A biologically plausible mechanism for neuronal coding organized by the phase of alpha oscillations

The visual system receives a wealth of sensory information of which only little is relevant for behaviour. We present a mechanism in which alpha oscillations serve to prioritize different components of visual information. By way of simulated neuronal networks, we show that inhibitory modulation in the alpha range (~ 10 Hz) can serve to temporally segment the visual information to prevent information overload. Coupled excitatory and inhibitory neurons generate a gamma rhythm in which information is segmented and sorted according to excitability in each alpha cycle. Further details are coded by distributed neuronal firing patterns within each gamma cycle. The network model produces coupling between alpha phase and gamma (40–100 Hz) amplitude in the simulated local field potential similar to that observed experimentally in human and animal recordings.

[1]  Fiona E. N. LeBeau,et al.  Multiple origins of the cortical gamma rhythm , 2011, Developmental neurobiology.

[2]  Y. Saalmann,et al.  Cognitive and Perceptual Functions of the Visual Thalamus , 2011, Neuron.

[3]  M. R. Mehta,et al.  Role of experience and oscillations in transforming a rate code into a temporal code , 2002, Nature.

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

[5]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[6]  David Hinkley,et al.  Bootstrap Methods: Another Look at the Jackknife , 2008 .

[7]  Rufin VanRullen,et al.  On the cyclic nature of perception in vision versus audition , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[9]  G. V. Simpson,et al.  Phase Locking of Single Neuron Activity to Theta Oscillations during Working Memory in Monkey Extrastriate Visual Cortex , 2003, Neuron.

[10]  Alexandre Hyafil,et al.  Speech encoding by coupled cortical theta and gamma oscillations , 2015, eLife.

[11]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

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

[13]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[14]  R Efron,et al.  The minimum duration of a perception. , 1970, Neuropsychologia.

[15]  F. H. Lopes da Silva,et al.  Relative contributions of intracortical and thalamo-cortical processes in the generation of alpha rhythms, revealed by partial coherence analysis. , 1980, Electroencephalography and clinical neurophysiology.

[16]  William H. Press,et al.  Numerical Recipes 3rd Edition: The Art of Scientific Computing , 2007 .

[17]  J. Csicsvari,et al.  Firing rate and theta‐phase coding by hippocampal pyramidal neurons during ‘space clamping’ , 1999, The European journal of neuroscience.

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

[19]  N. Logothetis,et al.  Phase-of-Firing Coding of Natural Visual Stimuli in Primary Visual Cortex , 2008, Current Biology.

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

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

[22]  J. Dormand,et al.  A family of embedded Runge-Kutta formulae , 1980 .

[23]  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.

[24]  J. Eccles,et al.  The time courses of excitatory and inhibitory synaptic actions , 1959, The Journal of physiology.

[25]  J L Gallant,et al.  Sparse coding and decorrelation in primary visual cortex during natural vision. , 2000, Science.

[26]  Michael W. Reimann,et al.  A Biophysically Detailed Model of Neocortical Local Field Potentials Predicts the Critical Role of Active Membrane Currents , 2013, Neuron.

[27]  W. Singer,et al.  The Phase of Thalamic Alpha Activity Modulates Cortical Gamma-Band Activity: Evidence from Resting-State MEG Recordings , 2013, The Journal of Neuroscience.

[28]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[29]  S. Hughes,et al.  Synchronized Oscillations at α and θ Frequencies in the Lateral Geniculate Nucleus , 2004, Neuron.

[30]  M. Wibral,et al.  Untangling cross-frequency coupling in neuroscience , 2014, Current Opinion in Neurobiology.

[31]  Michael J. Morais,et al.  Global network influences on local functional connectivity , 2015, Nature Neuroscience.

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

[33]  J. Lisman,et al.  Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. , 1996, Learning & memory.

[34]  D. V. van Essen,et al.  Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. , 1992, Journal of neurophysiology.

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

[36]  P. Rousseeuw.  Silhouettes: a graphical aid to the interpretation and validation of cluster analysis , 1987 .

[37]  S. Hughes,et al.  Synchronized oscillations at alpha and theta frequencies in the lateral geniculate nucleus. , 2004, Neuron.

[38]  B. McNaughton,et al.  Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model , 1998, Hippocampus.

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

[40]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

[41]  John J. Foxe,et al.  The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention , 2011, Front. Psychology.

[42]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

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

[44]  Peter De Weerd,et al.  Input-Dependent Frequency Modulation of Cortical Gamma Oscillations Shapes Spatial Synchronization and Enables Phase Coding , 2015, PLoS Comput. Biol..

[45]  D. Fitzpatrick,et al.  Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex , 1997, The Journal of Neuroscience.

[46]  Anders Lansner,et al.  Computing the Local Field Potential (LFP) from Integrate-and-Fire Network Models , 2015, PLoS Comput. Biol..

[47]  G. Buzsáki.  Rhythms of the brain , 2006 .

[48]  J. Ruppersberg.  Ion Channels in Excitable Membranes , 1996 .

[49]  Leon M. Hall,et al.  Special Functions , 1998 .

[50]  D James Surmeier,et al.  Nav1.6 Sodium Channels Are Critical to Pacemaking and Fast Spiking in Globus Pallidus Neurons , 2007, The Journal of Neuroscience.

[51]  H. Eichenbaum,et al.  Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. , 2010, Journal of neurophysiology.

[52]  W. Singer,et al.  Gamma-Phase Shifting in Awake Monkey Visual Cortex , 2010, The Journal of Neuroscience.

[53]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  W. Singer,et al.  Synchrony Makes Neurons Fire in Sequence, and Stimulus Properties Determine Who Is Ahead , 2011, The Journal of Neuroscience.

[55]  Kerstin Vogler,et al.  Table Of Integrals Series And Products , 2016 .

[56]  Martin Vinck,et al.  Attentional Modulation of Cell-Class-Specific Gamma-Band Synchronization in Awake Monkey Area V4 , 2013, Neuron.

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

[58]  Rufin VanRullen,et al.  The Gamma Slideshow: Object-Based Perceptual Cycles in a Model of the Visual Cortex , 2010, Front. Hum. Neurosci..

[59]  Arne D. Ekstrom,et al.  A comparative study of human and rat hippocampal low‐frequency oscillations during spatial navigation , 2013, Hippocampus.

[60]  T. Sejnowski,et al.  Cortical Enlightenment: Are Attentional Gamma Oscillations Driven by ING or PING? , 2009, Neuron.

[61]  W. Singer,et al.  Temporal binding and the neural correlates of sensory awareness , 2001, Trends in Cognitive Sciences.

[62]  J. Csicsvari,et al.  Theta phase–specific codes for two-dimensional position, trajectory and heading in the hippocampus , 2008, Nature Neuroscience.

[63]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[64]  J. Macke,et al.  Neural population coding: combining insights from microscopic and mass signals , 2015, Trends in Cognitive Sciences.

[65]  Roshan Cools,et al.  GABAergic Modulation of Visual Gamma and Alpha Oscillations and Its Consequences for Working Memory Performance , 2014, Current Biology.

[66]  Xiao-Jing Wang.  Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[67]  J. Lisman,et al.  Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. , 2000, Journal of neurophysiology.

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

[69]  P. Welch.  The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms , 1967 .

[70]  H. Berger.  Über das Elektrenkephalogramm des Menschen , 1929, Archiv für Psychiatrie und Nervenkrankheiten.

[71]  Marc W Howard,et al.  Theta and Gamma Oscillations during Encoding Predict Subsequent Recall , 2003, The Journal of Neuroscience.

[72]  Henry Markram,et al.  Minimal Hodgkin–Huxley type models for different classes of cortical and thalamic neurons , 2008, Biological Cybernetics.

[73]  C. Schroeder,et al.  Neuronal Mechanisms and Attentional Modulation of Corticothalamic Alpha Oscillations , 2011, The Journal of Neuroscience.

[74]  John O'Keefe,et al.  Independent rate and temporal coding in hippocampal pyramidal cells , 2003, Nature.

[75]  Josef Parvizi,et al.  Resting oscillations and cross-frequency coupling in the human posteromedial cortex , 2012, NeuroImage.

[76]  Ole Jensen,et al.  Information Transfer Between Rhythmically Coupled Networks: Reading the Hippocampal Phase Code , 2001, Neural Computation.

[77]  Gaute T. Einevoll,et al.  Frequency Dependence of Signal Power and Spatial Reach of the Local Field Potential , 2013, PLoS Comput. Biol..

[78]  Marcelo A. Montemurro,et al.  Spike-Phase Coding Boosts and Stabilizes Information Carried by Spatial and Temporal Spike Patterns , 2009, Neuron.

[79]  N. Kopell,et al.  Thalamic model of awake alpha oscillations and implications for stimulus processing , 2012, Proceedings of the National Academy of Sciences.

[80]  D. Leopold,et al.  Layer-Specific Entrainment of Gamma-Band Neural Activity by the Alpha Rhythm in Monkey Visual Cortex , 2012, Current Biology.

[81]  Christof Koch,et al.  Electrical Interactions via the Extracellular Potential Near Cell Bodies , 1999, Journal of Computational Neuroscience.

[82]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[83]  Marco Idiart,et al.  A Second Function of Gamma Frequency Oscillations: An E%-Max Winner-Take-All Mechanism Selects Which Cells Fire , 2009, The Journal of Neuroscience.

[84]  Markus Siegel,et al.  Phase-dependent neuronal coding of objects in short-term memory , 2009, Proceedings of the National Academy of Sciences.

[85]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[86]  J. A. Hartigan,et al.  A k-means clustering algorithm , 1979 .

[87]  E. Hairer,et al.  Solving Ordinary Differential Equations II: Stiff and Differential-Algebraic Problems , 2010 .

[88]  J. Lisman,et al.  The Theta-Gamma Neural Code , 2013, Neuron.

[89]  L Kellényi,et al.  Depth profiles of hippocampal rhythmic slow activity ('theta rhythm') depend on behaviour. , 1985, Electroencephalography and clinical neurophysiology.

[90]  I. S. Gradshteyn,et al.  8-9 – SPECIAL FUNCTIONS , 1980 .

[91]  Adriano B. L. Tort,et al.  Theta–gamma coupling increases during the learning of item–context associations , 2009, Proceedings of the National Academy of Sciences.

[92]  I. C. Whitfield,et al.  Chapter 5 – THE NEURAL CODE , 1978 .

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

[94]  Hjalmar K Turesson,et al.  Category-selective phase coding in the superior temporal sulcus , 2012, Proceedings of the National Academy of Sciences.

[95]  Michael J. Jutras,et al.  Oscillatory activity in the monkey hippocampus during visual exploration and memory formation , 2013, Proceedings of the National Academy of Sciences.

[96]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

[97]  Alex S. Ferecskó,et al.  Model‐based analysis of excitatory lateral connections in the visual cortex , 2006, The Journal of comparative neurology.

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

[99]  Bart Gips,et al.  Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing , 2014, Trends in Neurosciences.

[100]  W. Klimesch.  Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[101]  R. Romo,et al.  α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking , 2011, Proceedings of the National Academy of Sciences.

[102]  Robert Oostenveld,et al.  Localizing human visual gamma-band activity in frequency, time and space , 2006, NeuroImage.

[103]  R. Schmidt,et al.  Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus , 2012, The Journal of Neuroscience.

[104]  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.