Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition

In order to understand the working brain as a network, it is essential to identify the mechanisms by which information is gated between regions. We here propose that information is gated by inhibiting task-irrelevant regions, thus routing information to task-relevant regions. The functional inhibition is reflected in oscillatory activity in the alpha band (8–13 Hz). From a physiological perspective the alpha activity provides pulsed inhibition reducing the processing capabilities of a given area. Active processing in the engaged areas is reflected by neuronal synchronization in the gamma band (30–100 Hz) accompanied by an alpha band decrease. According to this framework the brain could be studied as a network by investigating cross-frequency interactions between gamma and alpha activity. Specifically the framework predicts that optimal task performance will correlate with alpha activity in task-irrelevant areas. In this review we will discuss the empirical support for this framework. Given that alpha activity is by far the strongest signal recorded by EEG and MEG, we propose that a major part of the electrophysiological activity detected from the working brain reflects gating by inhibition.

[1]  F. D. da Silva,et al.  Organization of thalamic and cortical alpha rhythms: spectra and coherences. , 1973, Electroencephalography and clinical neurophysiology.

[2]  M. Kinsbourne.  Hemi-neglect and hemisphere rivalry. , 1977, Advances in neurology.

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

[4]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[5]  A. J. Hermans,et al.  A model of the spatial-temporal characteristics of the alpha rhythm. , 1982, Bulletin of mathematical biology.

[6]  A. J. Hermans,et al.  A model of the spatial-temporal characteristics of the alpha rhythm , 1982 .

[7]  M. Kutas,et al.  Neural correlates of encoding in an incidental learning paradigm. , 1987, Electroencephalography and clinical neurophysiology.

[8]  G. Pfurtscheller.  Event-related synchronization (ERS): an electrophysiological correlate of cortical areas at rest. , 1992, Electroencephalography and clinical neurophysiology.

[9]  C. Rosenberg,et al.  Electroencephalography: Basic Principles, Clinical Applications, and Related Fields, 3rd Ed. , 1994 .

[10]  S. Bressler.  Large-scale cortical networks and cognition , 1995, Brain Research Reviews.

[11]  W. Singer,et al.  Integrator or coincidence detector? The role of the cortical neuron revisited , 1996, Trends in Neurosciences.

[12]  G. Pfurtscheller,et al.  Event-related synchronization (ERS) in the alpha band--an electrophysiological correlate of cortical idling: a review. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[13]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[14]  R. Hari,et al.  Human cortical oscillations: a neuromagnetic view through the skull , 1997, Trends in Neurosciences.

[15]  R. Vertes,et al.  Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. , 1997, Neuroscience.

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

[17]  D. Contreras,et al.  Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. , 1998, Journal of neurophysiology.

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

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

[20]  Christa Neuper,et al.  Do brain oscillations of different frequencies indicate interaction between cortical areas in humans? , 2000, Neuroscience Letters.

[21]  P. Dayan.  Fast oscillations in cortical circuits , 2000 .

[22]  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.

[23]  R. Eckhorn,et al.  Amplitude envelope correlation detects coupling among incoherent brain signals , 2000, Neuroreport.

[24]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[25]  G Pfurtscheller,et al.  Computational model of thalamo-cortical networks: dynamical control of alpha rhythms in relation to focal attention. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[27]  M. Kahana,et al.  Theta returns , 2001, Current Opinion in Neurobiology.

[28]  John J. Foxe,et al.  Attention-dependent suppression of distracter visual input can be cross-modally cued as indexed by anticipatory parieto-occipital alpha-band oscillations. , 2001, Brain research. Cognitive brain research.

[29]  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.

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

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

[32]  P Kahane,et al.  Intracranial EEG and human brain mapping , 2003, Journal of Physiology-Paris.

[33]  Andreas Kleinschmidt,et al.  EEG-correlated fMRI of human alpha activity , 2003, NeuroImage.

[34]  S. M. Daselaar,et al.  When less means more: deactivations during encoding that predict subsequent memory , 2004, NeuroImage.

[35]  One , 2004 .

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

[37]  K. Linkenkaer-Hansen,et al.  Prestimulus Oscillations Enhance Psychophysical Performance in Humans , 2004, The Journal of Neuroscience.

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

[39]  Mikko Pohja,et al.  On the human sensorimotor-cortex beta rhythm: Sources and modeling , 2005, NeuroImage.

[40]  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.

[41]  Werner Lutzenberger,et al.  Cortical Oscillatory Activity and the Dynamics of Auditory Memory Processing , 2005, Reviews in the neurosciences.

[42]  J. Lisman,et al.  Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer , 2005, Trends in Neurosciences.

[43]  J. Palva,et al.  Phase Synchrony among Neuronal Oscillations in the Human Cortex , 2005, The Journal of Neuroscience.

[44]  B. Feige,et al.  Cortical and subcortical correlates of electroencephalographic alpha rhythm modulation. , 2005, Journal of neurophysiology.

[45]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[46]  N. Crone,et al.  High-frequency gamma oscillations and human brain mapping with electrocorticography. , 2006, Progress in brain research.

[47]  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.

[48]  P. Rossini,et al.  Pre- and poststimulus alpha rhythms are related to conscious visual perception: a high-resolution EEG study. , 2005, Cerebral cortex.

[49]  Michael L. Lipton,et al.  Ipsilateral Hand Input to Area 3b Revealed by Converging Hemodynamic and Electrophysiological Analyses in Macaque Monkeys , 2006, The Journal of Neuroscience.

[50]  A. Doyle,et al.  Executive functions in attention-deficit/hyperactivity disorder. , 2006, The Journal of clinical psychiatry.

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

[52]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[53]  Simon Hanslmayr,et al.  Prestimulus oscillations predict visual perception performance between and within subjects , 2007, NeuroImage.

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

[55]  O. Jensen,et al.  Cross-frequency coupling between neuronal oscillations , 2007, Trends in Cognitive Sciences.

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

[57]  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.

[58]  J. Palva,et al.  New vistas for α-frequency band oscillations , 2007, Trends in Neurosciences.

[59]  Edward O. Mann,et al.  Role of GABAergic inhibition in hippocampal network oscillations , 2007, Trends in Neurosciences.

[60]  T. Womelsdorf,et al.  The role of neuronal synchronization in selective attention , 2007, Current Opinion in Neurobiology.

[61]  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.

[62]  J. Palva,et al.  New vistas for alpha-frequency band oscillations. , 2007, Trends in neurosciences.

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

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

[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]  Pascal Fries,et al.  Gamma-Band Activity in Human Posterior Parietal Cortex Encodes the Motor Goal during Delayed Prosaccades and Antisaccades , 2008, The Journal of Neuroscience.

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

[69]  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 .

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

[71]  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.

[72]  Erika E Fanselow,et al.  Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. , 2008, Journal of neurophysiology.

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

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

[75]  John J. Foxe,et al.  The strength of anticipatory spatial biasing predicts target discrimination at attended locations: a high‐density EEG study , 2009, The European journal of neuroscience.

[76]  Nicolas Robitaille,et al.  Oscillatory activity in parietal and dorsolateral prefrontal cortex during retention in visual short‐term memory: Additive effects of spatial attention and memory load , 2009, Human brain mapping.

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

[78]  O. Jensen,et al.  Prestimulus alpha and mu activity predicts failure to inhibit motor responses , 2009, Human brain mapping.

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

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

[81]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[82]  Stefan Haufe,et al.  Now You'll Feel It, Now You Won't: EEG Rhythms Predict the Effectiveness of Perceptual Masking , 2009, Journal of Cognitive Neuroscience.

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

[84]  R. VanRullen,et al.  The Phase of Ongoing EEG Oscillations Predicts Visual Perception , 2009, The Journal of Neuroscience.

[85]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[86]  Philippe Kahane,et al.  Task‐related gamma‐band dynamics from an intracerebral perspective: Review and implications for surface EEG and MEG , 2009, Human brain mapping.

[87]  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.

[88]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[89]  M. Corbetta,et al.  Frontoparietal Cortex Controls Spatial Attention through Modulation of Anticipatory Alpha Rhythms , 2009, The Journal of Neuroscience.

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

[91]  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.

[92]  M. V. Gerven,et al.  Attention modulations of posterior alpha as a control signal for two-dimensional brain–computer interfaces , 2009, Journal of Neuroscience Methods.

[93]  G. Mangun,et al.  Functional Disconnection of Frontal Cortex and Visual Cortex in Attention-Deficit/Hyperactivity Disorder , 2010, Biological Psychiatry.

[94]  Yan Zhang,et al.  Detection of a Weak Somatosensory Stimulus: Role of the Prestimulus Mu Rhythm and Its Top–Down Modulation , 2010, Journal of Cognitive Neuroscience.

[95]  R. Knight,et al.  Shifts in Gamma Phase–Amplitude Coupling Frequency from Theta to Alpha Over Posterior Cortex During Visual Tasks , 2010, Front. Hum. Neurosci..

[96]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[97]  T. Heskes,et al.  Covert attention allows for continuous control of brain–computer interfaces , 2010, The European journal of neuroscience.

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

[99]  J. Palva,et al.  Neuronal synchrony reveals working memory networks and predicts individual memory capacity , 2010, Proceedings of the National Academy of Sciences.

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

[101]  O. Jensen,et al.  Rhythmic Pulsing: Linking Ongoing Brain Activity with Evoked Responses , 2010, Front. Hum. Neurosci..

[102]  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.

[103]  Alfons Schnitzler,et al.  Faculty Opinions recommendation of Shaping functional architecture by oscillatory alpha activity: gating by inhibition. , 2010 .

[104]  Rajesh P. N. Rao,et al.  Cortical activity during motor execution, motor imagery, and imagery-based online feedback , 2010, Proceedings of the National Academy of Sciences.

[105]  Mingzhou Ding,et al.  From Prestimulus Alpha Oscillation to Visual-evoked Response: An Inverted-U Function and Its Attentional Modulation , 2011, Journal of Cognitive Neuroscience.

[106]  Ole Jensen,et al.  Alpha Oscillations Correlate with the Successful Inhibition of Unattended Stimuli , 2011, Journal of Cognitive Neuroscience.

[107]  O. Jensen,et al.  Increase in posterior alpha activity during rehearsal predicts successful long‐term memory formation of word sequences , 2011, Human brain mapping.