Parieto-premotor areas mediate directional interference during bimanual movements.

In bimanual movements, interference emerges when limbs are moved simultaneously along incompatible directions. The neural substrate and mechanisms underlying this phenomenon are largely unknown. We used functional magnetic resonance imaging to compare brain activation during directional incompatible versus compatible bimanual movements. Our main results were that directional interference emerges primarily within superior parietal, intraparietal and dorsal premotor areas of the right hemisphere. The same areas were also activated when the unimanual subtasks were executed in isolation. In light of previous findings in monkeys and humans, we conclude that directional interference activates a parieto-premotor circuit that is involved in the control of goal-directed movements under somatosensory guidance. Moreover, our data suggest that the parietal cortex might represent an important locus for integrating spatial aspects of the limbs' movements into a common action. It is hypothesized to be the candidate structure from where interference arises when directionally incompatible movements are performed. We discuss the possibility that interference emerges when computational resources in these parietal areas are insufficient to code two incompatible movement directions independently from each other.

[1]  S. Dehaene,et al.  Topographical Layout of Hand, Eye, Calculation, and Language-Related Areas in the Human Parietal Lobe , 2002, Neuron.

[2]  S. Swinnen,et al.  Directional interference during bimanual coordination: is interlimb coupling mediated by afferent or efferent processes , 2003, Behavioural Brain Research.

[3]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[4]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[5]  John J. Foxe,et al.  The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. , 2002, Brain research. Cognitive brain research.

[6]  A. Paans,et al.  Brain Activation Related to the Representations of External Space and Body Scheme in Visuomotor Control , 2001, NeuroImage.

[7]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Ravi S. Menon,et al.  A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing. , 2000, Journal of neurophysiology.

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

[10]  J. Kalaska,et al.  Deciding not to GO: neuronal correlates of response selection in a GO/NOGO task in primate premotor and parietal cortex. , 1995, Cerebral cortex.

[11]  A. Iriki,et al.  Book Review: Bilateral Activity and Callosal Connections in the Somatosensory Cortex , 2001, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[12]  H Heuer,et al.  Structural constraints on bimanual movements , 1993, Psychological research.

[13]  C. Colby,et al.  Heterogeneity of extrastriate visual areas and multiple parietal areas in the Macaque monkey , 1991, Neuropsychologia.

[14]  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.

[15]  A. P. Georgopoulos,et al.  Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex , 1983, Experimental Brain Research.

[16]  Stephan P. Swinnen,et al.  Directional tuning effects during cyclical two-joint arm movements in the horizontal plane , 2001, Experimental Brain Research.

[17]  K L Leenders,et al.  Right parieto-premotor activation related to limb-independent antiphase movement. , 2002, Cerebral cortex.

[18]  E A Franz,et al.  Spatial Coupling in the Coordination of Complex Actions , 1997, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[19]  F. Lacquaniti,et al.  Representing spatial information for limb movement: role of area 5 in the monkey. , 1995, Cerebral cortex.

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

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

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

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

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

[25]  K. Zilles,et al.  Human Somatosensory Area 2: Observer-Independent Cytoarchitectonic Mapping, Interindividual Variability, and Population Map , 2001, NeuroImage.

[26]  P. Roland,et al.  Interference between two concurrent tasks is associated with activation of overlapping fields in the cortex. , 1997, Brain research. Cognitive brain research.

[27]  R. Ivry,et al.  Callosotomy patients exhibit temporal uncoupling during continuous bimanual movements , 2002, Nature Neuroscience.

[28]  S. Scott,et al.  Cortical control of reaching movements , 1997, Current Opinion in Neurobiology.

[29]  G. Vallar,et al.  Spatial frames of reference and somatosensory processing: a neuropsychological perspective. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[30]  J. A. S. Kelso,et al.  Practice-dependent modulation of neural activity during human sensorimotor coordination: a functional Magnetic Resonance Imaging study , 2002, Neuroscience Letters.

[31]  P. Sinha,et al.  Functional neuroanatomy of biological motion perception in humans , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Gazzaniga,et al.  Dissociation of Spatial and Temporal Coupling in the Bimanual Movements of Callosotomy Patients , 1996 .

[33]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

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

[35]  E. Franz,et al.  The Effect of Callosotomy on Novel Versus Familiar Bimanual Actions: A Neural Dissociation Between Controlled and Automatic Processes? , 2000, Psychological science.

[36]  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.

[37]  J. Driver,et al.  Perceptual awareness and its loss in unilateral neglect and extinction , 2001, Cognition.

[38]  K. Zilles,et al.  Structural divisions and functional fields in the human cerebral cortex 1 Published on the World Wide Web on 20 February 1998. 1 , 1998, Brain Research Reviews.

[39]  Yoshiaki Iwamura,et al.  Representation of reaching and grasping in the monkey postcentral gyrus , 1996, Neuroscience Letters.

[40]  Natalia Dounskaia,et al.  Constraints during bimanual coordination: the role of direction in relation to amplitude and force requirements , 2001, Behavioural Brain Research.

[41]  Driss Boussaoud,et al.  Frontal lobe mechanisms subserving vision-for-action versus vision-for-perception , 1995, Behavioural Brain Research.

[42]  J. Jonides,et al.  Neuroimaging analyses of human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[43]  R. Andersen,et al.  Intention-related activity in the posterior parietal cortex: a review , 2000, Vision Research.

[44]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[45]  M. Tanaka,et al.  Processing of tactile and kinesthetic signals from bilateral sides of the body in the postcentral gyrus of awake monkeys , 2002, Behavioural Brain Research.

[46]  H N Zelaznik,et al.  Spatial topological constraints in a bimanual task. , 1991, Acta psychologica.

[47]  Nicole Wenderoth,et al.  Bimanual Training Reduces Spatial Interference , 2003, Journal of motor behavior.

[48]  F. Lacquaniti,et al.  Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. , 2001, Cerebral cortex.

[49]  J. Binder,et al.  Distributed Neural Systems Underlying the Timing of Movements , 1997, The Journal of Neuroscience.

[50]  L. Cohen,et al.  Transitions between dynamical states of differing stability in the human brain , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[52]  Lacquaniti,et al.  Visuo‐motor transformations for arm reaching , 1998, The European journal of neuroscience.

[53]  H. Pashler.  Dual-task interference in simple tasks: data and theory. , 1994, Psychological bulletin.

[54]  A. Berthoz,et al.  The neural basis of egocentric and allocentric coding of space in humans: a functional magnetic resonance study , 2000, Experimental Brain Research.

[55]  R. E. Passingham,et al.  Parietal cortex and movement I. Movement selection and reaching , 1997, Experimental Brain Research.

[56]  Francesco Lacquaniti,et al.  Multiple levels of representation of reaching in the parieto-frontal network. , 2003, Cerebral cortex.

[57]  R. Passingham.  Attention to action. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[58]  R. E. Passingham,et al.  Parietal cortex and movement II. Spatial representation , 1997, Experimental Brain Research.

[59]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

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

[61]  Paul Cisek,et al.  Neural activity in primary motor and dorsal premotor cortex in reaching tasks with the contralateral versus ipsilateral arm. , 2003, Journal of neurophysiology.

[62]  Christopher A. Buneo,et al.  Direct visuomotor transformations for reaching , 2002, Nature.

[63]  P. Goldman-Rakic,et al.  Functional neuroanatomy of executive processes involved in dual-task performance. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[65]  D. Pandya,et al.  Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey , 1982, The Journal of comparative neurology.

[66]  D. Yves von Cramon,et al.  The functional neuroanatomy of human working memory revisited Evidence from 3-T fMRI studies using classical domain-specific interference tasks , 2003, NeuroImage.

[67]  R Kawashima,et al.  Topographic representation in human intraparietal sulcus of reaching and saccade , 1996, Neuroreport.

[68]  F. Lacquaniti,et al.  Visuomotor Transformations for Reaching to Memorized Targets: A PET Study , 1997, NeuroImage.

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

[70]  W. Prinz,et al.  Perceptual basis of bimanual coordination , 2001, Nature.

[71]  Paul B. Johnson,et al.  Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. , 1996, Cerebral cortex.

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

[73]  T. Klingberg.  Concurrent performance of two working memory tasks: potential mechanisms of interference. , 1998, Cerebral cortex.

[74]  A. B. Mayer,et al.  Visuomotor transformations: early cortical mechanisms of reaching , 1998, Current Opinion in Neurobiology.

[75]  S. Swinnen,et al.  Bimanual coordination: constraints imposed by the relative timing of homologous muscle activation , 2004, Experimental Brain Research.

[76]  Michael S. Gazzaniga,et al.  Direction information coordinated via the posterior third of the corpus callosum during bimanual movements , 1999, Experimental Brain Research.

[77]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[78]  J D Gabrieli,et al.  A resource model of the neural basis of executive working memory. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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