Network activation during bimanual movements in humans

The coordination of movement between the upper limbs is a function highly distributed across the animal kingdom. How the central nervous system generates such bilateral, synchronous movements, and how this differs from the generation of unilateral movements, remain uncertain. Electrophysiologic and functional imaging studies support that the activity of many brain regions during bimanual and unimanual movement is quite similar. Thus, the same brain regions (and indeed the same neurons) respond similarly during unimanual and bimanual movements as measured by electrophysiological responses. How then are different motor behaviors generated? To address this question, we studied unimanual and bimanual movements using fMRI and constructed networks of activation using Structural Equation Modeling (SEM). Our results suggest that (1) the dominant hemisphere appears to initiate activity responsible for bimanual movement; (2) activation during bimanual movement does not reflect the sum of right and left unimanual activation; (3) production of unimanual movement involves a network that is distinct from, and not a mirror of, the network for contralateral unimanual movement; and (4) using SEM, it is possible to obtain robust group networks representative of a population and to identify individual networks which can be used to detect subtle differences both between subjects as well as within a single subject over time. In summary, these results highlight a differential role for the dominant and non-dominant hemispheres during bimanual movements, further elaborating the concept of handedness and dominance. This knowledge increases our understanding of cortical motor physiology in health and after neurological damage.

[1]  R. Caminiti,et al.  Callosal connections of dorso‐lateral premotor cortex , 2003, The European journal of neuroscience.

[2]  Simon B. Eickhoff,et al.  Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM , 2008, NeuroImage.

[3]  L. Krubitzer,et al.  Evidence for interhemispheric processing of inputs from the hands in human S2 and PV. , 2001, Journal of neurophysiology.

[4]  K. Zilles,et al.  The role of ventral medial wall motor areas in bimanual co-ordination. A combined lesion and activation study. , 1999, Brain : a journal of neurology.

[5]  Christophe Habas,et al.  The neural network involved in a bimanual tactile–tactile matching discrimination task: a functional imaging study at 3 T , 2007, Neuroradiology.

[6]  R Massarino,et al.  [The supplementary motor area is implicated in the coordination between posture and movement in man]. , 1989, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[7]  A Urbano,et al.  Responses of human primary sensorimotor and supplementary motor areas to internally triggered unilateral and simultaneous bilateral one-digit movements. A high-resolution EEG study. , 1997, The European journal of neuroscience.

[8]  K. Amunts,et al.  Consequences of large interindividual variability for human brain atlases: converging macroscopical imaging and microscopical neuroanatomy , 2005, Anatomy and Embryology.

[9]  Ana Solodkin,et al.  Complex Motor Function in Humans: Validating and Extending the Postulates of Alexandr R. Luria , 2006, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[10]  Robert Chen,et al.  Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. , 2003, Journal of neurophysiology.

[11]  F. Babiloni,et al.  Estimation of the cortical functional connectivity with the multimodal integration of high-resolution EEG and fMRI data by directed transfer function , 2005, NeuroImage.

[12]  L. White,et al.  Structure of the human sensorimotor system. I: Morphology and cytoarchitecture of the central sulcus. , 1997, Cerebral cortex.

[13]  R Caminiti,et al.  The callosal system of the superior parietal lobule in the monkey , 1985, The Journal of comparative neurology.

[14]  A. Salerno,et al.  Interhemispheric facilitation and inhibition studied in man with double magnetic stimulation. , 1996, Electroencephalography and clinical neurophysiology.

[15]  J. Liepert,et al.  Inhibition of ipsilateral motor cortex during phasic generation of low force , 2001, Clinical Neurophysiology.

[16]  M Wiesendanger,et al.  Effects of lesions in the mesial frontal cortex on bimanual co-ordination in monkeys , 1998, Neuroscience.

[17]  M. Filippi,et al.  Influence of body segment position during in‐phase and antiphase hand and foot movements: A kinematic and functional MRI study , 2007, Human brain mapping.

[18]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

[19]  B. M. de Jong,et al.  Brain Activation Related to the Change between Bimanual Motor Programs , 1999, NeuroImage.

[20]  S. Swinnen,et al.  Control of asymmetrical bimanual movements , 2004, Experimental Brain Research.

[21]  Philippe A. Chouinard,et al.  Changes in effective connectivity of the primary motor cortex in stroke patients after rehabilitative therapy , 2006, Experimental Neurology.

[22]  Sukhvinder S. Obhi,et al.  rTMS to the supplementary motor area disrupts bimanual coordination. , 2002, Motor control.

[23]  S P Swinnen,et al.  Spatial interactions during bimanual coordination patterns: the effect of directional compatibility. , 2001, Motor control.

[24]  James L. Arbuckle AMOS: Analysis of Moment Structures , 1989 .

[25]  Ingrid S. Johnsrude,et al.  Can Meaningful Effective Connectivities Be Obtained between Auditory Cortical Regions? , 2001, NeuroImage.

[26]  M. Wiesendanger,et al.  Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys , 2004, Experimental Brain Research.

[27]  A. Fuchs,et al.  Cortical and cerebellar activity of the human brain during imagined and executed unimanual and bimanual action sequences: a functional MRI study. , 2003, Brain research. Cognitive brain research.

[28]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[29]  Haim Sompolinsky,et al.  Cortical Representation of Bimanual Movements , 2003, The Journal of Neuroscience.

[30]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[31]  P. Brown,et al.  The importance of the dominant hemisphere in the organization of bimanual movements , 2003, Human brain mapping.

[32]  Kiyoshi Kurata,et al.  Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys , 1991, Neuroscience Research.

[33]  Elizabeth A Franz,et al.  Does Handedness Determine Which Hand Leads in a Bimanual Task? , 2002, Journal of motor behavior.

[34]  L. Deecke,et al.  Negative cortical DC shifts preceding and accompanying simultaneous and sequential finger movements , 2004, Experimental Brain Research.

[35]  S. Röricht,et al.  Topography of fibers in the human corpus callosum mediating interhemispheric inhibition between the motor cortices , 1998, Annals of neurology.

[36]  F. Gonzalez-Lima,et al.  Neural network interactions related to auditory learning analyzed with structural equation modeling , 1994 .

[37]  Karl J. Friston,et al.  On the Marriage of Cognition and Neuroscience , 2001, NeuroImage.

[38]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[39]  Paul Van Hecke,et al.  Brain Areas Involved in Interlimb Coordination: A Distributed Network , 2001, NeuroImage.

[40]  A. Fugl-Meyer,et al.  The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. , 1975, Scandinavian journal of rehabilitation medicine.

[41]  S. R. Jackson,et al.  The control of bimanual reach-to-grasp movements in hemiparkinsonian patients , 2000, Experimental Brain Research.

[42]  Daniel Cattaert,et al.  Simulating a neural cross-talk model for between-hand interference during bimanual circle drawing , 1999, Biological Cybernetics.

[43]  V. Mathiowetz,et al.  Adult norms for the Box and Block Test of manual dexterity. , 1985, The American journal of occupational therapy : official publication of the American Occupational Therapy Association.

[44]  M. Honda,et al.  Suppression of the non-dominant motor cortex during bimanual symmetric finger movement: A functional magnetic resonance imaging study , 2006, Neuroscience.

[45]  P. Brown,et al.  The functional role of interhemispheric synchronization in the control of bimanual timing tasks , 2002, Experimental Brain Research.

[46]  G. Schlaug,et al.  Differential magnetic resonance signal change in human sensorimotor cortex to finger movements of different rate of the dominant and subdominant hand. , 1998, Brain research. Cognitive brain research.

[47]  Hans Forssberg,et al.  Brain Regions Controlling Nonsynergistic versus Synergistic Movement of the Digits: a Functional Magnetic Resonance Imaging Study , 2002, The Journal of Neuroscience.

[48]  J. Kaas,et al.  The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys , 1983, The Journal of comparative neurology.

[49]  N. Sadato,et al.  Role of the Supplementary Motor Area and the Right Premotor Cortex in the Coordination of Bimanual Finger Movements , 1997, The Journal of Neuroscience.

[50]  Iwona Stepniewska,et al.  Ipsilateral cortical connections of dorsal and ventral premotor areas in New World owl monkeys , 2006, The Journal of comparative neurology.

[51]  A. Schnitzler,et al.  The oscillatory network of simple repetitive bimanual movements. , 2005, Brain research. Cognitive brain research.

[52]  Stephan Riek,et al.  Neuromuscular-skeletal constraints upon the dynamics of unimanual and bimanual coordination , 2000, Experimental Brain Research.

[53]  J. Jankovic,et al.  and J Jankovic The alien hand and related signs , 2022 .

[54]  Richard B. Ivry,et al.  Intermanual interactions during initiation and production of rhythmic and discrete movements in individuals lacking a corpus callosum , 2007, Experimental Brain Research.

[55]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[56]  M S Gazzaniga,et al.  Anterior and posterior callosal contributions to simultaneous bimanual movements of the hands and fingers. , 2000, Brain : a journal of neurology.

[57]  D J Serrien,et al.  Damage to the parietal lobe impairs bimanual coordination , 2001, Neuroreport.

[58]  I. Jenkins,et al.  Cerebral control of unimanual and bimanual movements: an H215O PET study , 1998, Neuroreport.

[59]  S. Cardoso de Oliveira The neuronal basis of bimanual coordination: recent neurophysiological evidence and functional models. , 2002, Acta psychologica.

[60]  Natalia Dounskaia,et al.  Patterns of Bimanual Interference Reveal Movement Encoding within a Radial Egocentric Reference Frame , 2002, Journal of Cognitive Neuroscience.

[61]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[62]  Stefan Klöppel,et al.  The effect of handedness on cortical motor activation during simple bilateral movements , 2007, NeuroImage.

[63]  I. Kermadi,et al.  Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination. , 1998, Somatosensory & motor research.

[64]  S. Wolf,et al.  Assessing Wolf Motor Function Test as Outcome Measure for Research in Patients After Stroke , 2001, Stroke.

[65]  A. Schleicher,et al.  Architectonics of the human cerebral cortex and transmitter receptor fingerprints: reconciling functional neuroanatomy and neurochemistry , 2002, European Neuropsychopharmacology.

[66]  M. Toyokura,et al.  Relation of bimanual coordination to activation in the sensorimotor cortex and supplementary motor area: Analysis using functional magnetic resonance imaging , 1999, Brain Research Bulletin.

[67]  C D Marsden,et al.  The execution of bimanual movements in patients with Parkinson's, Huntington's and cerebellar disease. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[68]  B. Meyer,et al.  Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. , 1995, Brain : a journal of neurology.

[69]  H. Forssberg,et al.  Neural networks for the coordination of the hands in time. , 2003, Journal of neurophysiology.

[70]  S. Small,et al.  Fine modulation in network activation during motor execution and motor imagery. , 2004, Cerebral cortex.

[71]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.

[72]  E. Vaadia,et al.  Timing of bimanual movements in human and non-human primates in relation to neuronal activity in primary motor cortex and supplementary motor area , 2002, Experimental Brain Research.

[73]  B. Christensen,et al.  The mechanisms of interhemispheric inhibition in the human motor cortex , 2002, The Journal of physiology.

[74]  G. Fink,et al.  Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging , 2008, Annals of neurology.

[75]  B. Hyland,et al.  Neural activity of supplementary and primary motor areas in monkeys and its relation to bimanual and unimanual movement sequences , 1999, Neuroscience.

[76]  Karl J. Friston,et al.  Attention to Action: Specific Modulation of Corticocortical Interactions in Humans , 2001, NeuroImage.

[77]  M. Toyokura,et al.  Activation of Pre–Supplementary Motor Area (SMA) and SMA Proper During Unimanual and Bimanual Complex Sequences: An Analysis Using Functional Magnetic Resonance Imaging , 2002, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[78]  I. Kermadi,et al.  Do bimanual motor actions involve the dorsal premotor (PMd), cingulate (CMA) and posterior parietal (PPC) cortices? Comparison with primary and supplementary motor cortical areas. , 2000, Somatosensory & motor research.

[79]  Mark Hallett,et al.  The role of the medial wall and its anatomical variations for bimanual anti-phase and in-phase movements , 2001, NeuroImage.

[80]  Scott Peltier,et al.  Connectivity exploration with structural equation modeling: an fMRI study of bimanual motor coordination , 2005, NeuroImage.

[81]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[82]  R. B. Ivry,et al.  Reduced Timing Variability in Patients with Unilateral Cerebellar Lesions during Bimanual Movements , 1996, Journal of Cognitive Neuroscience.

[83]  I. Whishaw,et al.  How skilled are the skilled limb movements of the raccoon (Procyon lotor)? , 1999, Behavioural Brain Research.

[84]  S. Swinnen,et al.  Between-limb asynchronies during bimanual coordination: Effects of manual dominance and attentional cueing , 1996, Neuropsychologia.

[85]  J. Cohen,et al.  Spiral K‐space MR imaging of cortical activation , 1995, Journal of magnetic resonance imaging : JMRI.

[86]  H N Zelaznik,et al.  Spatial Conceptual Influences on the Coordination of Bimanual Actions: When a Dual Task Becomes a Single Task , 2001, Journal of motor behavior.

[87]  Angela R. Laird,et al.  Modeling motor connectivity using TMS/PET and structural equation modeling , 2008, NeuroImage.

[88]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[89]  Deborah A. Hall,et al.  Connectivity analysis with structural equation modelling: an example of the effects of voxel selection , 2003, NeuroImage.

[90]  A. E. Schulman,et al.  Functional coupling of human cortical sensorimotor areas during bimanual skill acquisition. , 1999, Brain : a journal of neurology.

[91]  J Tanji,et al.  Input organization of distal and proximal forelimb areas in the monkey primary motor cortex: A retrograde double labeling study , 1993, The Journal of comparative neurology.

[92]  S. Swinnen,et al.  Two hands, one brain: cognitive neuroscience of bimanual skill , 2004, Trends in Cognitive Sciences.

[93]  E. Vaadia,et al.  Single-unit activity related to bimanual arm movements in the primary and supplementary motor cortices. , 2002, Journal of neurophysiology.

[94]  Seong-Gi Kim,et al.  The size of corpus callosum correlates with functional activation of medial motor cortical areas in bimanual and unimanual movements. , 2003, Cerebral cortex.

[95]  S. Small,et al.  Lateralization of motor circuits and handedness during finger movements , 2001, European journal of neurology.

[96]  M Wiesendanger,et al.  Time structure of a goal-directed bimanual skill and its dependence on task constraints , 1999, Behavioural Brain Research.

[97]  Richard S. Frackowiak,et al.  Aging is associated with contrasting changes in local and distant cortical connectivity in the human motor system , 2006, NeuroImage.

[98]  J. Kaas,et al.  Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: A correlative anatomical and electrophysiological study , 1986, The Journal of comparative neurology.

[99]  L. Cohen,et al.  Kinematically specific interhemispheric inhibition operating in the process of generation of a voluntary movement. , 2005, Cerebral cortex.

[100]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[101]  R W Cox,et al.  Real‐time 3D image registration for functional MRI , 1999, Magnetic resonance in medicine.

[102]  A. Schleicher,et al.  Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data. , 1995, Journal of anatomy.

[103]  A. McIntosh,et al.  Mapping cognition to the brain through neural interactions. , 1999, Memory.

[104]  I. Kermadi,et al.  Effects of reversible inactivation of the supplementary motor area (SMA) on unimanual grasp and bimanual pull and grasp performance in monkeys. , 1997, Somatosensory & motor research.

[105]  S. Swinnen Intermanual coordination: From behavioural principles to neural-network interactions , 2002, Nature Reviews Neuroscience.

[106]  M. Wiesendanger,et al.  Role of the corpus callosum in bimanual coordination: a comparison of patients with congenital and acquired callosal damage , 2001, The European journal of neuroscience.

[107]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[108]  W. Byblow,et al.  Disinhibition in the human motor cortex is enhanced by synchronous upper limb movements , 2002, The Journal of physiology.

[109]  E. Vaadia,et al.  Neural interactions between motor cortical hemispheres during bimanual and unimanual arm movements , 2001, The European journal of neuroscience.

[110]  C. Gerloff,et al.  Bimanual coordination and interhemispheric interaction. , 2002, Acta psychologica.

[111]  R. Hashimoto,et al.  Diagonistic dyspraxia. Clinical characteristics, responsible lesion and possible underlying mechanism. , 1996, Brain : a journal of neurology.

[112]  Robert Chen,et al.  Interactions between inhibitory and excitatory circuits in the human motor cortex , 2003, Experimental Brain Research.

[113]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[114]  Gabriel Leonard,et al.  Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe , 1988, Neuropsychologia.

[115]  G. Jackson,et al.  Changes in effective connectivity models in the presence of task‐correlated motion: An fMRI study , 2004, Human brain mapping.

[116]  Timothy Edward John Behrens,et al.  Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills , 2007, NeuroImage.

[117]  F. Gonzalez-Lima,et al.  Structural equation modeling and its application to network analysis in functional brain imaging , 1994 .

[118]  G. Geffen,et al.  Interhemispheric control of manual motor activity , 1994, Behavioural Brain Research.

[119]  Riitta Hari,et al.  Transient Suppression of Ipsilateral Primary Somatosensory Cortex during Tactile Finger Stimulation , 2006, The Journal of Neuroscience.

[120]  O. Donchin,et al.  Neuronal populations in primary motor cortex encode bimanual arm movements , 2002, The European journal of neuroscience.

[121]  Valentino Bettinardi,et al.  Hemispheric asymmetries and bimanual asynchrony in left- and right-handers , 1998, Experimental Brain Research.

[122]  G. Rizzolatti,et al.  Motor and cognitive functions of the ventral premotor cortex , 2002, Current Opinion in Neurobiology.

[123]  H. Mushiake,et al.  An output zone of the monkey primary motor cortex specialized for bilateral hand movement , 2004, Experimental Brain Research.

[124]  John D Carew,et al.  Hemispheric asymmetry in supplementary motor area connectivity during unilateral finger movements , 2004, NeuroImage.

[125]  E. Vaadia,et al.  Primary motor cortex is involved in bimanual coordination , 1998, Nature.

[126]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[127]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[128]  K. Stephan,et al.  Cerebral midline structures in bimanual coordination , 1999, Experimental Brain Research.

[129]  P. Mazzone,et al.  Direct demonstration of interhemispheric inhibition of the human motor cortex produced by transcranial magnetic stimulation , 1999, Experimental Brain Research.

[130]  Rupert Lanzenberger,et al.  The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling , 2008, NeuroImage.

[131]  F Debaere,et al.  Cerebellar and premotor function in bimanual coordination: parametric neural responses to spatiotemporal complexity and cycling frequency , 2004, NeuroImage.

[132]  K. E. Stephan,et al.  Multimodal characterisation of cortical areas by multivariate analyses of receptor binding and connectivity data , 2001, Anatomy and Embryology.