Motor learning-induced changes in functional brain connectivity as revealed by means of graph-theoretical network analysis

Complex bimanual motor learning causes specific changes in activation across brain regions. However, there is little information on how motor learning changes the functional connectivity between these regions, and whether this is influenced by different sensory feedback modalities. We applied graph-theoretical network analysis (GTNA) to examine functional networks based on motor-task-related fMRI activations. Two groups learned a complex 90° out-of-phase bimanual coordination pattern, receiving either visual or auditory feedback. 3T fMRI scanning occurred before (day 0) and after (day 5) training. In both groups, improved motor performance coincided with increased functional network connectivity (increased clustering coefficients, higher number of network connections and increased connection strength, and shorter communication distances). Day×feedback interactions were absent but, when examining network metrics across all examined brain regions, the visual group had a marginally better connectivity, higher connection strength, and more direct communication pathways. Removal of feedback had no acute effect on the functional connectivity of the trained networks. Hub analyses showed an importance of specific brain regions not apparent in the standard fMRI analyses. These findings indicate that GTNA can make unique contributions to the examination of functional brain connectivity in motor learning.

[1]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

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

[3]  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.

[4]  Nadim Joni Shah,et al.  Prefrontal involvement in imitation learning of hand actions: Effects of practice and expertise , 2007, NeuroImage.

[5]  Rachael D. Seidler,et al.  Failure to Engage Spatial Working Memory Contributes to Age-related Declines in Visuomotor Learning , 2011, Journal of Cognitive Neuroscience.

[6]  Byeong-Taek Lee,et al.  Brain activation during music listening in individuals with or without prior music training , 2005, Neuroscience Research.

[7]  Andreas Daffertshofer,et al.  Comparing Brain Networks of Different Size and Connectivity Density Using Graph Theory , 2010, PloS one.

[8]  Yong He,et al.  Disrupted small-world networks in schizophrenia. , 2008, Brain : a journal of neurology.

[9]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[10]  Ravi S. Menon,et al.  Learning-related fMRI activation associated with a rotational visuo-motor transformation. , 2005, Brain research. Cognitive brain research.

[11]  S. Swinnen,et al.  High-frequency transcranial magnetic stimulation of the supplementary motor area reduces bimanual coupling during anti-phase but not in-phase movements , 2003, Experimental Brain Research.

[12]  Agata Fronczak,et al.  Average path length in random networks. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[13]  Timothy Edward John Behrens,et al.  Training induces changes in white matter architecture , 2009, Nature Neuroscience.

[14]  Tracy L. Faber,et al.  Role of posterior parietal cortex in the recalibration of visually guided reaching , 1996, Nature.

[15]  Heidi Johansen-Berg,et al.  Model-free characterization of brain functional networks for motor sequence learning using fMRI , 2008, NeuroImage.

[16]  Tilo Kircher,et al.  Functional Connectivity Analyses in Imaging Genetics: Considerations on Methods and Data Interpretation , 2011, PloS one.

[17]  Karl J. Friston,et al.  Cerebral Cortex doi:10.1093/cercor/bhr050 Ongoing Brain Activity Fluctuations Directly Account for Intertrial and Indirectly for Intersubject Variability in Stroop Task Performance , 2011 .

[18]  Christian Büchel,et al.  Increased functional connectivity is crucial for learning novel muscle synergies , 2007, NeuroImage.

[19]  Timothy D. Verstynen,et al.  Using pulse oximetry to account for high and low frequency physiological artifacts in the BOLD signal , 2011, NeuroImage.

[20]  Habib Benali,et al.  Dynamics of motor-related functional integration during motor sequence learning , 2010, NeuroImage.

[21]  Habib Benali,et al.  Partial correlation for functional brain interactivity investigation in functional MRI , 2006, NeuroImage.

[22]  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.

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

[24]  M Hallett,et al.  Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. , 1997, Brain : a journal of neurology.

[25]  Olaf Sporns,et al.  Graph Theory Methods for the Analysis of Neural Connectivity Patterns , 2003 .

[26]  R. Kahn,et al.  Aberrant Frontal and Temporal Complex Network Structure in Schizophrenia: A Graph Theoretical Analysis , 2010, The Journal of Neuroscience.

[27]  Byron Bernal,et al.  DISSECTING NONVERBAL AUDITORY CORTEX ASYMMETRY: AN fMRI STUDY , 2004, The International journal of neuroscience.

[28]  Alain Ptito,et al.  Recovery From Mild Head Injury in Sports: Evidence From Serial Functional Magnetic Resonance Imaging Studies in Male Athletes , 2008, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[29]  Monica A. Perez,et al.  Motor skill training induces changes in the excitability of the leg cortical area in healthy humans , 2004, Experimental Brain Research.

[30]  Charles H. Shea,et al.  The learning of 90° continuous relative phase with and without Lissajous feedback: external and internally generated bimanual coordination. , 2011, Acta psychologica.

[31]  S. Kiebel,et al.  Visuomotor control within a distributed parieto-frontal network , 2002, Experimental Brain Research.

[32]  M. Hallett,et al.  The Role of the Medial Wall and Its Anatomical Variations for Bimanual Antiphase and In-Phase Movements , 2001, NeuroImage.

[33]  M. Himmelbach,et al.  fMRI study of bimanual coordination , 2000, Neuropsychologia.

[34]  J Tanji,et al.  Visually guided saccade versus eye-hand reach: contrasting neuronal activity in the cortical supplementary and frontal eye fields. , 1996, Journal of neurophysiology.

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

[36]  O. Sporns,et al.  Identification and Classification of Hubs in Brain Networks , 2007, PloS one.

[37]  H. Johansen-Berg,et al.  Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. , 2010, Cerebral cortex.

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

[39]  E. Bullmore,et al.  Neurophysiological architecture of functional magnetic resonance images of human brain. , 2005, Cerebral cortex.

[40]  Kevin Murphy,et al.  fMRI in the presence of task-correlated breathing variations , 2009, NeuroImage.

[41]  S. Swinnen,et al.  Changes in brain activation during the acquisition of a new bimanual coordination task , 2004, Neuropsychologia.

[42]  Shinobu Masaki,et al.  Learning-induced neural plasticity associated with improved identification performance after training of a difficult second-language phonetic contrast , 2003, NeuroImage.

[43]  Jason B. Boyle,et al.  Coding of on-line and pre-planned movement sequences. , 2010, Acta psychologica.

[44]  S. P. Swinnen,et al.  Relative Phase Alterations During Bimanual Skill Acquisition. , 1995, Journal of motor behavior.

[45]  K J Friston,et al.  The predictive value of changes in effective connectivity for human learning. , 1999, Science.

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

[47]  J. Hirsch,et al.  fMRI Evidence for Cortical Modification during Learning of Mandarin Lexical Tone , 2003, Journal of Cognitive Neuroscience.

[48]  Ivan Toni,et al.  Information processing in human parieto-frontal circuits during goal-directed bimanual movements , 2006, NeuroImage.

[49]  S. Swinnen,et al.  Age-related reduction in the differential pathways involved in internal and external movement generation , 2010, Neurobiology of Aging.

[50]  M. Fukunaga,et al.  Sources of functional magnetic resonance imaging signal fluctuations in the human brain at rest: a 7 T study. , 2009, Magnetic resonance imaging.

[51]  Nicole Wenderoth,et al.  Changes in Brain Activation during the Acquisition of a Multifrequency Bimanual Coordination Task: From the Cognitive Stage to Advanced Levels of Automaticity , 2005, The Journal of Neuroscience.

[52]  Bryon A. Mueller,et al.  Altered resting state complexity in schizophrenia , 2012, NeuroImage.

[53]  J. Doyon,et al.  Reorganization and plasticity in the adult brain during learning of motor skills , 2005, Current Opinion in Neurobiology.

[54]  S. Dager,et al.  Anxiety, respiration, and cerebral blood flow: implications for functional brain imaging. , 2007, Comprehensive psychiatry.

[55]  S P Swinnen,et al.  Coordination deficits on the ipsilesional side after unilateral stroke: the effect of practice on nonisodirectional ipsilateral coordination. , 2002, Acta psychologica.

[56]  M. Raichle,et al.  The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. , 1985, Journal of neurophysiology.

[57]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[58]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[59]  R. Miall,et al.  Functional imaging of changes in cerebellar activity related to learning during a novel eye–hand tracking task , 2005, Experimental Brain Research.

[60]  A. Kleinschmidt,et al.  Intrinsic Connectivity Networks, Alpha Oscillations, and Tonic Alertness: A Simultaneous Electroencephalography/Functional Magnetic Resonance Imaging Study , 2010, The Journal of Neuroscience.

[61]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

[62]  Ivan Toni,et al.  Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study , 1999, Experimental Brain Research.

[63]  Julien Doyon,et al.  Functional neuroanatomical networks associated with expertise in motor imagery , 2008, NeuroImage.

[64]  Stephan P. Swinnen,et al.  Acquisition of a new bimanual coordination pattern modulates the cerebral activations elicited by an intrinsic pattern: An fMRI study , 2008, Cortex.

[65]  Sharlene D. Newman,et al.  The Timecourse of Activation Within the Cortical Network Associated with Visual Imagery , 2007, The open neuroimaging journal.

[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]  R. Passingham,et al.  Changes of cortico-striatal effective connectivity during visuomotor learning. , 2002, Cerebral cortex.

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

[69]  Leslie G. Ungerleider,et al.  Dominance of the right hemisphere and role of area 2 in human kinesthesia. , 2005, Journal of neurophysiology.

[70]  Julien Doyon,et al.  The multifaceted nature of the relationship between performance and brain activity in motor sequence learning , 2010, NeuroImage.

[71]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[72]  A. Berthoz,et al.  Role of the different frontal lobe areas in the control of the horizontal component of memory-guided saccades in man , 2004, Experimental Brain Research.

[73]  E. Naito,et al.  Visuokinesthetic Perception of Hand Movement is Mediated by Cerebro–Cerebellar Interaction between the Left Cerebellum and Right Parietal Cortex , 2008, Cerebral cortex.

[74]  S. Swinnen,et al.  Motor learning with augmented feedback: modality-dependent behavioral and neural consequences. , 2011, Cerebral cortex.

[75]  M. Hallett,et al.  Role of the human motor cortex in rapid motor learning , 2001, Experimental Brain Research.

[76]  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.

[77]  Stephan P. Swinnen,et al.  Dual-task interference during initial learning of a new motor task results from competition for the same brain areas , 2010, Neuropsychologia.

[78]  A Berthoz,et al.  Cortical control of vestibular-guided saccades in man. , 1995, Brain : a journal of neurology.

[79]  Jun Tanji,et al.  Role for supplementary motor area cells in planning several movements ahead , 1994, Nature.

[80]  Todd B. Parrish,et al.  Altered Effective Connectivity within the Language Network in Primary Progressive Aphasia , 2007, The Journal of Neuroscience.

[81]  Charles H. Shea,et al.  Bimanual 1:1 with 90° continuous relative phase: difficult or easy! , 2009, Experimental Brain Research.

[82]  Jeff H. Duyn,et al.  Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal , 2007, NeuroImage.

[83]  E. Bullmore,et al.  The relationship between regional and inter‐regional functional connectivity deficits in schizophrenia , 2012, Human brain mapping.

[84]  S. Bouisset,et al.  [Voluntary movement]. , 1953, Journal de physiologie.

[85]  Francis M Miezin,et al.  Comparison of sustained and transient activity in children and adults using a mixed blocked/event-related fMRI design , 2004, NeuroImage.

[86]  O. Sporns Networks of the Brain , 2010 .

[87]  Danielle S Bassett,et al.  Brain graphs: graphical models of the human brain connectome. , 2011, Annual review of clinical psychology.

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

[89]  Renaud Ronsse,et al.  Multisensory Integration in Dynamical Behaviors: Maximum Likelihood Estimation across Bimanual Skill Learning , 2009, The Journal of Neuroscience.

[90]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[91]  Paul Van Hecke,et al.  Internal vs external generation of movements: differential neural pathways involved in bimanual coordination performed in the presence or absence of augmented visual feedback , 2003, NeuroImage.

[92]  Robert J. Zatorre,et al.  Experience-dependent neural substrates involved in vocal pitch regulation during singing , 2008, NeuroImage.

[93]  Charles H. Shea,et al.  Amplitude differences, spatial assimilation, and integrated feedback in bimanual coordination , 2010, Experimental Brain Research.

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

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

[96]  Jeff H. Duyn,et al.  Modulation of spontaneous fMRI activity in human visual cortex by behavioral state , 2009, NeuroImage.

[97]  S. Cichon,et al.  Neural Mechanisms of a Genome-Wide Supported Psychosis Variant , 2009, Science.

[98]  S. Swinnen,et al.  Interlimb coordination: Learning and transfer under different feedback conditions , 1997 .

[99]  Scott T. Grafton,et al.  Dynamic reconfiguration of human brain networks during learning , 2010, Proceedings of the National Academy of Sciences.

[100]  Guy Marchal,et al.  Passive somatosensory discrimination tasks in healthy volunteers: Differential networks involved in familiar versus unfamiliar shape and length discrimination , 2005, NeuroImage.

[101]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[102]  Nobuko Kemmotsu,et al.  Functional MRI of motor sequence acquisition: effects of learning stage and performance. , 2002, Brain research. Cognitive brain research.

[103]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[104]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

[105]  Biyu J. He Scale-Free Properties of the Functional Magnetic Resonance Imaging Signal during Rest and Task , 2011, The Journal of Neuroscience.