Cortical Activity Prior to, and During, Observation and Execution of Sequential Finger Movements

SummaryThe aim of this study was to provide further evidence for the existence of a mirror neuron system in humans using electroencephalography during the observation and execution of non-object-related movements. Event-related desynchronization and synchronization (ERD/ERS) were used to characterize brain activity prior to, and during, observation and execution of a finger movement in four frequency bands (7–10 Hz, 10–13 Hz, 13–20 Hz, and 20–30 Hz). Electroencephalograms (EEGs) were recorded from 19 electrode sites in eight participants. In all the frequency bands and electrode sites, results revealed that there was no significant differences in EEG cortical activity between the observation condition and the execution conditions. Comparison of the two stages of the movement (i.e., pre-movement and movement) in the observation and execution conditions showed, in most cases, that pre-movement ERD values were less than movement ERD values. Whilst there was not an identical match of EEG cortical indices, this study provides further support for the existence of a mirror neuron system in humans. The incomplete congruence may be explained by the different behaviors, the nature of the task and factors in the observed action coded by the mirror system.

[1]  D. Kiper,et al.  Visual stimulus-dependent changes in interhemispheric EEG coherence in ferrets. , 1999, Journal of neurophysiology.

[2]  G. Pfurtscheller,et al.  Early onset of post-movement beta electroencephalogram synchronization in the supplementary motor area during self-paced finger movement in man , 2003, Neuroscience Letters.

[3]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[4]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[5]  C. Stam,et al.  Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets , 2002 .

[6]  J. Meyer,et al.  Functional brain imaging. , 1995, Journal of neurology, neurosurgery, and psychiatry.

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

[8]  C. Stam,et al.  Variability of EEG synchronization prior to and during observation and execution of a sequential finger movement , 2006, Human brain mapping.

[9]  Michael Chopp,et al.  In vivo magnetic resonance imaging tracks adult neural progenitor cell targeting of brain tumor , 2004, NeuroImage.

[10]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[11]  M. Hallett,et al.  Task-related coherence and task-related spectral power changes during sequential finger movements. , 1998, Electroencephalography and clinical neurophysiology.

[12]  J C Mazziotta,et al.  Reafferent copies of imitated actions in the right superior temporal cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  K J Blinowska,et al.  Unbiased high resolution method of EEG analysis in time-frequency space. , 2001, Acta neurobiologiae experimentalis.

[14]  G. Pfurtscheller,et al.  Event-related cortical desynchronization detected by power measurements of scalp EEG. , 1977, Electroencephalography and clinical neurophysiology.

[15]  F. Boiten,et al.  Event-related desynchronization: the effects of energetic and computational demands. , 1992, Electroencephalography and clinical neurophysiology.

[16]  Martin Vetterli,et al.  Fast Fourier transforms: a tutorial review and a state of the art , 1990 .

[17]  P. Hazemann,et al.  Handbook of Electroencephalography and Clinical Neurophysiology , 1975 .

[18]  Andrew N. Meltzoff,et al.  Neural circuits involved in imitation and perspective-taking , 2006, NeuroImage.

[19]  G. Pfurtscheller,et al.  Post-movement beta synchronization. A correlate of an idling motor area? , 1996, Electroencephalography and clinical neurophysiology.

[20]  Blake W. Johnson,et al.  Changes in rolandic mu rhythm during observation of a precision grip. , 2004, Psychophysiology.

[21]  M. Sterman,et al.  Multiband topographic EEG analysis of a simulated visuomotor aviation task. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[22]  S. Blakemore,et al.  Motor activation prior to observation of a predicted movement , 2004, Nature Neuroscience.

[23]  M. Shiffrar,et al.  New aspects of motion perception: selective neural encoding of apparent human movements , 2000, Neuroreport.

[24]  N. A. Borghese,et al.  Different Brain Correlates for Watching Real and Virtual Hand Actions , 2001, NeuroImage.

[25]  A. E. Schulman,et al.  Functional coupling of human cortical sensorimotor areas during bimanual skill acquisition. , 1999, Brain : a journal of neurology.

[26]  B. Fisch,et al.  The role of quantitative topographic mapping or 'neurometrics' in the diagnosis of psychiatric and neurological disorders: the cons. , 1989, Electroencephalography and clinical neurophysiology.

[27]  Vladimir Medved,et al.  Standards for Reporting EMG Data , 2000, Journal of Electromyography and Kinesiology.

[28]  G. Rizzolatti,et al.  Neural Circuits Involved in the Recognition of Actions Performed by Nonconspecifics: An fMRI Study , 2004, Journal of Cognitive Neuroscience.

[29]  Blake W. Johnson,et al.  Mu rhythm modulation during observation of an object-directed grasp. , 2004, Brain research. Cognitive brain research.

[30]  J. Decety,et al.  Top down effect of strategy on the perception of human biological motion: a pet investigation. , 1998, Cognitive neuropsychology.

[31]  Á. Pascual-Leone,et al.  Motor facilitation while observing hand actions: specificity of the effect and role of observer's orientation. , 2002, Journal of neurophysiology.

[32]  A. Urbano,et al.  Performances of surface Laplacian estimators: A study of simulated and real scalp potential distributions , 2005, Brain Topography.

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

[34]  G. Rizzolatti The mirror neuron system and its function in humans , 2005, Anatomy and Embryology.

[35]  A. Urbano,et al.  Spline Laplacian estimate of EEG potentials over a realistic magnetic resonance-constructed scalp surface model. , 1996, Electroencephalography and clinical neurophysiology.

[36]  C. M. Michel,et al.  Intracerebral dipole sources of EEG FFT power maps , 2005, Brain Topography.

[37]  G. Holmes Event-Related Desynchronization. Handbook of Electroencephalography and Clinical Neurophysiology, Revised Series, Volume 6 Edited by G. Pfurtscheller and F.H. Lopes da Silva. Elsevier Science B.V., Amsterdam, 1999, 406 pp., $236.00 , 2002, Epilepsy Research.

[38]  Febo Cincotti,et al.  Human Cortical Electroencephalography (EEG) Rhythms during the Observation of Simple Aimless Movements: A High-Resolution EEG Study , 2002, NeuroImage.

[39]  G. Pfurtscheller Handbook of electroencephalography and clinical neurophysiology , 1978 .

[40]  F. Binkofski,et al.  The mirror neuron system and action recognition , 2004, Brain and Language.

[41]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[42]  Gert Pfurtscheller,et al.  Event-related desynchronization. Handbook of Electroencephalography and Clinical Neurophysiology. Revised Series, Volume 6 , 1999 .

[43]  Jia-Hong Gao,et al.  Is left inferior frontal gyrus a general mechanism for selection? , 2004, NeuroImage.

[44]  B. Rockstroh,et al.  Mapping EEG-potentials on the surface of the brain: A strategy for uncovering cortical sources , 2005, Brain Topography.

[45]  J. Mazziotta,et al.  Modulation of cortical activity during different imitative behaviors. , 2003, Journal of neurophysiology.

[46]  C Gerloff,et al.  Coherence of sequential movements and motor learning. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[47]  S. Cochin,et al.  Observation and execution of movement: similarities demonstrated by quantified electroencephalography , 1999, The European journal of neuroscience.

[48]  Robert Oostenveld,et al.  A comparative study of different references for EEG spectral mapping: the issue of the neutral reference and the use of the infinity reference , 2005, Physiological measurement.

[49]  B. Hjorth An on-line transformation of EEG scalp potentials into orthogonal source derivations. , 1975, Electroencephalography and clinical neurophysiology.

[50]  P. Derambure,et al.  Désynchronisation et synchronisation liées à l'événement Étude de la réactivité des rythmes électrocorticaux en relation avec la planification et l'exécution du mouvement volontaire , 1999, Neurophysiologie Clinique/Clinical Neurophysiology.

[51]  M. Makuuchi Is Broca's area crucial for imitation? , 2005, Cerebral cortex.

[52]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[53]  G. Rizzolatti,et al.  Motor facilitation during action observation: a magnetic stimulation study. , 1995, Journal of neurophysiology.

[54]  Joseph Dien,et al.  Issues in the application of the average reference: Review, critiques, and recommendations , 1998 .

[55]  J. Mazziotta,et al.  Modulation of motor and premotor activity during imitation of target-directed actions. , 2002, Cerebral cortex.

[56]  P Rappelsberger,et al.  Long-range EEG synchronization during word encoding correlates with successful memory performance. , 2000, Brain research. Cognitive brain research.

[57]  M Hallett,et al.  Event-related desynchronization (ERD) in the alpha frequency during development of implicit and explicit learning. , 1997, Electroencephalography and clinical neurophysiology.

[58]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[59]  G Pfurtscheller,et al.  Event-related beta synchronization after wrist, finger and thumb movement. , 1998, Electroencephalography and clinical neurophysiology.

[60]  U. Castiello,et al.  The Human Premotor Cortex Is 'Mirror' Only for Biological Actions , 2004, Current Biology.

[61]  H. Jasper Report of the committee on methods of clinical examination in electroencephalography , 1958 .

[62]  Paolo Manganotti,et al.  Modulation of motor cortex excitability in the left hemisphere during action observation: a single- and paired-pulse transcranial magnetic stimulation study of self- and non-self-action observation , 2003, Neuropsychologia.

[63]  Philippe Derambure,et al.  Article originalDésynchronisation et synchronisation liées à l'événement Étude de la réactivité des rythmes électrocorticaux en relation avec la planification et l'exécution du mouvement volontaireEvent-related desynchronization and synchronization. Reactivity of cortical electroencephalographic rhy , 1999 .

[64]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 1988, Experimental Brain Research.

[65]  D. Kiper,et al.  Visual stimulus-dependent changes in interhemispheric EEG coherence in humans. , 1999, Journal of neurophysiology.

[66]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.