Reduced neural differentiation between feedback conditions after training bimanual coordination with and without augmented visual feedback

It has been established that bimanual coordination with augmented feedback (FB) versus no augmented feedback (NFB) is associated with activity in different brain regions. It is unclear however, whether this distinction remains after practice comprising both these conditions. Functional magnetic resonance imaging (fMRI) was used in humans to compare visual FB versus NFB conditions for a bimanual tracking task, and their differential evolution across learning. Scanning occurred before (Pre) and after 2 weeks (Post) of mixed FB and NFB training using an event-related design, allowing differentiation between the planning and execution phase of the task. Activations at the whole brain level initially differed for FB versus NFB movements but this differentiation diminished with training for the movement execution phase. Specifically, in right PMd and right DLPFC activation increased for NFB and decreased for FB trials to converge towards the end of practice. This suggests that learning led to a decreased need to adjust the ongoing movement on the basis of FB, whereas online monitoring became more pronounced in NFB trials as discrepancies between the required and the produced motor output were detected more accurately after training, due to a generic internal reference of correctness supporting movement control under different conditions.

[1]  Jörn Diedrichsen,et al.  Skill learning strengthens cortical representations of motor sequences , 2013, eLife.

[2]  Olivier White,et al.  Flexible Switching of Feedback Control Mechanisms Allows for Learning of Different Task Dynamics , 2013, PloS one.

[3]  Axel Cleeremans,et al.  Lateralized implicit sequence learning in uni- and bi-manual conditions , 2013, Brain and Cognition.

[4]  S. Swinnen,et al.  Diffusion tensor imaging metrics of the corpus callosum in relation to bimanual coordination: Effect of task complexity and sensory feedback , 2013, Human brain mapping.

[5]  Iseult A. M. Beets,et al.  Microstructural organization of corpus callosum projections to prefrontal cortex predicts bimanual motor learning. , 2012, Learning & memory.

[6]  L. Cohen,et al.  Neuroplasticity Subserving Motor Skill Learning , 2011, Neuron.

[7]  Stephan P. Swinnen,et al.  Testing Multiple Coordination Constraints with a Novel Bimanual Visuomotor Task , 2011, PloS one.

[8]  Nicole Wenderoth,et al.  Hemispheric asymmetries of motor versus nonmotor processes during (visuo)motor control , 2011, Human brain mapping.

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

[10]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[11]  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.

[12]  Theodore P. Zanto,et al.  Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory , 2011, Nature Neuroscience.

[13]  Xue Zhang,et al.  Visual guidance modulates hemispheric asymmetries during an interlimb coordination task , 2010, NeuroImage.

[14]  Johan Wagemans,et al.  Shared neural resources between left and right interlimb coordination skills: The neural substrate of abstract motor representations , 2010, NeuroImage.

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

[16]  Stephan P. Swinnen,et al.  Ipsilateral coordination at preferred rate: Effects of age, body side and task complexity , 2009, NeuroImage.

[17]  Transient disruption of M1 during response planning impairs subsequent offline consolidation , 2009, Experimental Brain Research.

[18]  Jörn Diedrichsen,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[19]  Mark W. Woolrich,et al.  Bayesian analysis of neuroimaging data in FSL , 2009, NeuroImage.

[20]  Jeremy D. Schmahmann,et al.  Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies , 2009, NeuroImage.

[21]  P. Haggard Human volition: towards a neuroscience of will , 2008, Nature Reviews Neuroscience.

[22]  Claudio Babiloni,et al.  Human secondary somatosensory cortex is involved in the processing of somatosensory rare stimuli: An fMRI study , 2008, NeuroImage.

[23]  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.

[24]  Emily S. Cross,et al.  Neural Substrates of Contextual Interference during Motor Learning Support a Model of Active Preparation , 2007, Journal of Cognitive Neuroscience.

[25]  Simon B. Eickhoff,et al.  Assignment of functional activations to probabilistic cytoarchitectonic areas revisited , 2007, NeuroImage.

[26]  N. Makris,et al.  Hypothalamic Abnormalities in Schizophrenia: Sex Effects and Genetic Vulnerability , 2007, Biological Psychiatry.

[27]  Toshio Inui,et al.  Separating brain regions involved in internally guided and visual feedback control of moving effectors: An event-related fMRI study , 2006, NeuroImage.

[28]  Simon B. Eickhoff,et al.  Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps , 2006, NeuroImage.

[29]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.

[30]  Deborah L. Harrington,et al.  From preparation to online control: Reappraisal of neural circuitry mediating internally generated and externally guided actions , 2006, NeuroImage.

[31]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

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

[33]  N. Makris,et al.  Decreased volume of left and total anterior insular lobule in schizophrenia , 2006, Schizophrenia Research.

[34]  S. Swinnen,et al.  Dynamics of hemispheric specialization and integration in the context of motor control , 2006, Nature Reviews Neuroscience.

[35]  A. Amedi,et al.  Functional imaging of human crossmodal identification and object recognition , 2005, Experimental Brain Research.

[36]  S. Rauch,et al.  Structural brain magnetic resonance imaging of limbic and thalamic volumes in pediatric bipolar disorder. , 2005, The American journal of psychiatry.

[37]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[38]  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.

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

[40]  S M Smith,et al.  Overview of fMRI analysis. , 2004, The British journal of radiology.

[41]  A. Berthoz,et al.  Reference Frames for Spatial Cognition: Different Brain Areas are Involved in Viewer-, Object-, and Landmark-Centered Judgments About Object Location , 2004, Journal of Cognitive Neuroscience.

[42]  Nicole Wenderoth,et al.  Parieto-premotor areas mediate directional interference during bimanual movements. , 2004, Cerebral cortex.

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

[44]  R. Passingham,et al.  The sensory guidance of movement: a comparison of the cerebellum and basal ganglia , 1996, Experimental Brain Research.

[45]  Alvaro Pascual-Leone,et al.  Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions , 2003, NeuroImage.

[46]  M. Rushworth,et al.  The left parietal and premotor cortices: motor attention and selection , 2003, NeuroImage.

[47]  D. Vaillancourt,et al.  Neural Basis for the Processes That Underlie Visually-guided and Internally-guided Force Control in Humans , 2003 .

[48]  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.

[49]  Yufeng Zang,et al.  Functional organization of the primary motor cortex characterized by event-related fMRI during movement preparation and execution , 2003, Neuroscience Letters.

[50]  S. Bressler,et al.  Synchronized activity in prefrontal cortex during anticipation of visuomotor processing , 2002, Neuroreport.

[51]  A. Oliviero,et al.  Repetitive transcranial magnetic stimulation of the supplementary motor area (SMA) degrades bimanual movement control in humans , 2002, Neuroscience Letters.

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

[53]  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.

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

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

[56]  M. Wiesendanger,et al.  Different Ipsilateral Representations for Distal and Proximal Movements in the Sensorimotor Cortex: Activation and Deactivation Patterns , 2001, NeuroImage.

[57]  Yu-Feng Zang,et al.  Both sides of human cerebellum involved in preparation and execution of sequential movements , 2000, Neuroreport.

[58]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[59]  J F Stein,et al.  Temporary inactivation in the primate motor thalamus during visually triggered and internally generated limb movements. , 2000, Journal of neurophysiology.

[60]  H Burton,et al.  Tactile attention tasks enhance activation in somatosensory regions of parietal cortex: a positron emission tomography study. , 1999, Cerebral cortex.

[61]  J F Stein,et al.  Neuronal activity in the primate motor thalamus during visually triggered and internally generated limb movements. , 1999, Journal of neurophysiology.

[62]  J. Marshall,et al.  The neural consequences of conflict between intention and the senses. , 1999, Brain : a journal of neurology.

[63]  B R Rosen,et al.  Activation of distinct motor cortex regions during ipsilateral and contralateral finger movements. , 1999, Journal of neurophysiology.

[64]  Hiroshi Shibasaki,et al.  Attention modulates both primary and second somatosensory cortical activities in humans: a magnetoencephalographic study. , 1998, Journal of neurophysiology.

[65]  M. Jüptner,et al.  A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. , 1998, Brain : a journal of neurology.

[66]  N. Sadato,et al.  Regional cerebral blood flow changes in human brain related to ipsilateral and contralateral complex hand movements – a PET study , 1998, The European journal of neuroscience.

[67]  K Ugurbil,et al.  Activation of visuomotor systems during visually guided movements: a functional MRI study. , 1998, Journal of magnetic resonance.

[68]  A Schnitzler,et al.  Handedness and asymmetry of hand representation in human motor cortex. , 1998, Journal of neurophysiology.

[69]  Scott T. Grafton,et al.  Dorsal premotor cortex and conditional movement selection: A PET functional mapping study. , 1998, Journal of neurophysiology.

[70]  S. Kinomura,et al.  PET study of pointing with visual feedback of moving hands. , 1998, Journal of neurophysiology.

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

[72]  Natalia Dounskaia,et al.  Preferred and induced coordination modes during the acquisition of bimanual movements with a 2 :1 frequency ratio , 1997 .

[73]  A. Georgopoulos,et al.  Sequential activity in human motor areas during a delayed cued finger movement task studied by time‐resolved fMRI , 1997, Neuroreport.

[74]  V M Haughton,et al.  Ipsilateral hemisphere activation during motor and sensory tasks. , 1996, AJNR. American journal of neuroradiology.

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

[76]  P. van Donkelaar,et al.  Interactions between the eye and hand motor systems: disruptions due to cerebellar dysfunction. , 1994, Journal of neurophysiology.

[77]  S. Kinomura,et al.  Regional cerebral blood flow changes of cortical motor areas and prefrontal areas in humans related to ipsilateral and contralateral hand movement , 1993, Brain Research.

[78]  C R Olson,et al.  Posterior cingulate cortex: sensory and oculomotor properties of single neurons in behaving cat. , 1992, Cerebral cortex.

[79]  Scott T. Grafton,et al.  Human functional anatomy of visually guided finger movements. , 1992, Brain : a journal of neurology.

[80]  R. Schmidt,et al.  Reduced frequency of knowledge of results enhances motor skill learning. , 1990 .

[81]  J. Stein,et al.  Role of the cerebellum in the visual guidance of movement. , 1992, Nature.

[82]  J. F. Stein,et al.  Role of the cerebellum in the visual guidance of movement , 1986, Nature.

[83]  R. Passingham,et al.  Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis) , 1985, Behavioural Brain Research.

[84]  R. Schmidt,et al.  Knowledge of results and motor learning: a review and critical reappraisal. , 1984, Psychological bulletin.

[85]  Timothy D. Lee,et al.  Motor Control and Learning: A Behavioral Emphasis , 1982 .

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