Cerebral cortical dynamics during visuomotor transformation: adaptation to a cognitive-motor executive challenge.

EEG was employed during cognitive-motor adaptation to a visuomotor transformation that required inhibition of an established motor plan. Performance was positively related to frontal alpha and theta power during both planning and execution of reaching movements to visual targets. EEG changes suggest initial involvement of frontal executive functioning to suppress established visuomotor mappings followed by progressive idling (i.e., alpha synchrony). Also, progressive idling of the temporal and parietal sites over the trials was observed, suggesting a decreasing role of working memory and encoding of the new visuomotor map, respectively. The regional changes in the cortical dynamics translated into the quality of motor behavior. This study expands our understanding of the role of frontal executive processes beyond the cognitive domain to the cognitive-motor domain.

[1]  L. Cohen,et al.  Brain–computer interfaces: communication and restoration of movement in paralysis , 2007, The Journal of physiology.

[2]  Arthur P. Shimamura,et al.  The role of the prefrontal cortex in dynamic filtering , 2000, Psychobiology.

[3]  Joaquin A. Anguera,et al.  Changes in Performance Monitoring during Sensorimotor Adaptation Yfi(\ Aq: a ~·~i.ku"w , 2022 .

[4]  Simon Hanslmayr,et al.  Conflict processing in the anterior cingulate cortex constrains response priming , 2010, NeuroImage.

[5]  D. Noll,et al.  Bilateral basal ganglia activation associated with sensorimotor adaptation , 2006, Experimental Brain Research.

[6]  Michael E. Hasselmo,et al.  A Proposed Function for Hippocampal Theta Rhythm: Separate Phases of Encoding and Retrieval Enhance Reversal of Prior Learning , 2002, Neural Computation.

[7]  José Luis Contreras-Vidal,et al.  Decoding center-out hand velocity from MEG signals during visuomotor adaptation , 2009, NeuroImage.

[8]  G. Lynch,et al.  Theta pattern stimulation and the induction of LTP: the sequence in which synapses are stimulated determines the degree to which they potentiate , 1989, Brain Research.

[9]  J. Contreras-Vidal,et al.  Adaptation of sound localization induced by rotated visual feedback in reaching movements , 2009, Experimental Brain Research.

[10]  A. Sterr,et al.  Short-term learning of a visually guided power-grip task is associated with dynamic changes in EEG oscillatory activity , 2008, Clinical Neurophysiology.

[11]  A. Georgopoulos,et al.  Synchronous neural interactions assessed by magnetoencephalography: a functional biomarker for brain disorders , 2007, Journal of neural engineering.

[12]  Ehren L. Newman,et al.  Human θ Oscillations Related to Sensorimotor Integration and Spatial Learning , 2003, The Journal of Neuroscience.

[13]  Hiroshi Imamizu,et al.  Human cerebellar activity reflecting an acquired internal model of a new tool , 2000, Nature.

[14]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

[15]  D. Tucker,et al.  Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation , 2004, Clinical Neurophysiology.

[16]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[17]  John J. B. Allen,et al.  Theta EEG dynamics of the error-related negativity , 2007, Clinical Neurophysiology.

[18]  Scott E Kerick,et al.  Independent component analysis of dynamic brain responses during visuomotor adaptation , 2004, NeuroImage.

[19]  Claudio Del Percio,et al.  “Neural efficiency” of athletes’ brain for upright standing: A high-resolution EEG study , 2009, Brain Research Bulletin.

[20]  S. D. Berry,et al.  Oscillatory brain states and learning: Impact of hippocampal theta-contingent training , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[21]  B. Oken,et al.  Vigilance, alertness, or sustained attention: physiological basis and measurement , 2006, Clinical Neurophysiology.

[22]  Ivan Toni,et al.  Movement Preparation and Motor Intention , 2001, NeuroImage.

[23]  Ethan R. Buch,et al.  Effects of Parkinson's disease on visuomotor adaptation , 2003, Experimental Brain Research.

[24]  T. Braver,et al.  The Role of Frontopolar Cortex in Subgoal Processing during Working Memory , 2002, NeuroImage.

[25]  Joaquin A. Anguera,et al.  Neural correlates associated with intermanual transfer of sensorimotor adaptation , 2007, Brain Research.

[26]  B. Hatfield,et al.  Cerebral cortical adaptations associated with visuomotor practice. , 2004, Medicine and science in sports and exercise.

[27]  M. Hogge,et al.  Exploration of the neural substrates of executive functioning by functional neuroimaging , 2006, Neuroscience.

[28]  Bradley D. Hatfield,et al.  Neuro-cognitive activity during a self-paced visuospatial task: comparative EEG profiles in marksmen and novice shooters , 2000, Biological Psychology.

[29]  P. Rossini,et al.  The role of prefrontal cortex in visuo-spatial planning: a repetitive TMS study , 2006, Experimental Brain Research.

[30]  S. Slobounov,et al.  Modulation of cortical activity as a result of task-specific practice , 2007, Neuroscience Letters.

[31]  S. Kinomura,et al.  Activity in the parietal area during visuomotor learning with optical rotation , 1997, Neuroreport.

[32]  Andrea Berger,et al.  When things look wrong: Theta activity in rule violation , 2007, Neuropsychologia.

[33]  J. Gabrieli,et al.  The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex , 2000, Psychobiology.

[34]  Joseph R. Madsen,et al.  Human theta oscillations exhibit task dependence during virtual maze navigation , 1999, Nature.

[35]  R. Shadmehr,et al.  Neural correlates of motor memory consolidation. , 1997, Science.

[36]  R J Seitz,et al.  Representations of Graphomotor Trajectories in the Human Parietal Cortex: Evidence for Controlled Processing and Automatic Performance , 1997, The European journal of neuroscience.

[37]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

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

[39]  T. Sejnowski,et al.  Awareness during drowsiness: dynamics and electrophysiological correlates. , 2000, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[40]  P. Davis,et al.  HUMAN BRAIN POTENTIALS DURING THE ONSET OF SLEEP , 1938 .

[41]  F. Collette,et al.  Brain imaging of the central executive component of working memory , 2002, Neuroscience & Biobehavioral Reviews.

[42]  Claudio Del Percio,et al.  Is there a “neural efficiency” in athletes? A high-resolution EEG study , 2008, NeuroImage.

[43]  T. Jung,et al.  Changes in alertness are a principal component of variance in the EEG spectrum , 1995, Neuroreport.

[44]  H. Huynh,et al.  Estimation of the Box Correction for Degrees of Freedom from Sample Data in Randomized Block and Split-Plot Designs , 1976 .

[45]  O. Hikosaka,et al.  Transition of Brain Activation from Frontal to Parietal Areas in Visuomotor Sequence Learning , 1998, The Journal of Neuroscience.

[46]  Tsung-Min Hung,et al.  Electroencephalographic Studies of Skilled Psychomotor Performance , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[47]  R. Shadmehr,et al.  Inhibitory control of competing motor memories , 1999, Experimental Brain Research.

[48]  S. Blakemore,et al.  Action prediction in the cerebellum and in the parietal lobe , 2003, Experimental Brain Research.

[49]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[50]  Juliana Yordanova,et al.  Parallel systems of error processing in the brain , 2004, NeuroImage.

[51]  A. Gevins,et al.  Neurophysiological measures of working memory and individual differences in cognitive ability and cognitive style. , 2000, Cerebral cortex.

[52]  A. Sirigu,et al.  The Mental Representation of Hand Movements After Parietal Cortex Damage , 1996, Science.

[53]  John J. B. Allen,et al.  Prelude to and Resolution of an Error: EEG Phase Synchrony Reveals Cognitive Control Dynamics during Action Monitoring , 2009, The Journal of Neuroscience.

[54]  M. J. Emerson,et al.  The Unity and Diversity of Executive Functions and Their Contributions to Complex “Frontal Lobe” Tasks: A Latent Variable Analysis , 2000, Cognitive Psychology.

[55]  L. McEvoy,et al.  Neurophysiological indices of strategy development and skill acquisition. , 1999, Brain research. Cognitive brain research.

[56]  Paul Cisek,et al.  Cortical mechanisms of action selection: the affordance competition hypothesis , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[57]  G. Pfurtscheller,et al.  Event-related synchronization (ERS) in the alpha band--an electrophysiological correlate of cortical idling: a review. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[58]  D C Noll,et al.  Neuroanatomical correlates of motor acquisition and motor transfer. , 2008, Journal of neurophysiology.

[59]  Jörn Diedrichsen,et al.  Reach adaptation: what determines whether we learn an internal model of the tool or adapt the model of our arm? , 2008, Journal of neurophysiology.