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Stabilization of bimanual coordination due to active interhemispheric inhibition: a dynamical account

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Abstract

Based on recent brain-imaging data and congruent theoretical insights, a dynamical model is derived to account for the patterns of brain activity observed during stable performance of bimanual multifrequency patterns, as well as during behavioral instabilities in the form of phase transitions between such patterns. The model incorporates four dynamical processes, defined over both motor and premotor cortices, which are coupled through inhibitory and excitatory inter- and intrahemispheric connections. In particular, the model underscores the crucial role of interhemispheric inhibition in reducing the interference between disparate frequencies during stable performance, as well as the failure of this reduction during behavioral transitions. As an aside, the model also accounts for in- and antiphase preferences during isofrequency movements. The viability of the proposed model is illustrated by magnetoencephalographic signals that were recorded from an experienced subject performing a polyrhythmic tapping task that was designed to induce transitions between multifrequency patterns. Consistent with the model’s dynamics, contra- and ipsilateral cortical areas of activation were frequency- and phase-locked, while their activation strength changed markedly in the vicinity of transitions in coordination.

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References

  1. Andrew C, Pfurtscheller G (1999) Lack of bilateral coherence of post-movement central beta oscillations in the human electroencephalogram. Neurosci Lett 273(2):89–92

    Google Scholar 

  2. Armatas CA, Summers JJ, Bradshaw JL (1994) Mirror movements in normal adult subjects. J Clin Exp Neuropsychol 16(3):405–413

    Google Scholar 

  3. Babiloni C, Carducci F, Pizzella V, Indovina I, Romani GL, Rossini PM, Babiloni F (1999) Bilateral neuromagnetic activation of human primary sensorimotor cortex in preparation and execution of unilateral voluntary finger movements. Brain Res 827(1–2):234–236

    Google Scholar 

  4. Baraldi P, Porro CA, Serafini M, Pagnoni G, Murari C, Corazza R, Nichelli P (1999) Bilateral representation of sequential finger movements in human cortical areas. Neurosci Lett 269(2):95–98

    Google Scholar 

  5. Beek PJ, Peper CE, Daffertshofer A (2002) Modeling rhythmic interlimb coordination: beyond the Haken-Kelso-Bunz model. Brain Cogn 48(1):149–165

    Google Scholar 

  6. Boroojerdi B, Diefenbach K, Ferbert A (1996) Transcallosal inhibition in cortical and subcortical cerebral vascular lesions. J Neurol Sci 144(1–2):160–170

    Google Scholar 

  7. Brinkman C (1984) Supplementary motor area of the monkey’s cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section. J Neurosci 4(4):918–929

    Google Scholar 

  8. Brinkman J, Kuypers HG (1972) Splitbrain monkeys: cerebral control of ipsilateral and contralateral arm, hand, and finger movements. Science 176(34):536–539

    Google Scholar 

  9. Cardoso de Oliveira S, Gribova A, Donchin O, Bergman H, Vaadia E (2001) Neural interactions between motor cortical hemispheres during bimanual and unimanual arm movements. Eur J Neurosci 14(11):1881–1896

    Google Scholar 

  10. Carpenter AF, Georgopoulos AP, Pellizzer G (1999) Motor cortical encoding of serial order in a context-recall task. Science 283(5408):1752–1757

    Google Scholar 

  11. Chen R, Yung D, Li JY (2003) Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. J Neurophysiol 89(3):1256–1264

    Google Scholar 

  12. Cheyne D, Weinberg H (1989) Neuromagnetic fields accompanying unilateral finger movements: pre-movement and movement-evoked fields. Exp Brain Res 78(3):604–612

    Google Scholar 

  13. Chollet F, DiPiero V, Wise RJ, Brooks DJ, Dolan RJ, Frackowiak RS (1991) The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol 29(1):63–71

    Google Scholar 

  14. Cuadrado ML, Arias JA, Gonzalez-Gutierrez JL, Egido JA, Varela de Seijas E (1999) Cerebral activation during movement of both hands. A study with transcranial Doppler. Rev Neurol 29(9):793–796

    Google Scholar 

  15. Daffertshofer A, Peper CE, Beek PJ (2000) Spectral analyses of event-related encephalographic signals. Phys Lett A 266(4–6):290–302

    Google Scholar 

  16. Daffertshofer A, Peper CE, Frank TD, Beek PJ (2000) Spatio-temporal patterns of encephalographic signals during polyrhythmic tapping. Hum Mov Sci 19(4):475–498

    Google Scholar 

  17. Daffertshofer A, van den Berg C, Beek PJ (1999) A dynamical model for mirror movements. Physica D 132(1–2):243–266

    Google Scholar 

  18. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Roshan L, Chen R (2002) The mechanisms of interhemispheric inhibition in the human motor cortex. J Physiol 543(Pt 1):317–326

    Google Scholar 

  19. Deiber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RS (1991) Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 84(2):393–402

    Google Scholar 

  20. Donchin O, de Oliveira SC, Vaadia E (1999) Who tells one hand what the other is doing: the neurophysiology of bimanual movements. Neuron 23(1):15–18

    Google Scholar 

  21. Donchin O, Gribova A, Steinberg O, Bergman H, Vaadia E (1998) Primary motor cortex is involved in bimanual coordination. Nature 395(6699):274–278

    Google Scholar 

  22. Ermentrout GB, Cowan JD (1979) Temporal oscillations in neuronal nets. J Math Biol 7(3):265–280

    Google Scholar 

  23. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD (1992) Interhemispheric inhibition of the human motor cortex. J Physiol 453:525–546

    Google Scholar 

  24. Frank TD, Daffertshofer A, Peper CE, Beek PJ, Haken H (2000) Towards a comprehensive theory of brain activity: coupled oscillator systems under external forces. Physica D 144(1–2):62–86

    Google Scholar 

  25. Freeman WJ (1975) Mass action in the nervous system. Academic, New York

  26. Freund HJ (1996) Functional organization of the human supplementary motor area and dorsolateral premotor cortex. Adv Neurol 70:263–269

    Google Scholar 

  27. Fuchs A, Deecke L, Kelso JAS (2000) Phase transitions in the human brain revealed by large SQuID arrays: response to Daffertshofer, Peper, and Beek. Phys Lett A 266(4–6):303–308

    Google Scholar 

  28. Fuchs A, Jirsa VK, Kelso JA (2000) Theory of the relation between human brain activity (MEG) and hand movements. Neuroimage 11(5 Pt 1):359–369

    Google Scholar 

  29. Gazzaniga MS (1966) Visuomotor integration in split-brain monkeys with other cerebral lesions. Exp Neurol 16(3):289–298

    Google Scholar 

  30. Gerloff C, Andres FG (2002) Bimanual coordination and interhemispheric interaction. Acta Psychol 110(2–3):161–186

    Google Scholar 

  31. Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG (1998) The role of the human motor cortex in the control of complex and simple finger movement sequences. Brain 121(Pt 9):1695–1709

    Google Scholar 

  32. Gerloff C, Richard J, Hadley J, Schulman AE, Honda M, Hallett M (1998) Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. Brain 121(Pt 8):1513–1531

    Google Scholar 

  33. Geschwind N, Kaplan E (1998) A human cerebral deconnection syndrome: a preliminary report. 1962. Neurology 50(5):1201–1212

    Google Scholar 

  34. Gribova A, Donchin O, Bergman H, Vaadia E, Cardoso De Oliveira S (2002) Timing of bimanual movements in human and non-human primates in relation to neuronal activity in primary motor cortex and supplementary motor area. Exp Brain Res 146(3):322–335

  35. Haken H (1996) Principles of brain functioning. Springer, Berlin Heidelberg New York

  36. Haken H, Kelso JA, Bunz H (1985) A theoretical model of phase transitions in human hand movements. Biol Cybern 51(5):347–356

    Google Scholar 

  37. Haken H, Peper CE, Beek PJ, Daffertshofer A (1996) A model for phase transitions in human hand movements during multifrequency tapping. Physica D 90(1–2):179–196

    Google Scholar 

  38. 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):243–266

    Google Scholar 

  39. Hamzei F, Dettmers C, Rzanny R, Liepert J, Buchel C, Weiller C (2002) Reduction of excitability (“inhibition”) in the ipsilateral primary motor cortex is mirrored by fMRI signal decreases. Neuroimage 17(1):490–496

    Google Scholar 

  40. Hanajima R, Ugawa Y, Machii K, Mochizuki H, Terao Y, Enomoto H, Furubayashi T, Shiio Y, Uesugi H, Kanazawa I (2001) Interhemispheric facilitation of the hand motor area in humans. J Physiol 531(Pt 3):849–859

    Google Scholar 

  41. Ikeda A, Ohara S, Matsumoto R, Kunieda T, Nagamine T, Miyamoto S, Kohara N, Taki W, Hashimoto N, Shibasaki H (2000) Role of primary sensorimotor cortices in generating inhibitory motor response in humans. Brain 123(Pt 8):1710–1721

    Google Scholar 

  42. Jirsa VK, Haken H (1996) Field theory of electromagnetic brain activity. Phys Rev Lett 77(5):960–963

    Google Scholar 

  43. Jirsa VK, Jantzen KJ, Fuchs A, Kelso JA (2002) Spatiotemporal forward solution of the EEG and MEG using network modeling. IEEE Trans Med Imag 21(5):493–504

    Google Scholar 

  44. Kaiser J, Lutzenberger W, Preissl H, Mosshammer D, Birbaumer N (2000) Statistical probability mapping reveals high-frequency magnetoencephalographic activity in supplementary motor area during self-paced finger movements. Neurosci Lett 283(1):81–84

    Google Scholar 

  45. Kawashima R, Roland PE, O’Sullivan BT (1994) Activity in the human primary motor cortex related to ipsilateral hand movements. Brain Res 663(2):251–256

    Google Scholar 

  46. Kelso JAS, Bressler SL, Buchanan S, DeGuzman GC, Ding MAF, Fuchs A, Holroyd T (1992) A phase transition in human brain and behavior. Phys Lett A 169(3):134–144

    Google Scholar 

  47. Lang W, Obrig H, Lindinger G, Cheyne D, Deecke L (1990) Supplementary motor area activation while tapping bimanually different rhythms in musicians. Exp Brain Res 79(3):504–514

    Google Scholar 

  48. Leinsinger GL, Heiss DT, Jassoy AG, Pfluger T, Hahn K, Danek A (1997) Persistent mirror movements: functional MR imaging of the hand motor cortex. Radiology 203(2):545–552

    Google Scholar 

  49. Leocani L, Cohen LG, Wassermann EM, Ikoma K, Hallett M (2000) Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. Brain 123(Pt 6):1161–1173

    Google Scholar 

  50. Liley DTJ, Cadusch PJ, Wright JJ (1999) A continuum theory of electrocortical activity. Neurocomp 26–27(1–3):795–800

    Google Scholar 

  51. Manganotti P, Gerloff C, Toro C, Katsuta H, Sadato N, Zhuang P, Leocani L, Hallett M (1998) Task-related coherence and task-related spectral power changes during sequential finger movements. Electroencephalogr Clin Neurophysiol 109(1):50–62

    Google Scholar 

  52. Mark RF, Sperry RW (1968) Bimanual coordination in monkeys. Exp Neurol 21(1):92–104

    Google Scholar 

  53. Mayville JM, Fuchs A, Ding M, Cheyne D, Deecke L, Kelso JA (2001) Event-related changes in neuromagnetic activity associated with syncopation and synchronization timing tasks. Hum Brain Mapp 14(2):65–80

    Google Scholar 

  54. Mayville JM, Jantzen KJ, Fuchs A, Steinberg FL, Kelso JA (2002) Cortical and subcortical networks underlying syncopated and synchronized coordination revealed using fMRI. Hum Brain Mapp 17(4):214–229

    Google Scholar 

  55. Meyer BU, Roricht S, Gräfin von Einsiedel H, Kruggel F, Weindl A (1995) Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain 118(Pt 2):429–440

  56. 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(17):10948–10953

    Google Scholar 

  57. Mima T, Sadato N, Yazawa S, Hanakawa T, Fukuyama H, Yonekura Y, Shibasaki H (1999) Brain structures related to active and passive finger movements in man. Brain 122(Pt 10):1989–1997

    Google Scholar 

  58. Nunez PL, Ed (1995) Neocortical dynamics and human EEG rhythms. Oxford University Press, New York

  59. Ohara S, Ikeda A, Kunieda T, Yazawa S, Baba K, Nagamine T, Taki W, Hashimoto N, Mihara T, Shibasaki H (2000) Movement-related change of electrocorticographic activity in human supplementary motor area proper. Brain 123(Pt 6):1203–1215

    Google Scholar 

  60. Okuda B, Tanaka H, Tomino Y, Kawabata K, Tachibana H, Sugita M (1995) The role of the left somatosensory cortex in human hand movement. Exp Brain Res 106(3):493–498

    Google Scholar 

  61. Peper CE, Beek PJ, Van Wieringen PCW (1995a) Frequency-induced phase transitions in bimanual tapping. Biol Cybern 73(4):301–309

    Google Scholar 

  62. Peper CE, Beek PJ, Van Wieringen PCW (1995b) Multifrequency coordination in bimanual tapping: asymmetrical coupling and signs of supercriticality. J Exp Psychol Hum Percept Perform 21:1117–1138

    Google Scholar 

  63. Pfurtscheller G, Neuper C, Pichler-Zalaudek K, Edlinger G, Lopes da Silva FH (2000) Do brain oscillations of different frequencies indicate interaction between cortical areas in humans? Neurosci Lett 286(1):66–68

    Google Scholar 

  64. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (2002) Numerical recipes in C: the art of scientific computing. Cambridge University Press, Cambridge, UK

  65. Pulvermüller F, Lutzenberger W, Preißl H, Birbaumer N (1995) Motor programming in both hemispheres: an EEG study of the human brain. Neurosci Lett 190(1):5–8

    Google Scholar 

  66. Schneider C, Devanne H, Lavoie BA, Capaday C (2002) Neural mechanisms involved in the functional linking of motor cortical points. Exp Brain Res 146(1):86–94

    Google Scholar 

  67. Stinear CM, Byblow WD (2003) Role of intracortical inhibition in selective hand muscle activation. J Neurophysiol 89(4):2014–2020

    Google Scholar 

  68. Stinear CM, Byblow WD (2004) Modulation of corticospinal excitability and intracortical inhibition during motor imagery is task-dependent. Exp Brain Res 157(3):351–358

    Google Scholar 

  69. Stinear JW, Byblow WD (2002) Disinhibition in the human motor cortex is enhanced by synchronous upper limb movements. J Physiol 543(Pt 1):307–316

    Google Scholar 

  70. Stippich C, Kapfer D, Hempel E, Borgulya G, Bongers A, Heiland S, Sartor K (2000) Robust localization of the contralateral precentral gyrus in hemiparetic patients using the unimpaired ipsilateral hand: a clinical functional magnetic resonance imaging protocol. Neurosci Lett 285(2):155–159

    Google Scholar 

  71. Summers JJ, Rosenbaum DA, Burns BD, Ford SK (1993) Production of polyrhythms. J Exp Psychol Hum Percept Perform 19(2):416–428

    Google Scholar 

  72. Swinnen SP (2002) Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci 3(5):348–359

    Google Scholar 

  73. Tanji J, Okano K, Sato KC (1988) Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. J Neurophysiol 60(1):325–343

    Google Scholar 

  74. Waldvogel D, van Gelderen P, Muellbacher W, Ziemann U, Immisch I, Hallett M (2000) The relative metabolic demand of inhibition and excitation. Nature 406(6799):995–998

    Google Scholar 

  75. Wallenstein GV, Kelso JAS, Bressler SL (1995) Phase transitions in spatio-temporal patterns of brain activity and behavior. Physica D 84(3–4):626–634

    Google Scholar 

  76. Wilson HR, Cowan JD (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12(1):1–24

    Google Scholar 

  77. Winfree AT (1967) Biological rhythms and the behavior of populations of coupled oscillators. J Theor Biol 16(1):15–42

    Google Scholar 

  78. Wright JJ, Robinson PA, Rennie CJ, Gordon E, Bourke PD, Chapmar CLNH, Lees GJ, Alexander D (2001) Toward an integrated continuum model of cerebral dynamics: the cerebral rhythms, synchronous oscillation and cortical stability. Biosystems 63(1–3):71–88

    Google Scholar 

  79. Ziemann U, Ishii K, Borgheresi A, Yaseen Z, Battaglia F, Hallett M, Cincotta M, Wassermann EM (1999) Dissociation of the pathways mediating ipsilateral and contralateral motor-evoked potentials in human hand and arm muscles. J Physiol 518(Pt 3):895–906

    Google Scholar 

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The Netherlands Foundation for Behavioral Sciences (NWO) financially supported this research.

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Daffertshofer, A., Peper, C. & Beek, P. Stabilization of bimanual coordination due to active interhemispheric inhibition: a dynamical account. Biol Cybern 92, 101–109 (2005). https://doi.org/10.1007/s00422-004-0539-6

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  • DOI: https://doi.org/10.1007/s00422-004-0539-6

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