Experimental Brain Research

, Volume 203, Issue 2, pp 407–418 | Cite as

Resource-demanding versus cost-effective bimanual interaction in the brain

Research Article


When two hands require different information in bimanual asymmetric movements, interference can occur via callosal connections and ipsilateral corticospinal pathways. This interference could potentially work as a cost-effective measure in symmetric movements, allowing the same information to be commonly available to both hands at once. Using functional magnetic resonance imaging, we investigated supra-additive and sub-additive neural interactions in bimanual movements during the initiation and continuation phases of movement. We compared activity during bimanual asymmetric and symmetric movements with the sum of activity during unimanual right and left finger-tapping. Supra-additive continuation-related activation was found in the right dorsal premotor cortex and left cerebellum (lobule V) during asymmetric movements. In addition, for unimanual movements, the right dorsal premotor cortex and left cerebellum (lobule V) showed significant activation only for left-hand (non-dominant) movements, but not for right-hand movements. These results suggest that resource-demanding interactions in bimanual asymmetric movements are involved in a non-dominant hand motor network that functions to keep non-dominant hand movements stable. We found sub-additive continuation-related activation in the supplementary motor area (SMA), bilateral cerebellum (lobule VI) in symmetric movements, and the SMA in asymmetric movements. This suggests that no extra demands were placed on these areas in bimanual movements despite the conventional notion that they play crucial roles in bimanual coordination. Sub-additive initiation-related activation in the left anterior putamen suggests that symmetric movements place lower demands on motor programming. These findings indicate that, depending on coordination patterns, the neural substrates of bimanual movements either exhibit greater effort to keep non-dominant hand movements stable, or save neural cost by sharing information commonly to both hands.


Bimanual coordination fMRI Neural crosstalk 



This study was supported in part by a Grant-in-Aid for Young Scientists (B) # 20700479 (YA) and (S) #17100003 (NS) from the Japan Society for the Promotion of Science, and Special Coordination Funds for Promoting Science and Technology from the Ministry of Education, Culture, Sports, Science and Technology, the Japanese Government. We are very grateful to Mr. Toshinori Yoshioka (CNS Technical Support Group in ATR) for his technical support.

Supplementary material

221_2010_2244_MOESM1_ESM.pdf (105 kb)
Supplementary material 1 (PDF 105 kb)


  1. Aizawa H, Mushiake H, Inase M, Tanji J (1990) An output zone of the monkey primary motor cortex specialized for bilateral hand movement. Exp Brain Res 82:219–221CrossRefPubMedGoogle Scholar
  2. Aramaki Y, Honda M, Okada T, Sadato N (2006) Neural correlates of the spontaneous phase transition during bimanual coordination. Cereb Cortex 16:1338–1348CrossRefPubMedGoogle Scholar
  3. Bengtsson SL, Ehrsson HH, Forssberg H, Ullen F (2005) Effector-independent voluntary timing: behavioural and neuroimaging evidence. Eur J Neurosci 22:3255–3265CrossRefPubMedGoogle Scholar
  4. Brinkman C (1984) Supplementary motor area of the monkeys cerebral-cortex—short-term and long-term deficits after unilateral ablation and the effects of subsequent callosal section. J Neurosci 4:918–929PubMedGoogle 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. Chan JL, Ross ED (1988) Left-handed mirror writing following right anterior cerebral artery infarction: evidence for nonmirror transformation of motor programs by right supplementary motor area. Neurology 38:59–63PubMedGoogle Scholar
  7. Diedrichsen J, Grafton S, Albert N, Hazeltine E, Ivry RB (2006) Goal-selection and movement-related conflict during bimanual reaching movements. Cereb Cortex 16:1729–1738CrossRefPubMedGoogle Scholar
  8. Diedrichsen J, Criscimagna-Hemminger SE, Shadmehr R (2007) Dissociating timing and coordination as functions of the cerebellum. J Neurosci 27:6291–6301CrossRefPubMedGoogle Scholar
  9. Friston KJ, Ashburner J, Poline JB, Frith CD, Heather JD, Frackowiak RSJ (1995a) Spatial registration and normalization of images. Hum Brain Mapp 2:165–189CrossRefGoogle Scholar
  10. Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ (1995b) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210CrossRefGoogle Scholar
  11. Friston KJ, Holmes A, Poline JB, Price CJ, Frith CD (1996) Detecting activations in PET and fMRI: levels of inference and power. Neuroimage 4:223–235CrossRefPubMedGoogle Scholar
  12. Friston KJ, Holmes AP, Worsley KJ (1999) How many subjects constitute a study? Neuroimage 10:1–5CrossRefPubMedGoogle Scholar
  13. Grahn JA, Brett M (2007) Rhythm and beat perception in motor areas of the brain. J Cogn Neurosci 19:893–906CrossRefPubMedGoogle Scholar
  14. Grodd W, Hulsmann E, Lotze M, Wildgruber D, Erb M (2001) Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp 13:55–73CrossRefPubMedGoogle Scholar
  15. Halsband U, Ito N, Tanji J, Freund HJ (1993) The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. Brain 116(Pt 1):243–266CrossRefPubMedGoogle Scholar
  16. Heuer H, Kleinsorge T, Spijkers W, Steglich W (2001) Static and phasic cross-talk effects in discrete bimanual reversal movements. J Mot Behav 33:67–85CrossRefPubMedGoogle Scholar
  17. Immisch I, Waldvogel D, van Gelderen P, Hallett M (2001) The role of the medial wall and its anatomical variations for bimanual antiphase and in-phase movements. Neuroimage 14:674–684CrossRefPubMedGoogle Scholar
  18. Ivry RB, Spencer RM (2004) The neural representation of time. Curr Opin Neurobiol 14:225–232CrossRefPubMedGoogle Scholar
  19. Ivry RB, Keele SW, Diener HC (1988) Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res 73:167–180CrossRefPubMedGoogle Scholar
  20. Kelso JA (1984) Phase transitions and critical behavior in human bimanual coordination. Am J Physiol 246:R1000–R1004PubMedGoogle Scholar
  21. Kimura M (1990) Behaviorally contingent property of movement-related activity of the primate putamen. J Neurophysiol 63:1277–1296PubMedGoogle Scholar
  22. Kraft E, Chen AW, Flaherty AW, Blood AJ, Kwong KK, Jenkins BG (2007) The role of the basal ganglia in bimanual coordination. Brain Res 1151:62–73CrossRefPubMedGoogle Scholar
  23. Lehericy S, Ducros M, Krainik A, Francois C, Van de Moortele PF, Ugurbil K, Kim DS (2004a) 3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. Cereb Cortex 14:1302–1309CrossRefPubMedGoogle Scholar
  24. Lehericy S, Ducros M, Van de Moortele PF, Francois C, Thivard L, Poupon C, Swindale N, Ugurbil K, Kim DS (2004b) Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans. Ann Neurol 55:522–529CrossRefPubMedGoogle Scholar
  25. Lewis PA, Wing AM, Pope PA, Praamstra P, Miall RC (2004) Brain activity correlates differentially with increasing temporal complexity of rhythms during initialisation, synchronisation, and continuation phases of paced finger tapping. Neuropsychologia 42:1301–1312CrossRefPubMedGoogle Scholar
  26. Mechsner F, Kerzel D, Knoblich G, Prinz W (2001) Perceptual basis of bimanual coordination. Nature 414:69–73CrossRefPubMedGoogle Scholar
  27. Meyer-Lindenberg A, Ziemann U, Hajak G, Cohen L, Berman KF (2002) Transitions between dynamical states of differing stability in the human brain. Proc Natl Acad Sci USA 99:10948–10953CrossRefPubMedGoogle Scholar
  28. Müller K, Kleiser R, Mechsner F, Seitz RJ (2009) Perceptual influence on bimanual coordination: an fMRI study. Eur J Neurosci 30:116–124CrossRefPubMedGoogle Scholar
  29. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  30. Rao SM, Mayer AR, Harrington DL (2001) The evolution of brain activation during temporal processing. Nat Neurosci 4:317–323CrossRefPubMedGoogle Scholar
  31. Romo R, Scarnati E, Schultz W (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. II. Movement-related activity in the anterior striatum. Exp Brain Res 91:385–395CrossRefPubMedGoogle Scholar
  32. Sadato N, Yonekura Y, Waki A, Yamada H, Ishii Y (1997) Role of the supplementary motor area and the right premotor cortex in the coordination of bimanual finger movements. J Neurosci 17:9667–9674PubMedGoogle Scholar
  33. Sakai ST, Inase M, Tanji J (1999) Pallidal and cerebellar inputs to thalamocortical neurons projecting to the supplementary motor area in Macaca fuscata: a triple-labeling light microscopic study. Anat Embryol (Berl) 199:9–19CrossRefGoogle Scholar
  34. Sakai ST, Inase M, Tanji J (2002) The relationship between MI and SMA afferents and cerebellar and pallidal efferents in the macaque monkey. Somatosens Mot Res 19:139–148CrossRefPubMedGoogle Scholar
  35. Schaal S, Sternad D, Osu R, Kawato M (2004) Rhythmic arm movement is not discrete. Nat Neurosci 7:1136–1143CrossRefPubMedGoogle Scholar
  36. Schell GR, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. J Neurosci 4:539–560PubMedGoogle Scholar
  37. Schmahmann JD, Doyon J, Toga A, Petrides M, Evans A (2000) MRI atlas of the human cerebellum. Academic Press, San DiegoGoogle Scholar
  38. Semjen A, Summers JJ, Cattaert D (1995) Hand coordination in bimanual circle drawing. J Exp Psychol Human Percept Perform 21:1139–1157CrossRefGoogle Scholar
  39. Stephan KM, Binkofski F, Halsband U, Dohle C, Wunderlich G, Schnitzler A, Tass P, Posse S, Herzog H, Sturm V, Zilles K, Seitz RJ, Freund HJ (1999) The role of ventral medial wall motor areas in bimanual co-ordination. A combined lesion and activation study. Brain 122(Pt 2):351–368CrossRefPubMedGoogle Scholar
  40. Swinnen SP, Wenderoth N (2004) Two hands, one brain: cognitive neuroscience of bimanual skill. Trends Cogn Sci 8:18–25CrossRefPubMedGoogle Scholar
  41. Timmann D, Watts S, Hore J (1999) Failure of cerebellar patients to time finger opening precisely causes ball high-low inaccuracy in overarm throws. 82:103–114Google Scholar
  42. Timmann D, Citron R, Watts S, Hore J (2001) Increased variability in finger position occurs throughout overarm throws made by cerebellar and unskilled subjects. J Neurophysiol 86:2690–2702PubMedGoogle Scholar
  43. Wiesendanger R, Wiesendanger M (1985) The thalamic connections with medial area 6 (supplementary motor cortex) in the monkey (Macaca fascicularis). Exp Brain Res 59:91–104PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Center for Fostering Young and Innovative ResearchersNagoya Institute of TechnologyNagoyaJapan
  2. 2.Computational Neuroscience Sub-Group, Biological ITC GroupNational Institute of Information and Communications TechnologyKeihanna Science City, KyotoJapan
  3. 3.Department of Cerebral ResearchNational Institute for Physiological SciencesOkazakiJapan
  4. 4.ATR Computational Neuroscience LaboratoriesKeihanna Science City, KyotoJapan

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