Formation of visual memories controlled by gamma power phase-locked to alpha oscillations

Neuronal oscillations provide a window for understanding the brain dynamics that organize the flow of information from sensory to memory areas. While it has been suggested that gamma power reflects feedforward processing and alpha oscillations feedback control, it remains unknown how these oscillations dynamically interact. Magnetoencephalography (MEG) data was acquired from healthy subjects who were cued to either remember or not remember presented pictures. Our analysis revealed that in anticipation of a picture to be remembered, alpha power decreased while the cross-frequency coupling between gamma power and alpha phase increased. A measure of directionality between alpha phase and gamma power predicted individual ability to encode memory: stronger control of alpha phase over gamma power was associated with better memory. These findings demonstrate that encoding of visual information is reflected by a state determined by the interaction between alpha and gamma activity.

[1]  Marcel van Gerven,et al.  Measuring directionality between neuronal oscillations of different frequencies , 2015, NeuroImage.

[2]  Joachim Gross,et al.  Good practice for conducting and reporting MEG research , 2013, NeuroImage.

[3]  G. Nolte.  The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. , 2003, Physics in medicine and biology.

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

[5]  Adam Gazzaley,et al.  Anticipatory alpha phase influences visual working memory performance , 2014, NeuroImage.

[6]  M. Kahana,et al.  Synchronous and Asynchronous Theta and Gamma Activity during Episodic Memory Formation , 2013, The Journal of Neuroscience.

[7]  M. Kahana,et al.  Slow-Theta-to-Gamma Phase-Amplitude Coupling in Human Hippocampus Supports the Formation of New Episodic Memories. , 2016, Cerebral cortex.

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

[9]  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.

[10]  Taufik A Valiante,et al.  Phase–Amplitude Coupling and Interlaminar Synchrony Are Correlated in Human Neocortex , 2014, The Journal of Neuroscience.

[11]  A. E. Schulman,et al.  Electroencephalographic measurement of motor cortex control of muscle activity in humans , 2000, Clinical Neurophysiology.

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

[13]  H. Kennedy,et al.  Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas , 2016, Neuron.

[14]  Hyojin Park,et al.  Blocking of irrelevant memories by posterior alpha activity boosts memory encoding , 2014, Human brain mapping.

[15]  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.

[16]  S. Taulu,et al.  Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements , 2006, Physics in medicine and biology.

[17]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[18]  Ole Jensen,et al.  Gamma Activity Coupled to Alpha Phase as a Mechanism for Top-Down Controlled Gating , 2015, PloS one.

[19]  Jorge V. José,et al.  Synchronization as a mechanism for attentional gain modulation , 2004, Neurocomputing.

[20]  Paul Tiesinga,et al.  Oscillatory mechanisms of feedforward and feedback visual processing , 2015, Trends in Neurosciences.

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

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

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

[24]  J. Gotman.  Measurement of small time differences between EEG channels: method and application to epileptic seizure propagation. , 1983, Electroencephalography and clinical neurophysiology.

[25]  Nikolai Axmacher,et al.  Phase-amplitude coupling supports phase coding in human ECoG , 2015, eLife.

[26]  E. Chang,et al.  UC San Francisco UC San Francisco Previously Published Works Title Oscillatory dynamics coordinating human frontal networks in support of goal maintenance , 2015 .

[27]  Hyejin Kang,et al.  Cross-Frequency Power Correlations Reveal the Right Superior Temporal Gyrus as a Hub Region During Working Memory Maintenance , 2011, Brain Connect..

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

[29]  Adriano B. L. Tort,et al.  On cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus , 2016, eLife.

[30]  Nikolai Axmacher,et al.  Correction: Phase-amplitude coupling supports phase coding in human ECoG , 2015, eLife.

[31]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

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

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

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

[35]  Hans-Jochen Heinze,et al.  Corticothalamic phase synchrony and cross-frequency coupling predict human memory formation , 2014, eLife.

[36]  Adriano B. L. Tort,et al.  Sharp edge artifacts and spurious coupling in EEG frequency comodulation measures , 2008, Journal of Neuroscience Methods.

[37]  P. Uhlhaas,et al.  Working memory and neural oscillations: alpha–gamma versus theta–gamma codes for distinct WM information? , 2014, Trends in Cognitive Sciences.

[38]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

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

[40]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[41]  P. Roelfsema,et al.  Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex , 2014, Proceedings of the National Academy of Sciences.

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

[43]  Anne-Lise Giraud,et al.  The contribution of frequency-specific activity to hierarchical information processing in the human auditory cortex , 2014, Nature Communications.

[44]  K. Müller,et al.  Robustly estimating the flow direction of information in complex physical systems. , 2007, Physical review letters.

[45]  John J. Foxe,et al.  Propagating Neocortical Gamma Bursts Are Coordinated by Traveling Alpha Waves , 2013, The Journal of Neuroscience.

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

[47]  E. Halgren,et al.  High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research , 2012, Progress in Neurobiology.

[48]  C. Miniussi,et al.  The Functional Importance of Rhythmic Activity in the Brain , 2012, Current Biology.

[49]  Nikolai Axmacher,et al.  Good Vibrations: Cross-frequency Coupling in the Human Nucleus Accumbens during Reward Processing , 2009, Journal of Cognitive Neuroscience.

[50]  J. Fell,et al.  Rhythmic Working Memory Activation in the Human Hippocampus. , 2015, Cell reports.

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

[52]  L. Hazrati,et al.  In vitro recordings of human neocortical oscillations. , 2015, Cerebral cortex.

[53]  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.

[54]  S. Taulu,et al.  Applications of the signal space separation method , 2005, IEEE Transactions on Signal Processing.

[55]  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..

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