Sub-second dynamics of theta-gamma coupling in hippocampal CA1

Oscillatory brain activity reflects different internal brain states including neurons’ excitatory state and synchrony among neurons. However, characterizing these states is complicated by the fact that different oscillations are often coupled, such as gamma oscillations nested in theta in the hippocampus, and changes in coupling are thought to reflect distinct states. Here, we describe a new method to separate single oscillatory cycles into distinct states based on frequency and phase coupling. Using this method, we identified four theta-gamma coupling states in rat hippocampal CA1. These states differed in abundance across behaviors, phase synchrony with other hippocampal subregions, and neural coding properties suggesting that these states are functionally distinct. We captured cycle-to-cycle changes in oscillatory coupling states and found frequent switching between theta-gamma states showing that the hippocampus rapidly shifts between different functional states. This method provides a new approach to investigate oscillatory brain dynamics broadly.

[1]  Benjamin J. Kraus,et al.  Hippocampal “Time Cells”: Time versus Path Integration , 2013, Neuron.

[2]  L. Colgin Oscillations and hippocampal–prefrontal synchrony , 2011, Current Opinion in Neurobiology.

[3]  Albert K. Lee,et al.  Memory of Sequential Experience in the Hippocampus during Slow Wave Sleep , 2002, Neuron.

[4]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[5]  L. Colgin Rhythms of the hippocampal network , 2016, Nature Reviews Neuroscience.

[6]  Santiago Canals,et al.  Frequency-Dependent Gating of Hippocampal-Neocortical Interactions. , 2016, Cerebral cortex.

[7]  E. Rolls Pattern separation, completion, and categorisation in the hippocampus and neocortex , 2016, Neurobiology of Learning and Memory.

[8]  Martin Vinck,et al.  Improved measures of phase-coupling between spikes and the Local Field Potential , 2011, Journal of Computational Neuroscience.

[9]  L. Colgin,et al.  Slow and Fast Gamma Rhythms Coordinate Different Spatial Coding Modes in Hippocampal Place Cells , 2014, Neuron.

[10]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[11]  G. Batchelor,et al.  An Introduction to Fluid Dynamics , 1968 .

[12]  Richard Kempter,et al.  Quantifying circular–linear associations: Hippocampal phase precession , 2012, Journal of Neuroscience Methods.

[13]  G. Buzsáki,et al.  REM Sleep Reorganizes Hippocampal Excitability , 2012, Neuron.

[14]  Anat Sakov,et al.  The dynamics of spatial behavior: how can robust smoothing techniques help? , 2004, Journal of Neuroscience Methods.

[15]  P. Somogyi,et al.  Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations , 2008, Science.

[16]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[17]  B. McNaughton,et al.  Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences , 1996, Hippocampus.

[18]  Richard Kempter,et al.  Single-Trial Phase Precession in the Hippocampus , 2009, The Journal of Neuroscience.

[19]  L. Colgin,et al.  Spatial Sequence Coding Differs during Slow and Fast Gamma Rhythms in the Hippocampus , 2016, Neuron.

[20]  R. Morris,et al.  Memory consolidation. , 2015, Cold Spring Harbor perspectives in biology.

[21]  G. Buzsáki,et al.  Temporal Encoding of Place Sequences by Hippocampal Cell Assemblies , 2006, Neuron.

[22]  Kenneth D Harris,et al.  Theta-Mediated Dynamics of Spatial Information in Hippocampus , 2008, The Journal of Neuroscience.

[23]  Ehren L. Newman,et al.  Cholinergic Blockade Reduces Theta-Gamma Phase Amplitude Coupling and Speed Modulation of Theta Frequency Consistent with Behavioral Effects on Encoding , 2013, The Journal of Neuroscience.

[24]  Matthew A. Wilson,et al.  Hippocampal Replay of Extended Experience , 2009, Neuron.

[25]  G. K. Batchelor,et al.  An Introduction to Fluid Dynamics: Contents , 2000 .

[26]  G. Dragoi,et al.  Preplay of future place cell sequences by hippocampal cellular assemblies , 2011, Nature.

[27]  György Buzsáki,et al.  Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance , 2007, Proceedings of the National Academy of Sciences.

[28]  Jozsef Csicsvari,et al.  Homeostatic maintenance of neuronal excitability by burst discharges in vivo. , 2002, Cerebral cortex.

[29]  Caleb Kemere,et al.  Rapid and Continuous Modulation of Hippocampal Network State during Exploration of New Places , 2013, PloS one.

[30]  G. Buzsáki,et al.  Theta Oscillations Provide Temporal Windows for Local Circuit Computation in the Entorhinal-Hippocampal Loop , 2009, Neuron.

[31]  Martin Vinck,et al.  Oscillatory Dynamics and Place Field Maps Reflect Hippocampal Ensemble Processing of Sequence and Place Memory under NMDA Receptor Control , 2014, Neuron.

[32]  P. Fries,et al.  Robust Gamma Coherence between Macaque V1 and V2 by Dynamic Frequency Matching , 2013, Neuron.

[33]  Susumu Tonegawa,et al.  Direct Medial Entorhinal Cortex Input to Hippocampal CA1 Is Crucial for Extended Quiet Awake Replay , 2017, Neuron.

[34]  G. Buzsáki,et al.  Hippocampal Network Dynamics Constrain the Time Lag between Pyramidal Cells across Modified Environments , 2008, The Journal of Neuroscience.

[35]  G. Tononi,et al.  Sleep and synaptic homeostasis: a hypothesis , 2003, Brain Research Bulletin.

[36]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[37]  Viktor Jirsa,et al.  Functional architectures and structured flows on manifolds: a dynamical framework for motor behavior. , 2014, Psychological review.

[38]  H. Eichenbaum Time cells in the hippocampus: a new dimension for mapping memories , 2014, Nature Reviews Neuroscience.

[39]  Christof Koch,et al.  Theta Phase Segregation of Input-Specific Gamma Patterns in Entorhinal-Hippocampal Networks , 2014, Neuron.

[40]  Roxana A. Stefanescu,et al.  Recognition memory and theta–gamma interactions in the hippocampus , 2014, Hippocampus.

[41]  Davide Ciliberti,et al.  Real-time classification of experience-related ensemble spiking patterns for closed-loop applications , 2018, eLife.

[42]  M. Wilson,et al.  Uncovering representations of sleep-associated hippocampal ensemble spike activity , 2016, Scientific Reports.

[43]  Pascal Fries,et al.  Gamma Synchronization between V1 and V4 Improves Behavioral Performance , 2018, Neuron.

[44]  André A Fenton,et al.  Control of recollection by slow gamma dominating mid-frequency gamma in hippocampus CA1 , 2017, bioRxiv.

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

[46]  Sean M Montgomery,et al.  Theta and Gamma Coordination of Hippocampal Networks during Waking and Rapid Eye Movement Sleep , 2008, The Journal of Neuroscience.

[47]  Jessica A. Cardin,et al.  Snapshots of the Brain in Action: Local Circuit Operations through the Lens of γ Oscillations , 2016, The Journal of Neuroscience.

[48]  S. Daan,et al.  The two‐process model of sleep regulation: a reappraisal , 2016, Journal of sleep research.

[49]  M. Pinsk,et al.  A Dynamic Interplay within the Frontoparietal Network Underlies Rhythmic Spatial Attention , 2018, Neuron.

[50]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[51]  Matthijs A. A. van der Meer,et al.  Hippocampal Replay Is Not a Simple Function of Experience , 2010, Neuron.

[52]  Dheeraj S. Roy,et al.  Ventral CA1 neurons store social memory , 2016, Science.

[53]  S. P. Lloyd,et al.  Least squares quantization in PCM , 1982, IEEE Trans. Inf. Theory.

[54]  G. Buzsáki,et al.  Entorhinal-CA3 Dual-Input Control of Spike Timing in the Hippocampus by Theta-Gamma Coupling , 2017, Neuron.

[55]  B. McNaughton,et al.  Self-Motion and the Hippocampal Spatial Metric , 2005, The Journal of Neuroscience.

[56]  Bruno Poucet,et al.  Goal-Related Activity in Hippocampal Place Cells , 2007, The Journal of Neuroscience.

[57]  G. Buzsáki,et al.  Interaction between neocortical and hippocampal networks via slow oscillations. , 2005, Thalamus & related systems.

[58]  Chen Sun,et al.  Distinct Neural Circuits for the Formation and Retrieval of Episodic Memories , 2017, Cell.

[59]  Roddy M. Grieves,et al.  The Yin and Yang of Memory Consolidation: Hippocampal and Neocortical , 2017, PLoS biology.

[60]  L. Colgin,et al.  Theta–gamma Coupling in the Entorhinal–hippocampal System This Review Comes from a Themed Issue on Brain Rhythms and Dynamic Coordination Sciencedirect , 2022 .

[61]  T. Bliss,et al.  The Hippocampus Book , 2006 .

[62]  Uri T Eden,et al.  Rapid classification of hippocampal replay content for real-time applications. , 2016, Journal of neurophysiology.

[63]  Edmund T. Rolls,et al.  Spatial representations in the primate hippocampus, and their functions in memory and navigation , 2018, Progress in Neurobiology.

[64]  G. Buzsáki,et al.  Hippocampal CA1 pyramidal cells form functionally distinct sublayers , 2011, Nature Neuroscience.

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

[66]  P. Fuller,et al.  The Biology of REM Sleep , 2017, Current Biology.

[67]  Andres D. Grosmark,et al.  Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences , 2016, Science.

[68]  Daniel Levenstein,et al.  Network Homeostasis and State Dynamics of Neocortical Sleep , 2016, Neuron.

[69]  E. Rolls,et al.  Object, space, and object-space representations in the primate hippocampus. , 2005, Journal of neurophysiology.

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

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

[72]  J. Born,et al.  About sleep's role in memory. , 2013, Physiological reviews.

[73]  Makoto Tamura,et al.  Hippocampal-prefrontal theta-gamma coupling during performance of a spatial working memory task , 2017, Nature Communications.

[74]  J. Born,et al.  The memory function of sleep , 2010, Nature Reviews Neuroscience.

[75]  J. O’Keefe,et al.  Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells , 2005, Hippocampus.

[76]  Margaret F. Carr,et al.  Transient Slow Gamma Synchrony Underlies Hippocampal Memory Replay , 2012, Neuron.

[77]  Viktor K. Jirsa,et al.  Cross-frequency coupling in real and virtual brain networks , 2013, Front. Comput. Neurosci..

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

[79]  A. Redish,et al.  Hippocampal Theta-Gamma Coupling Reflects State-Dependent Information Processing in Decision Making , 2018, Cell reports.

[80]  G. Buzsáki,et al.  A 4 Hz Oscillation Adaptively Synchronizes Prefrontal, VTA, and Hippocampal Activities , 2011, Neuron.

[81]  Thomas Klausberger,et al.  Layer-Specific GABAergic Control of Distinct Gamma Oscillations in the CA1 Hippocampus , 2014, Neuron.

[82]  E A Leicht,et al.  Community structure in directed networks. , 2007, Physical review letters.

[83]  Mattias P. Karlsson,et al.  Awake replay of remote experiences in the hippocampus , 2009, Nature Neuroscience.

[84]  Asohan Amarasingham,et al.  Internally Generated Cell Assembly Sequences in the Rat Hippocampus , 2008, Science.

[85]  A. Borbély A two process model of sleep regulation. , 1982, Human neurobiology.

[86]  Howard Eichenbaum,et al.  A cognitive map for object memory in the hippocampus. , 2009, Learning & memory.

[87]  J. A. Scott Kelso,et al.  Brain coordination dynamics: True and false faces of phase synchrony and metastability , 2009, Progress in Neurobiology.

[88]  Thomas Klausberger,et al.  Temporal redistribution of inhibition over neuronal subcellular domains underlies state-dependent rhythmic change of excitability in the hippocampus , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[89]  Andreas Draguhn,et al.  Impaired theta-gamma coupling in APP-deficient mice , 2016, Scientific Reports.

[90]  Fraser T. Sparks,et al.  Control of recollection by slow gamma dominating mid-frequency gamma in hippocampus CA1 , 2017, bioRxiv.

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

[92]  György Buzsáki,et al.  Space and time in the brain , 2017, Science.

[93]  V. Sohal How Close Are We to Understanding What (if Anything) γ Oscillations Do in Cortical Circuits? , 2016, The Journal of Neuroscience.

[94]  A. D. Grosmark,et al.  Recordings from hippocampal area CA1, PRE, during and POST novel spatial learning. , 2016 .

[95]  Bryan C. Souza,et al.  Theta-associated high-frequency oscillations (110–160Hz) in the hippocampus and neocortex , 2013, Progress in Neurobiology.

[96]  M. Wilson,et al.  Temporally Structured Replay of Awake Hippocampal Ensemble Activity during Rapid Eye Movement Sleep , 2001, Neuron.

[97]  J. Born,et al.  In search of a role of REM sleep in memory formation , 2015, Neurobiology of Learning and Memory.

[98]  A. Redish,et al.  Theta phase shift in spike timing and modulation of gamma oscillation: a dynamic code for spatial alternation during fixation in rat hippocampal area CA1. , 2014, Journal of neurophysiology.

[99]  Adriano B. L. Tort,et al.  Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task , 2008, Proceedings of the National Academy of Sciences.

[100]  B. McNaughton,et al.  Spatial representation in the hippocampal formation: a history , 2017, Nature Neuroscience.

[101]  E. Moser,et al.  Faculty Opinions recommendation of Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. , 2009 .

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

[103]  Michael E. Hasselmo,et al.  A Proposed Function for Hippocampal Theta Rhythm: Separate Phases of Encoding and Retrieval Enhance Reversal of Prior Learning , 2002, Neural Computation.

[104]  Omar J. Ahmed,et al.  Running Speed Alters the Frequency of Hippocampal Gamma Oscillations , 2012, The Journal of Neuroscience.

[105]  Emilio Kropff,et al.  Place cells, grid cells, and the brain's spatial representation system. , 2008, Annual review of neuroscience.

[106]  Michel Le Van Quyen,et al.  Analysis of dynamic brain oscillations: methodological advances , 2007, Trends in Neurosciences.

[107]  Thomas Klausberger,et al.  Hippocampal Place Cells Couple to Three Different Gamma Oscillations during Place Field Traversal , 2016, Neuron.

[108]  G. Buzsáki,et al.  Hippocampal network patterns of activity in the mouse , 2003, Neuroscience.

[109]  Antoine Adamantidis,et al.  Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation , 2016, Science.

[110]  N. Logothetis,et al.  Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms , 2013, Neuron.

[111]  Alexander J Morley,et al.  Parsing Hippocampal Theta Oscillations by Nested Spectral Components during Spatial Exploration and Memory-Guided Behavior , 2018, Neuron.

[112]  GyÖrgy BuzsÁk Memory consolidation during sleep: a neurophysiological perspective , 1998 .

[113]  M. Moser,et al.  A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation , 2015, Nature.

[114]  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.

[115]  Jean-Loup Guillaume,et al.  Fast unfolding of communities in large networks , 2008, 0803.0476.

[116]  Laura Lee Colgin,et al.  Do slow and fast gamma rhythms correspond to distinct functional states in the hippocampal network? , 2015, Brain Research.

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

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

[119]  Edvard I Moser,et al.  Development of the Spatial Representation System in the Rat , 2010, Science.

[120]  Anoopum S. Gupta,et al.  Segmentation of spatial experience by hippocampal theta sequences , 2012, Nature Neuroscience.

[121]  Alexei L. Vyssotski,et al.  Selective Coupling between Theta Phase and Neocortical Fast Gamma Oscillations during REM-Sleep in Mice , 2011, PloS one.

[122]  Savita Gupta,et al.  Image Recognition using Coefficient of Correlation and Structural SIMilarity Index in Uncontrolled Environment , 2012 .

[123]  Sean M Montgomery,et al.  Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm , 2008, Neuron.

[124]  G. Tononi,et al.  Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration , 2014, Neuron.

[125]  P. Fries Rhythms for Cognition: Communication through Coherence , 2015, Neuron.

[126]  G. Buzsáki,et al.  Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells , 2002, Nature.

[127]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[128]  Li Lu,et al.  Coordination of entorhinal–hippocampal ensemble activity during associative learning , 2014, Nature.

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

[130]  Sean M Montgomery,et al.  Relationships between Hippocampal Sharp Waves, Ripples, and Fast Gamma Oscillation: Influence of Dentate and Entorhinal Cortical Activity , 2011, The Journal of Neuroscience.

[131]  G. Buzsáki Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory , 2005, Hippocampus.

[132]  Takashi Kitamura,et al.  Engrams and circuits crucial for systems consolidation of a memory , 2017, Science.