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
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
Armatas CA, Summers JJ, Bradshaw JL (1994) Mirror movements in normal adult subjects. J Clin Exp Neuropsychol 16(3):405–413
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
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
Beek PJ, Peper CE, Daffertshofer A (2002) Modeling rhythmic interlimb coordination: beyond the Haken-Kelso-Bunz model. Brain Cogn 48(1):149–165
Boroojerdi B, Diefenbach K, Ferbert A (1996) Transcallosal inhibition in cortical and subcortical cerebral vascular lesions. J Neurol Sci 144(1–2):160–170
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
Brinkman J, Kuypers HG (1972) Splitbrain monkeys: cerebral control of ipsilateral and contralateral arm, hand, and finger movements. Science 176(34):536–539
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
Carpenter AF, Georgopoulos AP, Pellizzer G (1999) Motor cortical encoding of serial order in a context-recall task. Science 283(5408):1752–1757
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
Cheyne D, Weinberg H (1989) Neuromagnetic fields accompanying unilateral finger movements: pre-movement and movement-evoked fields. Exp Brain Res 78(3):604–612
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
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
Daffertshofer A, Peper CE, Beek PJ (2000) Spectral analyses of event-related encephalographic signals. Phys Lett A 266(4–6):290–302
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
Daffertshofer A, van den Berg C, Beek PJ (1999) A dynamical model for mirror movements. Physica D 132(1–2):243–266
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
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
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
Donchin O, Gribova A, Steinberg O, Bergman H, Vaadia E (1998) Primary motor cortex is involved in bimanual coordination. Nature 395(6699):274–278
Ermentrout GB, Cowan JD (1979) Temporal oscillations in neuronal nets. J Math Biol 7(3):265–280
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
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
Freeman WJ (1975) Mass action in the nervous system. Academic, New York
Freund HJ (1996) Functional organization of the human supplementary motor area and dorsolateral premotor cortex. Adv Neurol 70:263–269
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
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
Gazzaniga MS (1966) Visuomotor integration in split-brain monkeys with other cerebral lesions. Exp Neurol 16(3):289–298
Gerloff C, Andres FG (2002) Bimanual coordination and interhemispheric interaction. Acta Psychol 110(2–3):161–186
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
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
Geschwind N, Kaplan E (1998) A human cerebral deconnection syndrome: a preliminary report. 1962. Neurology 50(5):1201–1212
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
Haken H (1996) Principles of brain functioning. Springer, Berlin Heidelberg New York
Haken H, Kelso JA, Bunz H (1985) A theoretical model of phase transitions in human hand movements. Biol Cybern 51(5):347–356
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
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
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
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
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
Jirsa VK, Haken H (1996) Field theory of electromagnetic brain activity. Phys Rev Lett 77(5):960–963
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
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
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
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
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
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
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
Liley DTJ, Cadusch PJ, Wright JJ (1999) A continuum theory of electrocortical activity. Neurocomp 26–27(1–3):795–800
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
Mark RF, Sperry RW (1968) Bimanual coordination in monkeys. Exp Neurol 21(1):92–104
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
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
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
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
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
Nunez PL, Ed (1995) Neocortical dynamics and human EEG rhythms. Oxford University Press, New York
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
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
Peper CE, Beek PJ, Van Wieringen PCW (1995a) Frequency-induced phase transitions in bimanual tapping. Biol Cybern 73(4):301–309
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
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
Press WH, Teukolsky SA, Vetterling WT, Flannery BP (2002) Numerical recipes in C: the art of scientific computing. Cambridge University Press, Cambridge, UK
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
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
Stinear CM, Byblow WD (2003) Role of intracortical inhibition in selective hand muscle activation. J Neurophysiol 89(4):2014–2020
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
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
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
Summers JJ, Rosenbaum DA, Burns BD, Ford SK (1993) Production of polyrhythms. J Exp Psychol Hum Percept Perform 19(2):416–428
Swinnen SP (2002) Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci 3(5):348–359
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
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
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
Wilson HR, Cowan JD (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12(1):1–24
Winfree AT (1967) Biological rhythms and the behavior of populations of coupled oscillators. J Theor Biol 16(1):15–42
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
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
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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