Rhythmic Pulsing: Linking Ongoing Brain Activity with Evoked Responses

The conventional assumption in human cognitive electrophysiology using EEG and MEG is that the presentation of a particular event such as visual or auditory stimuli evokes a “turning on” of additional brain activity that adds to the ongoing background activity. Averaging multiple event-locked trials is thought to result in the cancellation of the seemingly random phased ongoing activity while leaving the evoked response. However, recent work strongly challenges this conventional view and demonstrates that the ongoing activity is not averaged out due to specific non-sinusoidal properties. As a consquence, systematic modulations in ongoing activity can produce slow cortical evoked responses reflecting cognitive processing. In this review we introduce the concept of “rhythmic pulsing” to account for this specific non-sinusoidal property. We will explain how rhythmic pulsing can create slow evoked responses from a physiological perspective. We will also discuss how the notion of rhythmic pulsing provides a unifying framework linking ongoing oscillations, evoked responses and the brain's capacity to process incoming information.

[1]  G. H. Bishop,et al.  CYCLIC CHANGES IN EXCITABILITY OF THE OPTIC PATHWAY OF THE RABBIT , 1932 .

[2]  E. Callaway,et al.  Relationship between Reaction Time and Electroencephalographic Alpha Phase , 1960, Science.

[3]  W. Walter,et al.  Contingent Negative Variation : An Electric Sign of Sensori-Motor Association and Expectancy in the Human Brain , 1964, Nature.

[4]  F. H. Lopes da Silva,et al.  Models of neuronal populations: the basic mechanisms of rhythmicity. , 1976, Progress in brain research.

[5]  M. Kutas,et al.  Reading senseless sentences: brain potentials reflect semantic incongruity. , 1980, Science.

[6]  J. Rohrbaugh,et al.  Electrocortical signs of levels of processing: perceptual analysis and recognition memory. , 1980, Psychophysiology.

[7]  E. John,et al.  Perceptual framing and cortical alpha rhythm , 1981, Neuropsychologia.

[8]  津田 敏雄,et al.  Contingent negative variation , 1984 .

[9]  Vincenzo Crunelli,et al.  A role for GABAB receptors in excitation and inhibition of thalamocortical cells , 1991, Trends in Neurosciences.

[10]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[11]  G. Pfurtscheller,et al.  Event-related desynchronization (ERD) and the Dm effect: does alpha desynchronization during encoding predict later recall performance? , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[12]  V. Jousmäki,et al.  Modulation of Human Cortical Rolandic Rhythms during Natural Sensorimotor Tasks , 1997, NeuroImage.

[13]  Riitta Salmelin,et al.  Evidence for reactive magnetic 10-Hz rhythm in the human auditory cortex , 1997, Neuroscience Letters.

[14]  W. Klimesch,et al.  'Paradoxical' alpha synchronization in a memory task. , 1999, Brain research. Cognitive brain research.

[15]  Cornelis J. Stam,et al.  Investigation of the dynamics underlying periodic complexes in the EEG , 1999, Biological Cybernetics.

[16]  W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[17]  Y. Okada,et al.  Roles of a potassium afterhyperpolarization current in generating neuromagnetic fields and field potentials in longitudinal CA3 slices of the guinea-pig , 1999, Clinical Neurophysiology.

[18]  R. Knight,et al.  Neural origins of the P300. , 2000, Critical reviews in neurobiology.

[19]  G. V. Simpson,et al.  Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex , 2000, The Journal of Neuroscience.

[20]  Colin M. Brown,et al.  ERP effects of listening to speech compared to reading: the P600/SPS to syntactic violations in spoken sentences and rapid serial visual presentation , 2000, Neuropsychologia.

[21]  E. Basar,et al.  Gamma, alpha, delta, and theta oscillations govern cognitive processes. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[22]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

[23]  J. Lisman,et al.  Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. , 2002, Cerebral cortex.

[24]  Mark S. Cohen,et al.  Simultaneous EEG and fMRI of the alpha rhythm , 2002, Neuroreport.

[25]  C. Koch,et al.  Is perception discrete or continuous? , 2003, Trends in Cognitive Sciences.

[26]  Gregor Thut,et al.  Differential effects of low-frequency rTMS at the occipital pole on visual-induced alpha desynchronization and visual-evoked potentials , 2003, NeuroImage.

[27]  Maro G. Machizawa,et al.  Neural activity predicts individual differences in visual working memory capacity , 2004, Nature.

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

[29]  Ankoor S. Shah,et al.  Neural dynamics and the fundamental mechanisms of event-related brain potentials. , 2004, Cerebral cortex.

[30]  T. Sejnowski,et al.  Electroencephalographic Brain Dynamics Following Manually Responded Visual Targets , 2004, PLoS biology.

[31]  Nancy Kopell,et al.  Alpha-Frequency Rhythms Desynchronize over Long Cortical Distances: A Modeling Study , 2000, Journal of Computational Neuroscience.

[32]  Thomas Grunwald,et al.  Neural Bases of Cognitive ERPs: More than Phase Reset , 2004, Journal of Cognitive Neuroscience.

[33]  Manuel Schabus,et al.  Phase-locked alpha and theta oscillations generate the P1-N1 complex and are related to memory performance. , 2004, Brain research. Cognitive brain research.

[34]  Maro G. Machizawa,et al.  Neural measures reveal individual differences in controlling access to working memory , 2005, Nature.

[35]  S. Hughes,et al.  Thalamic Mechanisms of EEG Alpha Rhythms and Their Pathological Implications , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[36]  Hannu Tiitinen,et al.  Auditory event-related responses are generated independently of ongoing brain activity , 2005, NeuroImage.

[37]  W. Klimesch,et al.  Alpha phase synchronization predicts P1 and N1 latency and amplitude size. , 2005, Cerebral cortex.

[38]  W. Klimesch,et al.  Relevance of EEG alpha and theta oscillations during task switching , 2006, Experimental Brain Research.

[39]  Catherine Tallon-Baudry,et al.  The many faces of the gamma band response to complex visual stimuli , 2005, NeuroImage.

[40]  T. Picton,et al.  EEG spectral dynamics during discrimination of auditory and visual targets. , 2005, Brain research. Cognitive brain research.

[41]  R. Oostenveld,et al.  Successful declarative memory formation is associated with ongoing activity during encoding in a distributed neocortical network related to working memory: A magnetoencephalography study , 2006, Neuroscience.

[42]  P. Hagoort,et al.  Oscillatory neuronal dynamics during language comprehension. , 2006, Progress in brain research.

[43]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[44]  Natasha M. Maurits,et al.  Correlating the alpha rhythm to BOLD using simultaneous EEG/fMRI: Inter-subject variability , 2006, NeuroImage.

[45]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[46]  John J. Foxe,et al.  Increases in alpha oscillatory power reflect an active retinotopic mechanism for distracter suppression during sustained visuospatial attention. , 2006, Journal of neurophysiology.

[47]  Y. Okada,et al.  Contributions of principal neocortical neurons to magnetoencephalography and electroencephalography signals , 2006, The Journal of physiology.

[48]  Helmut Laufs,et al.  Where the BOLD signal goes when alpha EEG leaves , 2006, NeuroImage.

[49]  O. Jensen,et al.  Posterior α activity is not phase-reset by visual stimuli , 2006 .

[50]  Steven Lemm,et al.  A novel mechanism for evoked responses in the human brain , 2007, The European journal of neuroscience.

[51]  D. Davidson,et al.  An inverse relation between event-related and time–frequency violation responses in sentence processing , 2007, Brain Research.

[52]  W. Singer,et al.  The gamma cycle , 2007, Trends in Neurosciences.

[53]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[54]  O. Jensen,et al.  Modulation of Gamma and Alpha Activity during a Working Memory Task Engaging the Dorsal or Ventral Stream , 2007, The Journal of Neuroscience.

[55]  Simon Hanslmayr,et al.  The best of both worlds: phase-reset of human EEG alpha activity and additive power contribute to ERP generation. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[56]  G. Thut,et al.  Mechanisms of selective inhibition in visual spatial attention are indexed by α‐band EEG synchronization , 2007, The European journal of neuroscience.

[57]  J. Schoffelen,et al.  Oscillatory activity in human parietal and occipital cortex shows hemispheric lateralization and memory effects in a delayed double-step saccade task. , 2007, Cerebral cortex.

[58]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[59]  M. Rugg,et al.  Event-related potentials and recognition memory , 2007, Trends in Cognitive Sciences.

[60]  J. Schoffelen,et al.  Parieto‐occipital sources account for the increase in alpha activity with working memory load , 2007, Human brain mapping.

[61]  C. Schroeder,et al.  Neuronal Oscillations and Multisensory Interaction in Primary Auditory Cortex , 2007, Neuron.

[62]  W. Klimesch,et al.  Event-related phase reorganization may explain evoked neural dynamics , 2007, Neuroscience & Biobehavioral Reviews.

[63]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[64]  Arno Villringer,et al.  Influence of ongoing alpha rhythm on the visual evoked potential , 2008, NeuroImage.

[65]  J. Schoffelen,et al.  Prestimulus Oscillatory Activity in the Alpha Band Predicts Visual Discrimination Ability , 2008, The Journal of Neuroscience.

[66]  I. Toni,et al.  Oscillations , 2018, Physics to a Degree.

[67]  Yan Zhang,et al.  Prestimulus Cortical Activity is Correlated with Speed of Visuomotor Processing , 2008, Journal of Cognitive Neuroscience.

[68]  Gregor Thut,et al.  Resting electroencephalogram alpha-power over posterior sites indexes baseline visual cortex excitability , 2008, Neuroreport.

[69]  O. Jensen,et al.  Asymmetric Amplitude Modulations of Brain Oscillations Generate Slow Evoked Responses , 2008, The Journal of Neuroscience.

[70]  Vincenzo Crunelli,et al.  Cellular Dynamics of Cholinergically Induced α (8–13 Hz) Rhythms in Sensory Thalamic Nuclei In Vitro , 2008, The Journal of Neuroscience.

[71]  Á. Pascual-Leone,et al.  Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. , 2008, Cerebral cortex.

[72]  O. Jensen,et al.  Gamma Power Is Phase-Locked to Posterior Alpha Activity , 2008, PloS one.

[73]  Timothy J. Gawne,et al.  The Visual Evoked Potential Is Independent of Surface Alpha Rhythm Phase the Visual Evoked Potential Is Independent of Surface Alpha Rhythm Phase , 2022 .

[74]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[75]  C. Miniussi,et al.  Combining TMS and EEG Offers New Prospects in Cognitive Neuroscience , 2009, Brain Topography.

[76]  Diane M. Beck,et al.  To See or Not to See: Prestimulus α Phase Predicts Visual Awareness , 2009, The Journal of Neuroscience.

[77]  S. Hughes,et al.  Temporal Framing of Thalamic Relay-Mode Firing by Phasic Inhibition during the Alpha Rhythm , 2009, Neuron.

[78]  C. Miniussi,et al.  New insights into rhythmic brain activity from TMS–EEG studies , 2009, Trends in Cognitive Sciences.

[79]  A. Villringer,et al.  Rolandic alpha and beta EEG rhythms' strengths are inversely related to fMRI‐BOLD signal in primary somatosensory and motor cortex , 2009, Human brain mapping.

[80]  Robert Oostenveld,et al.  Trial-by-trial coupling between EEG and BOLD identifies networks related to alpha and theta EEG power increases during working memory maintenance , 2009, NeuroImage.

[81]  Wolfgang Klimesch,et al.  The functional relevance of phase reset A comment to Risner et al. (2009): The visual evoked potential of surface alpha rhythm phase , 2009, NeuroImage.

[82]  Petra Ritter,et al.  Detecting alpha rhythm phase reset by phase sorting: Caveats to consider , 2009, NeuroImage.

[83]  A. Karim,et al.  Brain Oscillatory Substrates of Visual Short-Term Memory Capacity , 2009, Current Biology.

[84]  W. Medendorp,et al.  Modulations in oscillatory activity with amplitude asymmetry can produce cognitively relevant event-related responses , 2009, Proceedings of the National Academy of Sciences.

[85]  Antoine J. Shahin,et al.  Brain oscillations during semantic evaluation of speech , 2009, Brain and Cognition.

[86]  Sebastiaan Overeem,et al.  Corticospinal Beta-Band Synchronization Entails Rhythmic Gain Modulation , 2010, The Journal of Neuroscience.

[87]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[88]  Antoine J. Shahin,et al.  Attentional Gain Control of Ongoing Cortical Speech Representations in a “Cocktail Party” , 2010, The Journal of Neuroscience.

[89]  R. VanRullen,et al.  The phase of ongoing EEG oscillations predicts visual perception , 2010 .

[90]  Amplitude asymmetry as a mechanism for the generation of slow evoked responses , 2010, Clinical Neurophysiology.

[91]  O. Jensen,et al.  Left temporal alpha band activity increases during working memory retention of pitches , 2010, The European journal of neuroscience.

[92]  Curio Gabriel Non-zero mean and asymmetry of neuronal oscillations have different implications for evoked responses , 2010 .

[93]  E. Vogel,et al.  Discrete capacity limits in visual working memory , 2010, Current Opinion in Neurobiology.

[94]  R. Oostenveld,et al.  Somatosensory working memory performance in humans depends on both engagement and disengagement of regions in a distributed network , 2009, Human brain mapping.

[95]  Bin He,et al.  Negative covariation between task-related responses in alpha/beta-band activity and BOLD in human sensorimotor cortex: An EEG and fMRI study of motor imagery and movements , 2010, NeuroImage.

[96]  Risto J. Ilmoniemi,et al.  EEG oscillations and magnetically evoked motor potentials reflect motor system excitability in overlapping neuronal populations , 2010, Clinical Neurophysiology.