EEG dynamics of the frontoparietal network during reaching preparation in humans

Visuomotor transformation processes are essential when accurate reaching movements towards a visual target have to be performed. In contrast, those transformations are not needed for similar, but non-visually guided, arm movements. According to previous studies, these transformations are carried out by neuronal populations located in the parietal and frontal cortical areas (the so-called "dorsal visual stream"). However, it is still debated whether these processes are mediated by the sequential and/or parallel activation of the frontoparietal areas. To investigate this issue, we designed a task where the same visual cue could represent either the target of a reaching/pointing movement or the go-signal for a similar but non-targeting arm movement. By subtracting the event-related potentials (ERPs) recorded from healthy subjects performing the two conditions, we identified the brain processes underlying the visuomotor transformations needed for accurate reaching/pointing movements. We then localized the generators by means of cortical current density (CCD) reconstruction and studied their dynamics from visual cue presentation to movement onset. The results showed simultaneous activation of the parietal and frontal areas from 140 to 260 ms. The results are interpreted as neural correlates of two critical phases of visuomotor integration, namely target selection and movement selection. Our findings suggest that the visuomotor transformation processes required for correct reaching/pointing movements do not rely on a purely sequential activation of the frontoparietal areas, but mainly on a parallel information processing system, where feedback circuits play an important role before movement onset.

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

[2]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[3]  M. Corbetta,et al.  Functional Organization of Human Intraparietal and Frontal Cortex for Attending, Looking, and Pointing , 2003, The Journal of Neuroscience.

[4]  Jun Tanji,et al.  Area-selective neuronal activity in the dorsolateral prefrontal cortex for information retrieval and action planning. , 2004, Journal of neurophysiology.

[5]  Michela Gamberini,et al.  ‘Arm‐reaching’ neurons in the parietal area V6A of the macaque monkey , 2001, The European journal of neuroscience.

[6]  Anthony R. Dickinson,et al.  Non-spatial, motor-specific activation in posterior parietal cortex , 2002, Nature Neuroscience.

[7]  J. Kalaska,et al.  Cerebral cortical mechanisms of reaching movements. , 1992, Science.

[8]  C. Galletti,et al.  Spatial tuning of reaching activity in the medial parieto‐occipital cortex (area V6A) of macaque monkey , 2005, The European journal of neuroscience.

[9]  M. Hallett,et al.  Integrative visuomotor behavior is associated with interregionally coherent oscillations in the human brain. , 1998, Journal of neurophysiology.

[10]  M. Perenin,et al.  Cortical control of visually guided reaching: evidence from patients with optic ataxia. , 2005, Cerebral cortex.

[11]  M. Fuchs,et al.  Linear and nonlinear current density reconstructions. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[12]  E. Harth,et al.  Electric Fields of the Brain: The Neurophysics of Eeg , 2005 .

[13]  Heinrich H Bülthoff,et al.  Effects of rearranged vision on event-related lateralizations of the EEG during pointing , 2004, Biological Psychology.

[14]  C. Galletti,et al.  Cortical mechanisms for visual perception of object motion and position in space , 1996, Behavioural Brain Research.

[15]  Kaleb McDowell,et al.  Behavioral and electrocortical evidence of an interaction between probability and task metrics in movement preparation , 2002, Experimental Brain Research.

[16]  T. Vilis,et al.  Integration of target and effector information in human posterior parietal cortex for the planning of action. , 2005, Journal of neurophysiology.

[17]  David J. Turk,et al.  Placing a tool in the spotlight: spatial attention modulates visuomotor responses in cortex , 2005, NeuroImage.

[18]  J. Tanji,et al.  Functional specialization in dorsal and ventral premotor areas. , 2004, Progress in brain research.

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

[20]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[21]  C. Galletti,et al.  Functional Demarcation of a Border Between Areas V6 and V6A in the Superior Parietal Gyrus of the Macaque Monkey , 1996, The European journal of neuroscience.

[22]  P. Roland,et al.  Functional anatomy of reaching and visuomotor learning: a positron emission tomography study. , 1995, Cerebral cortex.

[23]  J. Culham,et al.  The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? , 2006, Neuropsychologia.

[24]  W. Singer,et al.  Visuomotor integration is associated with zero time-lag synchronization among cortical areas , 1997, Nature.

[25]  G. Fink,et al.  REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys , 2005, Journal of anatomy.

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

[27]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[28]  F. Lacquaniti,et al.  Parieto-frontal coding of reaching: an integrated framework , 1999, Experimental Brain Research.

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

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

[31]  Donatella Spinelli,et al.  Electrophysiological evidence for an early attentional mechanism in visual processing in humans , 1999, Vision Research.

[32]  J. Tanji,et al.  Differential roles of neuronal activity in the supplementary and presupplementary motor areas: from information retrieval to motor planning and execution. , 2004, Journal of neurophysiology.

[33]  Scott T. Grafton,et al.  Functional anatomy of pointing and grasping in humans. , 1996, Cerebral cortex.

[34]  Kenneth F. Valyear,et al.  Human parietal cortex in action , 2006, Current Opinion in Neurobiology.

[35]  E. Halgren,et al.  Spatiotemporal mapping of brain activity by integration of multiple imaging modalities , 2001, Current Opinion in Neurobiology.

[36]  Yale E. Cohen,et al.  A common reference frame for movement plans in the posterior parietal cortex , 2002, Nature Reviews Neuroscience.

[37]  T. Ebner,et al.  Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. , 1995, Journal of neurophysiology.

[38]  Heinrich H Bülthoff,et al.  Effects of pointing direction and direction predictability on event-related lateralizations of the EEG. , 2002, Human movement science.

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

[40]  Richard A. Andersen,et al.  FMRI evidence for a 'parietal reach region' in the human brain , 2003, Experimental Brain Research.

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

[42]  B. Feige,et al.  The Role of Higher-Order Motor Areas in Voluntary Movement as Revealed by High-Resolution EEG and fMRI , 1999, NeuroImage.

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