoted their time and efforts in this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aramaki Y, Honda M, Okada T, Sadato N (2006) Neural correlates of the spontaneous phase transition during bimanual coordination. Cereb Cortex 16:1338–1348.  https://doi.org/10.1093/cercor/bhj075 CrossRefPubMedGoogle Scholar
  2. Awiszus F, Feistner H, Urbach D, Bostock H (1999) Characterisation of paired-pulse transcranial magnetic stimulation conditions yielding intracortical inhibition or I-wave facilitation using a threshold-hunting paradigm. Exp Brain Res 129:317–324CrossRefPubMedGoogle Scholar
  3. Bailey RR, Klaesner JW, Lang CE (2015) Quantifying real-world upper-limb activity in nondisabled adults and adults with chronic stroke. Neurorehabil Neural Repair 29:969–978CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bäumer T, Dammann E, Bock F, Klöppel S, Siebner H, Münchau A (2007) Laterality of interhemispheric inhibition depends on handedness. Exp Brain Res 180:195–203CrossRefPubMedGoogle Scholar
  5. Cardoso de Oliveira S (2002) The neuronal basis of bimanual coordination: recent neurophysiological evidence and functional models. Acta Psychol (Amst) 110:139–159CrossRefGoogle Scholar
  6. Carson RG (2005) Neural pathways mediating bilateral interactions between the upper limbs. Brain Res Rev 49:641–662.  https://doi.org/10.1016/j.brainresrev.2005.03.005 CrossRefPubMedGoogle Scholar
  7. Cattaert D, Semjen A, Summers JJ (1999) Simulating a neural cross-talk model for between-hand interference during bimanual circle drawing. Biol Cybern 81:343–358.  https://doi.org/10.1007/s004220050567 CrossRefPubMedGoogle Scholar
  8. Chen JT, Lin YY, Shan DE, Wu ZA, Hallett M, Liao KK (2005) Effect of transcranial magnetic stimulation on bimanual movements. J Neurophysiol 93:53–63.  https://doi.org/10.1152/jn.01063.2003 CrossRefPubMedGoogle Scholar
  9. Cohen RG, Sternad D (2009) Variability in motor learning: relocating, channeling and reducing noise. Exp Brain Res 193:69–83.  https://doi.org/10.1007/s00221-008-1596-1 CrossRefPubMedGoogle Scholar
  10. Cunningham DA, Roelle SM, Allexandre D et al (2017) The effect of motor overflow on bimanual asymmetric force coordination. Exp Brain Res 235:1097–1105CrossRefPubMedPubMedCentralGoogle Scholar
  11. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Roshan L, Chen R (2002) The mechanisms of interhemispheric inhibition in the human motor cortex. J Physiol 543:317–326CrossRefPubMedPubMedCentralGoogle Scholar
  12. Davey NJ, Romaiguère P, Maskill DW, Ellaway PH (1994) Suppression of voluntary motor activity revealed using transcranial magnetic stimulation of the motor cortex in man. J Physiol 477:223–235CrossRefPubMedPubMedCentralGoogle Scholar
  13. Diedrichsen J (2007) Optimal task-dependent changes of bimanual feedback control and adaptation. Current biology: CB 17:1675–1679.  https://doi.org/10.1016/j.cub.2007.08.051 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Diedrichsen J, Dowling N (2009) Bimanual coordination as task-dependent linear control policies. Hum Mov Sci 28:334–347.  https://doi.org/10.1016/j.humov.2008.10.003 CrossRefPubMedGoogle Scholar
  15. Diedrichsen J, Hazeltine E, Nurss WK, Ivry RB (2003) The role of the corpus callosum in the coupling of bimanual isometric force pulses. J Neurophysiol 90:2409–2418.  https://doi.org/10.1152/jn.00250.2003 CrossRefPubMedGoogle Scholar
  16. Duque J, Davare M, Delaunay L et al (2010) Monitoring coordination during bimanual movements: where is the mastermind? J Cogn Neurosci 22:526–542.  https://doi.org/10.1162/jocn.2009.21213 CrossRefPubMedGoogle Scholar
  17. Eliasziw M, Donner A (1991) Application of the McNemar test to non-independent matched pair data. Stat Med 10:1981–1991CrossRefPubMedGoogle Scholar
  18. Fisher RA (1915) Frequency distribution of the values of the correlation coefficient in samples from an indefinitely large population. Biometrika 10:507–521Google Scholar
  19. Fisher RJ, Nakamura Y, Bestmann S, Rothwell JC, Bostock H (2002) Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking. Exp Brain Res 143:240–248.  https://doi.org/10.1007/s00221-001-0988-2 CrossRefPubMedGoogle Scholar
  20. Fling BW, Seidler RD (2012) Task-dependent effects of interhemispheric inhibition on motor control. Behav Brain Res 226:211–217.  https://doi.org/10.1016/j.bbr.2011.09.018 CrossRefPubMedGoogle Scholar
  21. Foltys H, Sparing R, Boroojerdi B, Krings T, Meister IG, Mottaghy FM, Topper R (2001) Motor control in simple bimanual movements: a transcranial magnetic stimulation and reaction time study. Clin Neurophysiol 112:265–274CrossRefPubMedGoogle Scholar
  22. Fox PT, Fox JM, Raichle ME, Burde RM (1985) The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. J Neurophysiol 54:348–369CrossRefPubMedGoogle Scholar
  23. Gelfand IM, Latash ML (1998) On the problem of adequate language in motor control. Motor control 2:306–313CrossRefPubMedGoogle Scholar
  24. Grefkes C, Eickhoff SB, Nowak DA, Dafotakis M, Fink GR (2008) Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. Neuroimage 41:1382–1394.  https://doi.org/10.1016/j.neuroimage.2008.03.048 CrossRefPubMedGoogle Scholar
  25. Haaland KY, Prestopnik JL, Knight RT, Lee RR (2004) Hemispheric asymmetries for kinematic and positional aspects of reaching. Brain J Neurol 127:1145–1158.  https://doi.org/10.1093/brain/awh133 CrossRefGoogle Scholar
  26. Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394:780–784.  https://doi.org/10.1038/29528 CrossRefPubMedGoogle Scholar
  27. Heuer H, Spijkers W, Steglich C, Kleinsorge T (2002) Parametric coupling and generalized decoupling revealed by concurrent and successive isometric contractions of distal muscles. Acta Psychol (Amst) 111:205–242CrossRefGoogle Scholar
  28. Hoffman JI (1976) The incorrect use of Chi-square analysis for paired data. Clin Exp Immunol 24:227–229PubMedPubMedCentralGoogle Scholar
  29. Ilic TV, Meintzschel F, Cleff U, Ruge D, Kessler KR, Ziemann U (2002) Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol 545:153–167CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kagerer FA (2016) Asymmetric interference in left-handers during bimanual movements reflects switch in lateralized control characteristics. Exp Brain Res 234:1545–1553CrossRefPubMedGoogle Scholar
  31. Kang N, Cauraugh JH (2014) Bimanual force variability and chronic stroke: asymmetrical hand control. PLoS One 9:e101817.  https://doi.org/10.1371/journal.pone.0101817 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kantak S, McGrath R, Zahedi N (2016) Goal conceptualization and symmetry of arm movements affect bimanual coordination in individuals after stroke. Neurosci Lett 626:86–93.  https://doi.org/10.1016/j.neulet.2016.04.064 CrossRefPubMedGoogle Scholar
  33. Kazennikov O, Perrig S, Wiesendanger M (2002) Kinematics of a coordinated goal-directed bimanual task. Behav Brain Res 134:83–91CrossRefPubMedGoogle Scholar
  34. Kelso JA (1984) Phase transitions and critical behavior in human bimanual coordination. Am J Physiol 246:R1000-1004Google Scholar
  35. Kelso JA, Southard DL, Goodman D (1979) On the nature of human interlimb coordination. Science 203:1029–1031CrossRefPubMedGoogle Scholar
  36. Kennedy DM, Boyle JB, Wang C, Shea CH (2016) Bimanual force control: cooperation and interference? Psychol Res 80:34–54.  https://doi.org/10.1007/s00426-014-0637-6 CrossRefPubMedGoogle Scholar
  37. Kugler PN, Kelso JS, Turvey MT (1980) On the concept of coordinative structures as dissipative structures: I. Theoretical lines of convergence. Tutor Motor Behav 3:3–47CrossRefGoogle Scholar
  38. Kujirai T, Caramia MD, Rothwell JC et al (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519CrossRefPubMedPubMedCentralGoogle Scholar
  39. Latash ML, Scholz JF, Danion F, Schoner G (2001) Structure of motor variability in marginally redundant multifinger force production tasks. Exp Brain Res 141:153–165.  https://doi.org/10.1007/s002210100861 CrossRefPubMedGoogle Scholar
  40. Latash ML, Scholz JP, Schoner G (2007) Toward a new theory of motor synergies. Motor control 11:276–308CrossRefPubMedGoogle Scholar
  41. Maki Y, Wong KF, Sugiura M, Ozaki T, Sadato N (2008) Asymmetric control mechanisms of bimanual coordination: an application of directed connectivity analysis to kinematic and functional MRI data. Neuroimage 42:1295–1304.  https://doi.org/10.1016/j.neuroimage.2008.06.045 CrossRefPubMedGoogle Scholar
  42. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  43. Ortu E, Deriu F, Suppa A, Tolu E, Rothwell JC (2008) Effects of volitional contraction on intracortical inhibition and facilitation in the human motor cortex. J Physiol 586:5147–5159CrossRefPubMedPubMedCentralGoogle Scholar
  44. Peper CE, Beek PJ, van Wieringen PC (1995) Frequency-induced phase transitions in bimanual tapping. Biol Cybern 73:301–309CrossRefPubMedGoogle Scholar
  45. Perez MA, Butler JE, Taylor JL (2014) Modulation of transcallosal inhibition by bilateral activation of agonist and antagonist proximal arm muscles. J Neurophysiol 111:405–414CrossRefPubMedGoogle Scholar
  46. Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039.  https://doi.org/10.1016/j.clinph.2009.08.016 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Rossini PM, Burke D, Chen R et al (2015) Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 126:1071–1107CrossRefPubMedGoogle Scholar
  48. Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W (1999) Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol 52:97–103Google Scholar
  49. Sainburg RL (2002) Evidence for a dynamic-dominance hypothesis of handedness. Exp Brain Res 142:241–258.  https://doi.org/10.1007/s00221-001-0913-8 CrossRefPubMedGoogle Scholar
  50. Sainburg RL, Kalakanis D (2000) Differences in control of limb dynamics during dominant and nondominant arm reaching. J Neurophysiol 83:2661–2675CrossRefPubMedGoogle Scholar
  51. Sainburg R, Good D, Przybyla A (2013) Bilateral synergy: a framework for post-stroke rehabilitation. J Neurol Transl Neurosci 1:1025PubMedPubMedCentralGoogle Scholar
  52. Serrien DJ, Spapé MM (2009) The role of hand dominance and sensorimotor congruence in voluntary movement. Exp Brain Res 199:195–200CrossRefPubMedPubMedCentralGoogle Scholar
  53. Serrien DJ, Cassidy MJ, Brown P (2003) The importance of the dominant hemisphere in the organization of bimanual movements. Hum Brain Mapp 18:296–305.  https://doi.org/10.1002/hbm.10086 CrossRefPubMedGoogle Scholar
  54. Shabbott BA, Sainburg RL (2008) Differentiating between two models of motor lateralization. J Neurophysiol 100:565–575.  https://doi.org/10.1152/jn.90349.2008 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Shmuelof L, Krakauer JW, Mazzoni P (2012) How is a motor skill learned? Change and invariance at the levels of task success and trajectory control. J Neurophysiol 108:578–594.  https://doi.org/10.1152/jn.00856.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Silver NC, Dunlap WP (1987) Averaging correlation coefficients: should Fisher’s z transformation be used? J Appl Psychol 72:146CrossRefGoogle Scholar
  57. Stewart KC, Cauraugh JH, Summers JJ (2006) Bilateral movement training and stroke rehabilitation: a systematic review and meta-analysis. J Neurol Sci 244:89–95CrossRefPubMedGoogle Scholar
  58. Stinear JW, Byblow WD (2004) An interhemispheric asymmetry in motor cortex disinhibition during bimanual movement. Brain Res 1022:81–87.  https://doi.org/10.1016/j.brainres.2004.06.062 CrossRefPubMedGoogle Scholar
  59. Stucchi N, Viviani P (1993) Cerebral dominance and asynchrony between bimanual two-dimensional movements. J Exp Psychol Hum Percept Perform 19:1200–1220CrossRefPubMedGoogle Scholar
  60. Swinnen SP (2002) Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci 3:348–359.  https://doi.org/10.1038/nrn807 CrossRefPubMedGoogle Scholar
  61. Swinnen SP, Jardin K, Meulenbroek R (1996) Between-limb asynchronies during bimanual coordination: effects of manual dominance and attentional cueing. Neuropsychologia 34:1203–1213CrossRefPubMedGoogle Scholar
  62. Swinnen SP, Dounskaia N, Levin O, Duysens J (2001) Constraints during bimanual coordination: the role of direction in relation to amplitude and force requirements. Behav Brain Res 123:201–218CrossRefPubMedGoogle Scholar
  63. Tazoe T, Sasada S, Sakamoto M, Komiyama T (2013) Modulation of interhemispheric interactions across symmetric and asymmetric bimanual force regulations. Eur J Neurosci 37:96–104CrossRefPubMedGoogle Scholar
  64. Toyokura M, Muro I, Komiya T, Obara M (1999) Relation of bimanual coordination to activation in the sensorimotor cortex and supplementary motor area: analysis using functional magnetic resonance imaging. Brain Res Bull 48:211–217CrossRefPubMedGoogle Scholar
  65. Tseng YW, Scholz JP (2005) Unilateral vs. bilateral coordination of circle-drawing tasks. Acta Psychol (Amst) 120:172–198.  https://doi.org/10.1016/j.actpsy.2005.04.001 CrossRefGoogle Scholar
  66. Tseng YW, Scholz JP, Galloway JC (2009) The organization of intralimb and interlimb synergies in response to different joint dynamics. Exp Brain Res 193:239–254.  https://doi.org/10.1007/s00221-008-1616-1 CrossRefPubMedGoogle Scholar
  67. Turvey MT (1990) Coordination. Am Psychol 45:938CrossRefPubMedGoogle Scholar
  68. Van Delden A, Peper CLE, Kwakkel G, Beek PJ (2012) A systematic review of bilateral upper limb training devices for poststroke rehabilitation. Stroke Res Treat 2012:972069.  https://doi.org/10.1155/2012/972069 PubMedGoogle Scholar
  69. Vines BW, Nair D, Schlaug G (2008) Modulating activity in the motor cortex affects performance for the two hands differently depending upon which hemisphere is stimulated. Eur J Neurosci 28:1667–1673.  https://doi.org/10.1111/j.1460-9568.2008.06459.x CrossRefPubMedGoogle Scholar
  70. Viviani P, Perani D, Grassi F, Bettinardi V, Fazio F (1998) Hemispheric asymmetries and bimanual asynchrony in left- and right-handers. Exp Brain Res 120:531–536CrossRefPubMedGoogle Scholar
  71. Walsh RR, Small SL, Chen EE, Solodkin A (2008) Network activation during bimanual movements in humans. Neuroimage 43:540–553.  https://doi.org/10.1016/j.neuroimage CrossRefPubMedPubMedCentralGoogle Scholar
  72. Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol 108:1–16Google Scholar
  73. Whitall J, Waller SM, Silver KH, Macko RF (2000) Repetitive bilateral arm training with rhythmic auditory cueing improves motor function in chronic hemiparetic stroke. Stroke 31:2390–2395CrossRefPubMedGoogle Scholar
  74. Yahagi S, Kasai T (1999) Motor evoked potentials induced by motor imagery reveal a functional asymmetry of cortical motor control in left-and right-handed human subjects. Neurosci Lett 276:185–188CrossRefPubMedGoogle Scholar
  75. Ziemann U, Hallett M (2001) Hemispheric asymmetry of ipsilateral motor cortex activation during unimanual motor tasks: further evidence for motor dominance. Clin Neurophysiol 112:107–113CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Physical Therapy and Rehabilitation Science, School of MedicineUniversity of Maryland BaltimoreBaltimoreUSA
  2. 2.Faculty of Health SciencesUniversity of SouthamptonSouthamptonUK
  3. 3.Department of Neurology, School of MedicineUniversity of Maryland BaltimoreBaltimoreUSA

Personalised recommendations