On the Time Course of Synchronization Patterns of Neuronal Discharges in the Human Brain during Cognitive Tasks

Using intracerebral EEG recordings in a large cohort of human subjects, we investigate the time course of neural cross-talk during a simple cognitive task. Our results show that human brain dynamics undergo a characteristic sequence of synchronization patterns across different frequency bands following a visual oddball stimulus. In particular, an initial global reorganization in the delta and theta bands (2–8 Hz) is followed by gamma (20–95 Hz) and then beta band (12–20 Hz) synchrony.

[1]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[2]  P. Jurák,et al.  The role of frontal and temporal lobes in visual discrimination task — depth ERP studies , 1999, Neurophysiologie Clinique/Clinical Neurophysiology.

[3]  A. Engel,et al.  Neuronal Synchronization along the Dorsal Visual Pathway Reflects the Focus of Spatial Attention , 2008, Neuron.

[4]  J. Talairach.  Atlas d'anatomie stéréotaxique du télencéphale : études anatomo-radiologiques , 1967 .

[5]  G. Buzsáki,et al.  Natural logarithmic relationship between brain oscillators , 2003 .

[6]  H Petsche,et al.  Synchronization between temporal and parietal cortex during multimodal object processing in man. , 1999, Cerebral cortex.

[7]  Wolf Singer,et al.  Striving for coherence , 1999 .

[8]  A. Schnitzler,et al.  Normal and pathological oscillatory communication in the brain , 2005, Nature Reviews Neuroscience.

[9]  M Kukleta,et al.  Beta 2-band synchronization during a visual oddball task. , 2009, Physiological research.

[10]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[11]  R. Eckhorn,et al.  Task-related coupling from high- to low-frequency signals among visual cortical areas in human subdural recordings. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[12]  Juan R. Vidal,et al.  Long-Distance Amplitude Correlations in the High Gamma Band Reveal Segregation and Integration within the Reading Network , 2012, The Journal of Neuroscience.

[13]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[14]  N. Barbaro,et al.  Spatiotemporal Dynamics of Word Processing in the Human Brain , 2007, Front. Neurosci..

[15]  J. Fell,et al.  Cross-frequency coupling supports multi-item working memory in the human hippocampus , 2010, Proceedings of the National Academy of Sciences.

[16]  M Kukleta,et al.  Cognitive network interactions and beta 2 coherence in processing non-target stimuli in visual oddball task. , 2009, Physiological research.

[17]  C C Wood,et al.  Intracranial recordings of endogenous ERPs in humans. , 1985, Electroencephalography and clinical neurophysiology. Supplement.

[18]  P. Fries.  A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[19]  S. Dehaene,et al.  Neural signature of the conscious processing of auditory regularities , 2009, Proceedings of the National Academy of Sciences.

[20]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[21]  Robert Oostenveld,et al.  Neural Mechanisms of Visual Attention : How Top-Down Feedback Highlights Relevant Locations , 2007 .

[22]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[23]  J. Polich.  Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[24]  S. Dehaene,et al.  Converging Intracranial Markers of Conscious Access , 2009, PLoS biology.

[25]  Eric Halgren,et al.  Generators of the human scalp P3(s) , 1986 .

[26]  P. König,et al.  Top-down processing mediated by interareal synchronization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Robert T. Knight,et al.  Five-dimensional neuroimaging: Localization of the time–frequency dynamics of cortical activity , 2008, NeuroImage.

[28]  Nikolai Axmacher,et al.  Interactions between Medial Temporal Lobe, Prefrontal Cortex, and Inferior Temporal Regions during Visual Working Memory: A Combined Intracranial EEG and Functional Magnetic Resonance Imaging Study , 2008, The Journal of Neuroscience.

[29]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[30]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[31]  E. Halgren,et al.  Generators of the late cognitive potentials in auditory and visual oddball tasks. , 1998, Electroencephalography and clinical neurophysiology.

[32]  F. Varela,et al.  A quantitative study of gamma‐band activity in human intracranial recordings triggered by visual stimuli , 2000, The European journal of neuroscience.

[33]  Ciprian M Crainiceanu,et al.  Dynamics of event‐related causality in brain electrical activity , 2008, Human brain mapping.

[34]  K. Koepsell,et al.  Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies , 2010, Proceedings of the National Academy of Sciences.

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

[36]  Edgar M. Housepian.  Atlas d'anatomie stereotaxique du telencephale. , 1968 .

[37]  K. Koepsell,et al.  Detecting event-related changes of multivariate phase coupling in dynamic brain networks. , 2012, Journal of neurophysiology.

[38]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[39]  J. Rohrbaugh,et al.  Endogenous potentials generated in the human hippocampal formation and amygdala by infrequent events. , 1980, Science.

[40]  Wolf Singer,et al.  Distributed processing and temporal codes in neuronal networks , 2009, Cognitive Neurodynamics.

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

[42]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[43]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[44]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[45]  Robert Roman,et al.  Directional functional coupling of cerebral rhythms between anterior cingulate and dorsolateral prefrontal areas during rare stimuli: A directed transfer function analysis of human depth EEG signal , 2009, Human brain mapping.

[46]  C C Wood,et al.  On the neural origin of P300 in man. , 1980, Progress in brain research.

[47]  S. Bressler.  Interareal synchronization in the visual cortex , 1996, Behavioural Brain Research.

[48]  W. Klimesch,et al.  What does phase information of oscillatory brain activity tell us about cognitive processes? , 2008, Neuroscience & Biobehavioral Reviews.

[49]  Viktor K. Jirsa,et al.  Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire , 2008, PLoS Comput. Biol..

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