Analyzing a complex visuomotor tracking task with brain-electrical event related potentials.

Non-invasive techniques such as neuroimaging and event-related potential (ERP) methods have dramatically enhanced our understanding of the human brain. According to the requirements of the applied method, it is useful to simplify tasks for methodological reasons. In the present study we tested whether ERP measures are also suitable for analyzing complex tasks. In order to do this, we developed an analysis strategy based on the post hoc analysis of the behavioural data. We applied this method to a pursuit-tracking task of 25 s trial duration, consisting of repeated and non-repeated waveforms, where subjects had to track a target cross with a mouse-controlled cursor cross. An EEG was recorded from 62 channels. Response-locked ERPs were computed for two types of error correction: the correction of errors induced externally by the change of target direction and of internal errors generated by the subject itself. We found several ERP components that could be assigned to different feedback and feedforward controlled processing steps in the frontoparietal circuitry underlying visuomotor control, such as movement planning, movement execution (motor potential), reafferent activity, visuospatial analysis, and attentional (P300) processes. Our results support newer models that propose a role for the posterior parietal cortex in integrating multimodal sensory information. In addition, fast (about 180 ms and probably facilitated by anticipation) and slow (about 230-260 ms) error corrections could be differentiated by the time course of ERP activity. Our results show that complex (motor) tasks can be investigated with ERPs. This opens fruitful perspectives for future research on motor control in an ecological setting.

[1]  Margot J. Taylor,et al.  Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. , 2000, Psychophysiology.

[2]  J Decety,et al.  Is perceptual anticipation a motor simulation? A PET study , 2001, Neuroreport.

[3]  R. Cooper,et al.  Slow potential changes related to the velocity of target movement in a tracking task. , 1989, Electroencephalography and clinical neurophysiology.

[4]  Scott T. Grafton,et al.  Abstract and Effector-Specific Representations of Motor Sequences Identified with PET , 1998, The Journal of Neuroscience.

[5]  Jun Tanji,et al.  Integration of target and body-part information in the premotor cortex when planning action , 2000, Nature.

[6]  Jane Dywan,et al.  Error-negativity and positivity as they relate to other ERP indices of attentional control and stimulus processing , 2001, Biological Psychology.

[7]  O Bertrand,et al.  A theoretical justification of the average reference in topographic evoked potential studies. , 1985, Electroencephalography and clinical neurophysiology.

[8]  H Shibasaki,et al.  Components of the movement-related cortical potential and their scalp topography. , 1980, Electroencephalography and clinical neurophysiology.

[9]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[10]  D. Wolpert,et al.  The cerebellum is involved in predicting the sensory consequences of action , 1999, Neuroreport.

[11]  Takashi Hanakawa,et al.  Functional mapping of human medial frontal motor areas , 2001, Experimental Brain Research.

[12]  J. Polich,et al.  P3a and P3b from typical auditory and visual stimuli , 1999, Clinical Neurophysiology.

[13]  A M Paans,et al.  The distribution of cerebral activity related to visuomotor coordination indicating perceptual and executional specialization. , 1999, Brain research. Cognitive brain research.

[14]  M Hallett,et al.  Source analysis of scalp-recorded movement-related electrical potentials. , 1993, Electroencephalography and clinical neurophysiology.

[15]  Peter D. Neilson,et al.  What limits high speed tracking performance , 1993 .

[16]  H. Kornhuber,et al.  Brain Potentials Associated with Voluntary Manual Tracking: Bereitschaftspotential, Conditioned Premotion Positivity, Directed Attention Potential, and Relaxation Potential , 1984, Annals of the New York Academy of Sciences.

[17]  Peter D. Neilson,et al.  A neuroengineering solution to the optimal tracking problem , 1999 .

[18]  R T Knight,et al.  Neural representations of skilled movement. , 2000, Brain : a journal of neurology.

[19]  S. Slobounov,et al.  Movement-related potentials are task or end-effector dependent: evidence from a multifinger experiment , 2000, Experimental Brain Research.

[20]  J. Nedzelski.  Advances in Audiology , 1985 .

[21]  R. Knight,et al.  Frontal-parietal event-related potential changes associated with practising a novel visuomotor task. , 2002, Brain research. Cognitive brain research.

[22]  R. Miall,et al.  Cues and control strategies in visually guided tracking. , 1989, Journal of motor behavior.

[23]  J. Donoghue,et al.  Shared neural substrates controlling hand movements in human motor cortex. , 1995, Science.

[24]  R. Miall,et al.  The cerebellum coordinates eye and hand tracking movements , 2001, Nature Neuroscience.

[25]  D. Tucker,et al.  Scalp electrode impedance, infection risk, and EEG data quality , 2001, Clinical Neurophysiology.

[26]  William J. Ray,et al.  Movement-related potentials with reference to isometric force output in discrete and repetitive tasks , 1998, Experimental Brain Research.

[27]  John Polich,et al.  P3a from a passive visual stimulus task , 2001, Clinical Neurophysiology.

[28]  R. Schmidt,et al.  VARIABILITY OF PRACTICE AND IMPLICIT MOTOR LEARNING , 1997 .

[29]  The cortical basis of motor planning: does it take two to tango? , 2002, Nature Neuroscience.

[30]  D. V. von Cramon,et al.  Functional organization of the lateral premotor cortex: fMRI reveals different regions activated by anticipation of object properties, location and speed. , 2001, Brain research. Cognitive brain research.

[31]  Methoden der Quellenanalyse spontaner und evozierter Hirnstromaktivität , 1993 .

[32]  G. V. Simpson,et al.  Flow of activation from V1 to frontal cortex in humans , 2001, Experimental Brain Research.

[33]  Shigenobu Nakamura,et al.  Role of human SII cortices in sensorimotor integration , 2002, Clinical Neurophysiology.

[34]  Paolo Maria Rossini,et al.  Changes in movement-related brain activity during transient deafferentation: a neuromagnetic study , 1996, Brain Research.

[35]  R. Ivry,et al.  Can We Teach the Cerebellum New Tricks? , 2002, Science.

[36]  Guang H. Yue,et al.  Relationship between motor activity-related cortical potential and voluntary muscle activation , 2000, Experimental Brain Research.

[37]  Scott T. Grafton,et al.  Role of the posterior parietal cortex in updating reaching movements to a visual target , 1999, Nature Neuroscience.

[38]  W Lang,et al.  Generation of movement-related potentials and fields in the supplementary sensorimotor area and the primary motor area. , 1996, Advances in neurology.

[39]  V. Ramachandran,et al.  Encyclopedia of the Human Brain , 2002 .

[40]  R. Malmo,et al.  On electromyographic (EMG) gradients and movement-related brain activity: significance for motor control, cognitive functions, and certain psychopathologies. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  G. McCarthy,et al.  Functional organization of human supplementary motor cortex studied by electrical stimulation , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  J. Cohen,et al.  P300, stimulus intensity, modality, and probability. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[43]  P. Strick,et al.  Motor areas in the frontal lobe of the primate , 2002, Physiology & Behavior.

[44]  Jing Z. Liu,et al.  Relationship between muscle output and functional MRI-measured brain activation , 2001, Experimental Brain Research.

[45]  J. Röschke,et al.  Single trial analysis of event related potentials: A comparison between schizophrenics and depressives , 1996, Biological Psychiatry.

[46]  W. Pritchard.  Psychophysiology of P300. , 1981, Psychological bulletin.

[47]  T Fernández,et al.  Primary task demands modulate P3a amplitude. , 2000, Brain research. Cognitive brain research.

[48]  E. Holst,et al.  Das Reafferenzprinzip , 2004, Naturwissenschaften.

[49]  M Hallett,et al.  Movement-related cortical potentials. , 1994, Electromyography and clinical neurophysiology.

[50]  R. Goebel,et al.  The experimental combination of rTMS and fMRI reveals the functional relevance of parietal cortex for visuospatial functions. , 2002, Brain research. Cognitive brain research.

[51]  M Barinaga.  Remapping the motor cortex. , 1995, Science.

[52]  D. Wolpert,et al.  Central cancellation of self-produced tickle sensation , 1998, Nature Neuroscience.

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

[54]  M. Honda,et al.  Both primary motor cortex and supplementary motor area play an important role in complex finger movement. , 1993, Brain : a journal of neurology.

[55]  J. Nielsen,et al.  Cerebral activation during bicycle movements in man , 2000, Experimental Brain Research.

[56]  R. Passingham,et al.  Signal-, set-, and movement-related activity in the human premotor cortex , 1998, Neuropsychologia.

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

[58]  Marilyn K. Strube,et al.  Automatic vs. controlled processes in semantic priming--differentiation by event-related potentials. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[59]  S. Small,et al.  Somatotopy in human primary motor and somatosensory hand representations revisited. , 2001, Cerebral cortex.

[60]  Ravi S. Menon,et al.  Human fMRI evidence for the neural correlates of preparatory set , 2002, Nature Neuroscience.

[61]  E. C. Poulton,et al.  THE BASIS OF PERCEPTUAL ANTICIPATION IN TRACKING , 1952 .

[62]  M. Scherg.  Fundamentals if dipole source potential analysis , 1990 .

[63]  Scott T. Grafton,et al.  Motor Learning of Compatible and Incompatible Visuomotor Maps , 2001, Journal of Cognitive Neuroscience.

[64]  Dylan F. Cooke,et al.  The Cortical Control of Movement Revisited , 2002, Neuron.

[65]  E Grünewald-Zuberbier,et al.  Movement‐Associated Potentials and Motor Control Report of the EPIC VI Motor Panel , 1984, Annals of the New York Academy of Sciences.

[66]  M. Iacoboni.  Adjusting reaches: feedback in the posterior parietal cortex , 1999, Nature Neuroscience.

[67]  K. Bötzel,et al.  Topography and dipole analysis of reafferent electrical brain activity following the Bereitschaftspotential , 1997, Experimental Brain Research.

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

[69]  C. Shea,et al.  Principles derived from the study of simple skills do not generalize to complex skill learning , 2002, Psychonomic bulletin & review.