Synchronization of parietal and premotor areas during preparation and execution of praxis hand movements

OBJECTIVE We sought to determine temporal patterns of functional connectivity between the parietal, premotor, and motor cortices during preparation and execution of praxis hand movements. METHODS Normal subjects were instructed to perform six transitive (tool use) and intransitive (communicative gesture) self-paced pantomimes with the right hand while recording 64-channel electroencephalography (EEG) and electromyography (EMG) from right thumb and forearm flexors. Focusing on corticocortical coherence, we explored the time-course of synchronously active parietal and premotor circuits involved in these motor tasks. Trials were marked for EMG onset and averaged across subjects to determine changes in coherence relative to baseline between parietal, premotor, and motor areas. RESULTS Coherence of homologous electrode pairs was similar when comparing transitive and intransitive movements. During preparation, beta band (18-22 Hz) coherence was maximal between electrodes over the left parietal lobe and left premotor electrodes. Additionally during preparation, the premotor area showed high coherence to the motor hand area and the parietal cortex. Electrodes over the supplementary motor area also showed coherence to the motor and parietal, but not the premotor area. Before and during execution, a second peak of high coherence increase was present in each area that demonstrated coherence increases during preparation. There was no coherence increase between parietal and motor areas. Coherence rapidly diminished 1.5-2.0 s after movement onset. CONCLUSIONS Patterns of increased corticocortical coupling within a parietal, premotor, and motor network are present during preparation and execution of praxis movements. SIGNIFICANCE This study adds to evidence that parietofrontal networks may be critical for integrating preparatory and motor-related activity for praxis movements.

[1]  D. Kareken,et al.  Functional brain imaging in apraxia. , 1998, Archives of neurology.

[2]  Scott T. Grafton,et al.  Selective Activation of a Parietofrontal Circuit during Implicitly Imagined Prehension , 2002, NeuroImage.

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

[4]  D. Halliday,et al.  The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. , 1993, The Journal of physiology.

[5]  Stephen M. Rao,et al.  Specialized Neural Systems Underlying Representations of Sequential Movements , 2000, Journal of Cognitive Neuroscience.

[6]  G. Rizzolatti,et al.  Cortical mechanism for the visual guidance of hand grasping movements in the monkey: A reversible inactivation study. , 2001, Brain : a journal of neurology.

[7]  Christoph Braun,et al.  Coherence of gamma-band EEG activity as a basis for associative learning , 1999, Nature.

[8]  T. Mima,et al.  Increased Synchronization of Cortical Oscillatory Activities between Human Supplementary Motor and Primary Sensorimotor Areas during Voluntary Movements , 2001, The Journal of Neuroscience.

[9]  Tao Wu,et al.  The role of the dorsal stream for gesture production , 2006, NeuroImage.

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

[11]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

[12]  S. Small,et al.  Functional Lateralization of the Human Premotor Cortex during Sequential Movements , 2002, Brain and Cognition.

[13]  R. J. Seitz,et al.  A fronto‐parietal circuit for object manipulation in man: evidence from an fMRI‐study , 1999, The European journal of neuroscience.

[14]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[15]  A Bartolo,et al.  Pantomimes are special gestures which rely on working memory , 2003, Brain and Cognition.

[16]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[17]  J. Tanji.  Sequential organization of multiple movements: involvement of cortical motor areas. , 2001, Annual review of neuroscience.

[18]  Mark Hallett,et al.  Generators of the Movement-Related Cortical Potentials and Dipole Source Analysis , 2003 .

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

[20]  J. Brandt,et al.  Ideomotor limb apraxia in Huntington’s disease: implications for corticostriate involvement , 2003, Neuropsychologia.

[21]  P. H. Weiss,et al.  Motor impairment in patients with parietal lesions: disturbances of meaningless arm movement sequences , 2001, Neuropsychologia.

[22]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[23]  Subcortical projections of the parietal lobes. , 2003, Advances in neurology.

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

[25]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[26]  M. Hallett,et al.  Identifying true brain interaction from EEG data using the imaginary part of coherency , 2004, Clinical Neurophysiology.

[27]  Hiroshi Shibasaki,et al.  Temporal activation pattern of parietal and premotor areas related to praxis movements , 2005, Clinical Neurophysiology.

[28]  D Yves von Cramon,et al.  Sequences of Abstract Nonbiological Stimuli Share Ventral Premotor Cortex with Action Observation and Imagery , 2004, The Journal of Neuroscience.

[29]  M. Hallett,et al.  Transient Interhemispheric Neuronal Synchrony Correlates with Object Recognition , 2001, The Journal of Neuroscience.

[30]  K M Heilman,et al.  Apraxia and the supplementary motor area. , 1986, Archives of neurology.

[31]  G Pfurtscheller,et al.  Event-related Coherence during Finger Movement: A Pilot Study - Ereignisbezogene Kohärenz während der Bewegung von Fingern: Eine Pilotstudie , 1995, Biomedizinische Technik. Biomedical engineering.

[32]  M. Hallett,et al.  Event-related coherence and event-related desynchronization/synchronization in the 10 Hz and 20 Hz EEG during self-paced movements. , 1997, Electroencephalography and clinical neurophysiology.

[33]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[34]  H. Sakata,et al.  Deficit of hand preshaping after muscimol injection in monkey parietal cortex , 1994, Neuroreport.

[35]  K. Heilman,et al.  Cortical and subcortical contributions to ideomotor apraxia: analysis of task demands and error types. , 2001, Brain : a journal of neurology.

[36]  J. R. Rosenberg,et al.  The Fourier approach to the identification of functional coupling between neuronal spike trains. , 1989, Progress in biophysics and molecular biology.

[37]  C. G. Phillips,et al.  A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis) , 1987, The Journal of comparative neurology.

[38]  A. Murata,et al.  Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4) , 1999, Experimental Brain Research.

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

[40]  S. Sala,et al.  On Crossed Apraxia. Description of a Right-Handed Apraxic Patient with Right Supplementary Motor Area Damage , 1997, Cortex.