Decreases in theta and increases in high frequency activity underlie associative memory encoding

Episodic memory encoding refers to the cognitive process by which items and their associated contexts are stored in memory. To investigate changes directly attributed to the formation of explicit associations, we examined oscillatory power captured through intracranial electroencephalography (iEEG) as 27 neurosurgical patients receiving subdural and depth electrodes for seizure monitoring participated in a paired associates memory task. We examined low (3-8Hz) and high (45-95Hz) frequency activity, and found that the successful formation of new associations was accompanied by broad decreases in low frequency activity and a posterior to anterior progression of increases in high frequency activity in the left hemisphere. These data suggest that the observed patterns of activity may reflect the neural mechanisms underlying the formation of novel item-item associations.

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

[2]  Per B Sederberg,et al.  Power shifts track serial position and modulate encoding in human episodic memory. , 2014, Cerebral cortex.

[3]  D. C. Mccarthy,et al.  Hippocampal and neocortical gamma oscillations predict memory formation in humans. , 2006, Cerebral cortex.

[4]  J. Maunsell,et al.  Network Rhythms Influence the Relationship between Spike-Triggered Local Field Potential and Functional Connectivity , 2011, The Journal of Neuroscience.

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

[6]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[7]  W. Klimesch,et al.  Theta band power in the human scalp EEG and the encoding of new information , 1996, Neuroreport.

[8]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

[9]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[10]  Matt Stead,et al.  Network oscillations modulate interictal epileptiform spike rate during human memory. , 2013, Brain : a journal of neurology.

[11]  M. Kahana,et al.  Prestimulus theta in the human hippocampus predicts subsequent recognition but not recall , 2014, Hippocampus.

[12]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[13]  E. Fetz,et al.  Decoupling the Cortical Power Spectrum Reveals Real-Time Representation of Individual Finger Movements in Humans , 2009, The Journal of Neuroscience.

[14]  K. Paller,et al.  Observing the transformation of experience into memory , 2002, Trends in Cognitive Sciences.

[15]  Michael J Kahana,et al.  Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility? , 2015, Current Opinion in Neurobiology.

[16]  Jeremy B. Caplan,et al.  Associative isolation: Unifying associative and list memory , 2005 .

[17]  S. Hanslmayr,et al.  Theta Oscillations at Encoding Mediate the Context-Dependent Nature of Human Episodic Memory , 2013, Current Biology.

[18]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[19]  N. Logothetis,et al.  The Amplitude and Timing of the BOLD Signal Reflects the Relationship between Local Field Potential Power at Different Frequencies , 2012, The Journal of Neuroscience.

[20]  J. Poulet,et al.  Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice , 2008, Nature.

[21]  M. Kahana,et al.  Human hippocampal theta oscillations and the formation of episodic memories , 2012, Hippocampus.

[22]  Paul S. Addison,et al.  The Illustrated Wavelet Transform Handbook Introductory Theory And Applications In Science , 2002 .

[23]  Sean M. Polyn,et al.  A context maintenance and retrieval model of organizational processes in free recall. , 2009, Psychological review.

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

[25]  K. Harris,et al.  Cortical state and attention , 2011, Nature Reviews Neuroscience.

[26]  Simon Hanslmayr,et al.  How brain oscillations form memories — A processing based perspective on oscillatory subsequent memory effects , 2014, NeuroImage.

[27]  Simon Hanslmayr,et al.  The Relationship between Brain Oscillations and BOLD Signal during Memory Formation: A Combined EEG–fMRI Study , 2011, The Journal of Neuroscience.

[28]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[29]  T. Curran,et al.  Functional role of gamma and theta oscillations in episodic memory , 2010, Neuroscience & Biobehavioral Reviews.

[30]  P. Nunez,et al.  Electric fields of the brain , 1981 .

[31]  Nicole M. Long,et al.  Human intracranial high-frequency activity maps episodic memory formation in space and time , 2014, NeuroImage.

[32]  D. A. Bergstrom,et al.  Neuronal responses of the globus pallidus to systemic administration of d-amphetamine: investigation of the involvement of dopamine, norepinephrine, and serotonin , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  E. Düzel,et al.  Medial temporal theta state before an event predicts episodic encoding success in humans , 2009, Proceedings of the National Academy of Sciences.

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

[35]  T Bussey Novelty in the brain , 1999, Trends in Cognitive Sciences.

[36]  Nicole M. Long,et al.  Subsequent memory effect in intracranial and scalp EEG , 2014, NeuroImage.

[37]  Michael J. Kahana,et al.  Foundations of Human Memory , 2012 .

[38]  Michael Hornberger,et al.  Medial Temporal Lobe Contributions to Intra-Item Associative Recognition Memory in the Aging Brain , 2014, Front. Behav. Neurosci..

[39]  Marc W. Howard,et al.  A distributed representation of temporal context , 2002 .

[40]  K. Meador,et al.  Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. , 2010, Cerebral cortex.

[41]  Chantal E. Stern,et al.  Theta rhythm and the encoding and retrieval of space and time , 2014, NeuroImage.

[42]  G. Ojemann,et al.  Neurons in Human Temporal Cortex Active with Verbal Associative Learning , 1998, Brain and Language.

[43]  Michael J. Kahana,et al.  Direct brain recordings fuel advances in cognitive electrophysiology , 2010, Trends in Cognitive Sciences.

[44]  K. Bäuml,et al.  The Relationship between Brain Oscillations and BOLD Signal during Memory Formation: A Combined EEG–fMRI Study , 2011, The Journal of Neuroscience.

[45]  Jeremy B. Caplan,et al.  The roles of EEG oscillations in learning relational information , 2007, NeuroImage.

[46]  J. Poulet,et al.  Thalamic control of cortical states , 2012, Nature Neuroscience.

[47]  R. O’Reilly,et al.  Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. , 2003, Psychological review.

[48]  J. Born,et al.  EEG theta synchronization conjoined with alpha desynchronization indicate intentional encoding , 2002, The European journal of neuroscience.

[49]  J. Kingsbury The Illustrated Wavelet Transform Handbook: Introductory Theory and Applications in Science, Engineering, Medicine and Finance , 2004 .

[50]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Jeremy R. Manning,et al.  Oscillatory patterns in temporal lobe reveal context reinstatement during memory search , 2011, Proceedings of the National Academy of Sciences.

[52]  B. Staresina,et al.  Medial Temporal Theta/Alpha Power Enhancement Precedes Successful Memory Encoding: Evidence Based on Intracranial EEG , 2011, The Journal of Neuroscience.

[53]  Christopher K. Kovach,et al.  Manifestation of ocular-muscle EMG contamination in human intracranial recordings , 2011, NeuroImage.

[54]  Ellen M. Migo,et al.  Associative memory and the medial temporal lobes , 2007, Trends in Cognitive Sciences.