Non-linear EEG synchronization during observation and execution of simple and complex sequential finger movements

The main aim of this study was to examine the temporal aspects of neuronal changes during the observation and execution of simple and complex tasks to gain a greater understanding of the mirror neuron system’s involvement in complex motor tasks. Eleven right-handed subjects observed simple and complex finger movement sequences. Electroencephalograms were recorded from 19 electrodes. Activity was considered in four frequency bands (8–10, 10–13, 13–20, and 20–30 Hz) using a new measure, synchronization likelihood. The results show that motor tasks of different levels of complexity did not have a significant influence on cortical synchronization. The results also provide additional indirect evidence for mirror neuron activity associated with intransitive tasks. Data are discussed in the light of recent findings from the cognitive and behavioral neuroscience literature.

[1]  G. Rizzolatti,et al.  Understanding motor events: a neurophysiological study , 2004, Experimental Brain Research.

[2]  J. Binder,et al.  Functional magnetic resonance imaging of complex human movements , 1993, Neurology.

[3]  M. Ding,et al.  Task-related power and coherence changes in neuromagnetic activity during visuomotor coordination , 2002, Experimental Brain Research.

[4]  W. Klimesch Memory processes, brain oscillations and EEG synchronization. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[5]  M. Hallett,et al.  Involvement of the ipsilateral motor cortex in finger movements of different complexities , 1997, Annals of neurology.

[6]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

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

[8]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

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

[10]  Alexa M. Morcom,et al.  Does the brain have a baseline? Why we should be resisting a rest , 2007, NeuroImage.

[11]  Vilayanur S. Ramachandran,et al.  EEG evidence for mirror neuron activity during the observation of human and robot actions: Toward an analysis of the human qualities of interactive robots , 2007, Neurocomputing.

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

[13]  A. Schnitzler,et al.  Do simple intransitive finger movements consistently activate frontoparietal mirror neuron areas in humans? , 2007, NeuroImage.

[14]  S. Cochin,et al.  Perception of motion and qEEG activity in human adults. , 1998, Electroencephalography and clinical neurophysiology.

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

[16]  Erol Başar,et al.  Beta oscillations in face recognition. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[17]  Luciano Fadiga,et al.  The mirror system in humans , 2002 .

[18]  Wolfgang Klimesch Event-related band power changes and memory performance , 1999 .

[19]  S. Small,et al.  Lateralization of motor circuits and handedness during finger movements , 2001, European journal of neurology.

[20]  Werner Lutzenberger,et al.  Motor programming in both hemispheres: an EEG study of the human brain , 1995, Neuroscience Letters.

[21]  M. Hallett,et al.  Frequency-Dependent Changes of Regional Cerebral Blood Flow during Finger Movements , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

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

[23]  M. Hallett,et al.  The functional neuroanatomy of simple and complex sequential finger movements: a PET study. , 1998, Brain : a journal of neurology.

[24]  Kurt Wiesenfeld,et al.  Neural correlates of the complexity of rhythmic finger tapping , 2003, NeuroImage.

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

[26]  J. Pineda The functional significance of mu rhythms: Translating “seeing” and “hearing” into “doing” , 2005, Brain Research Reviews.

[27]  A. Labarga,et al.  Alpha and beta oscillatory activity during a sequence of two movements , 2004, Clinical Neurophysiology.

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

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

[30]  N. Thakor,et al.  Spectral analysis methods for neurological signals , 1998, Journal of Neuroscience Methods.

[31]  R. Magill Motor learning and control : concepts and applications , 2004 .

[32]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[34]  W. Shebilske,et al.  Motor Learning and Control , 1993 .

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

[36]  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.

[37]  Istvan Molnar-Szakacs,et al.  Observing complex action sequences: The role of the fronto-parietal mirror neuron system , 2006, NeuroImage.

[38]  Karl J. Friston The labile brain. I. Neuronal transients and nonlinear coupling. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

[40]  Seong-Gi Kim,et al.  Effects of movement predictability on cortical motor activation , 1998, Neuroscience Research.

[41]  H. Semlitsch,et al.  A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. , 1986, Psychophysiology.

[42]  H. Théoret,et al.  EEG evidence for the presence of an action observation–execution matching system in children , 2006, The European journal of neuroscience.

[43]  F. Pulvermüller,et al.  The Concept of Transcortical Cell Assemblies: a Key to the Understanding of Cortical Lateralization and Interhemispheric Interaction , 1996, Neuroscience & Biobehavioral Reviews.

[44]  Perrine Ruby,et al.  A relation between rest and the self in the brain? , 2003, Brain Research Reviews.

[45]  M. Hallett,et al.  Complexity affects regional cerebral blood flow change during sequential finger movements , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[47]  Milan Palus,et al.  Nonlinearity in normal human EEG: cycles, temporal asymmetry, nonstationarity and randomness, not chaos , 1996, Biological Cybernetics.

[48]  R. Passingham Attention to action. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  H Shibasaki,et al.  Enhanced negative slope of cortical potentials before sequential as compared with simultaneous extensions of two fingers. , 1993, Electroencephalography and clinical neurophysiology.

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

[51]  M. Hallett,et al.  How self-initiated memorized movements become automatic: a functional MRI study. , 2004, Journal of neurophysiology.

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

[53]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

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

[55]  Michael Vourkas,et al.  Changes in Linear and Nonlinear EEG Measures as a Function of Task Complexity: Evidence for Local and Distant Signal Synchronization , 2004, Brain Topography.

[56]  R. E Passingham,et al.  Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study , 2003, NeuroImage.

[57]  A. Pérez-Villalba Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[58]  H. Berendse,et al.  Generalized Synchronization of MEG Recordings in Alzheimer’s Disease: Evidence for Involvement of the Gamma Band , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[59]  A. E. Schulman,et al.  Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. , 1998, Brain : a journal of neurology.

[60]  Cornelis J. Stam,et al.  Neural networks involved in mathematical thinking: evidence from linear and non-linear analysis of electroencephalographic activity , 2005, Neuroscience Letters.

[61]  Christian Gerloff,et al.  Ipsilateral cortical activation during finger sequences of increasing complexity: representation of movement difficulty or memory load? , 2003, Clinical Neurophysiology.

[62]  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.

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

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

[65]  H. Gastaut,et al.  EEG changes during cinematographic presentation; moving picture activation of the EEG. , 1954, Electroencephalography and clinical neurophysiology.

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

[67]  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.

[68]  C. Stam,et al.  Variability of EEG synchronization during a working memory task in healthy subjects. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[69]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

[70]  J. Pineda,et al.  Recognition of point-light biological motion: Mu rhythms and mirror neuron activity , 2007, Behavioural Brain Research.

[71]  Shanbao Tong,et al.  Advances in quantitative electroencephalogram analysis methods. , 2004, Annual review of biomedical engineering.

[72]  Gabriel Curio,et al.  Tonic neuronal activation during simple and complex finger movements analyzed by DC-magnetoencephalography , 2006, Neuroscience Letters.

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

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

[75]  Vittorio Gallese,et al.  Mirror Neurons and the Evolution of Brain and Language , 2002 .

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

[77]  Cornelis J. Stam,et al.  Synchronization likelihood with explicit time-frequency priors , 2006, NeuroImage.

[78]  Michela Romani,et al.  Motor facilitation during action observation: topographic mapping of the target muscle and influence of the onlooker's posture , 2006, The European journal of neuroscience.

[79]  F. L. D. Silva,et al.  Dynamics of the human alpha rhythm: evidence for non-linearity? , 1999, Clinical Neurophysiology.