Hippocampal CA1 Ripples as Inhibitory Transients

Memories are stored and consolidated as a result of a dialogue between the hippocampus and cortex during sleep. Neurons active during behavior reactivate in both structures during sleep, in conjunction with characteristic brain oscillations that may form the neural substrate of memory consolidation. In the hippocampus, replay occurs within sharp wave-ripples: short bouts of high-frequency activity in area CA1 caused by excitatory activation from area CA3. In this work, we develop a computational model of ripple generation, motivated by in vivo rat data showing that ripples have a broad frequency distribution, exponential inter-arrival times and yet highly non-variable durations. Our study predicts that ripples are not persistent oscillations but result from a transient network behavior, induced by input from CA3, in which the high frequency synchronous firing of perisomatic interneurons does not depend on the time scale of synaptic inhibition. We found that noise-induced loss of synchrony among CA1 interneurons dynamically constrains individual ripple duration. Our study proposes a novel mechanism of hippocampal ripple generation consistent with a broad range of experimental data, and highlights the role of noise in regulating the duration of input-driven oscillatory spiking in an inhibitory network.

[1]  P. Golshani,et al.  Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice , 2012, Proceedings of the National Academy of Sciences.

[2]  G. Buzsáki,et al.  tFast Network Oscillations in the Hippocampal CA1 Region of the Behaving Rat , 1999, The Journal of Neuroscience.

[3]  Michaël Zugaro,et al.  Hippocampal ripples and memory consolidation , 2011, Current Opinion in Neurobiology.

[4]  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.

[5]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

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

[7]  Dennis A. Turner,et al.  Interneurons of the Dentate–Hilus Border of the Rat Dentate Gyrus: Morphological and Electrophysiological Heterogeneity , 1997, The Journal of Neuroscience.

[8]  Nancy Kopell,et al.  Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network. , 2005, Journal of neurophysiology.

[9]  B Sakmann,et al.  Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  J. Born,et al.  Effects of early and late nocturnal sleep on priming and spatial memory. , 1999, Psychophysiology.

[11]  G. Buzsáki,et al.  High-frequency network oscillation in the hippocampus. , 1992, Science.

[12]  J. Born,et al.  Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. , 2001, Learning & memory.

[13]  G. Buzsáki Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning , 2015, Hippocampus.

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

[15]  Ole Paulsen,et al.  Priming of Hippocampal Population Bursts by Individual Perisomatic-Targeting Interneurons , 2010, The Journal of Neuroscience.

[16]  T. Sejnowski,et al.  Model of Thalamocortical Slow-Wave Sleep Oscillations and Transitions to Activated States , 2002, The Journal of Neuroscience.

[17]  R. Stickgold,et al.  Sleep, memory, and plasticity. , 2006, Annual review of psychology.

[18]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[19]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[20]  Michael Lagler,et al.  Behavior-dependent specialization of identified hippocampal interneurons , 2012, Nature Neuroscience.

[21]  Roger D. Traub,et al.  A Model of High-Frequency Ripples in the Hippocampus Based on Synaptic Coupling Plus Axon–Axon Gap Junctions between Pyramidal Neurons , 2000, The Journal of Neuroscience.

[22]  J. Csicsvari,et al.  Replay and Time Compression of Recurring Spike Sequences in the Hippocampus , 1999, The Journal of Neuroscience.

[23]  Michael E. Hasselmo,et al.  Spatial Memory Sequence Encoding and Replay During Modeled Theta and Ripple Oscillations , 2011, Cognitive Computation.

[24]  U. Heinemann,et al.  Effects of the GABAA receptor antagonists bicuculline and gabazine on stimulus‐induced sharp wave‐ripple complexes in adult rat hippocampus in vitro , 2007 .

[25]  Carol M. Petito The Synaptic Organization of the Brain, 4th Ed , 1998 .

[26]  Stephen Coombes,et al.  Modeling sharp wave‐ripple complexes through a CA3‐CA1 network model with chemical synapses , 2012, Hippocampus.

[27]  Adriano B. L. Tort,et al.  On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus , 2007, Proceedings of the National Academy of Sciences.

[28]  Ivan Soltesz,et al.  Quantitative assessment of CA1 local circuits: Knowledge base for interneuron‐pyramidal cell connectivity , 2013, Hippocampus.

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

[30]  U. Heinemann,et al.  Effects of the GABA(A) receptor antagonists bicuculline and gabazine on stimulus-induced sharp wave-ripple complexes in adult rat hippocampus in vitro. , 2007, The European journal of neuroscience.

[31]  Peter Somogyi,et al.  Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro , 2000, The Journal of physiology.

[32]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[33]  Wulfram Gerstner,et al.  Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. , 2005, Journal of neurophysiology.

[34]  Martin Fuhrmann,et al.  Long-Term In Vivo Imaging of Dendritic Spines in the Hippocampus Reveals Structural Plasticity , 2014, The Journal of Neuroscience.

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

[36]  A. Destexhe,et al.  Stochastic Methods in Neuroscience , 2012 .

[37]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[38]  R. Traub,et al.  Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro , 1998, Nature.

[39]  Horacio G Rotstein,et al.  Orthogonal arrangement of rhythm-generating microcircuits in the hippocampus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[40]  G. Buzsáki,et al.  Pyramidal Cell-Interneuron Interactions Underlie Hippocampal Ripple Oscillations , 2014, Neuron.

[41]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[42]  P. Bressloff,et al.  Entorhinal Stellate Cells Show Preferred Spike Phase-Locking to Theta Inputs That Is Enhanced by Correlations in Synaptic Activity , 2013, The Journal of Neuroscience.

[43]  R. Traub,et al.  High-frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axoaxonal gap junctions , 1999, Neuroscience.

[44]  Bruce P. Graham,et al.  Comprar Hippocampal Microcircuits · A Computational Modeler's Resource Book | Cutsuridis, Vassilis | 9781441909954 | Springer , 2010 .

[45]  G. Buzsáki,et al.  Preconfigured, skewed distribution of firing rates in the hippocampus and entorhinal cortex. , 2013, Cell reports.

[46]  N. Kopell,et al.  Phase resetting reduces theta–gamma rhythmic interaction to a one-dimensional map , 2013, Journal of mathematical biology.

[47]  Monika Schönauer,et al.  Exploring the effect of sleep and reduced interference on different forms of declarative memory. , 2014, Sleep.

[48]  M. Frotscher,et al.  Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Eran Stark,et al.  Excitation and Inhibition Compete to Control Spiking during Hippocampal Ripples: Intracellular Study in Behaving Mice , 2014, The Journal of Neuroscience.

[50]  J. Csicsvari,et al.  Ensemble Patterns of Hippocampal CA3-CA1 Neurons during Sharp Wave–Associated Population Events , 2000, Neuron.

[51]  Bruce P. Graham,et al.  Hippocampal Microcircuits: A Computational Modeler's Resource Book , 2010, Springer Series in Computational Neuroscience.

[52]  G. Buzsáki,et al.  Local Generation and Propagation of Ripples along the Septotemporal Axis of the Hippocampus , 2013, The Journal of Neuroscience.

[53]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[54]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[55]  Nicolas Brunel,et al.  Sparsely synchronized neuronal oscillations. , 2008, Chaos.

[56]  Paul W. Frankland,et al.  Neurons Are Recruited to a Memory Trace Based on Relative Neuronal Excitability Immediately before Training , 2014, Neuron.

[57]  Adriano B. L. Tort,et al.  OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons , 2012, Nature Neuroscience.

[58]  B. McNaughton,et al.  Hippocampal sharp wave bursts coincide with neocortical "up-state" transitions. , 2004, Learning & memory.

[59]  R. Traub,et al.  Inhibition-based rhythms: experimental and mathematical observations on network dynamics. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[60]  Paul W Frankland,et al.  Dorsal hippocampal CREB is both necessary and sufficient for spatial memory. , 2010, Learning & memory.

[61]  A. Posłuszny,et al.  The contribution of electrical synapses to field potential oscillations in the hippocampal formation , 2014, Front. Neural Circuits.

[62]  R. Kempter,et al.  Coherent Phasic Excitation during Hippocampal Ripples , 2011, Neuron.

[63]  Szabolcs Káli,et al.  Mechanisms of Sharp Wave Initiation and Ripple Generation , 2014, The Journal of Neuroscience.

[64]  P. Somogyi,et al.  Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo , 2003, Nature.

[65]  Kenneth D Harris,et al.  Selective Impairment of Hippocampal Gamma Oscillations in Connexin-36 Knock-Out Mouse In Vivo , 2003, The Journal of Neuroscience.

[66]  Susumu Tonegawa,et al.  Hippocampal CA3 Output Is Crucial for Ripple-Associated Reactivation and Consolidation of Memory , 2009, Neuron.

[67]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[68]  Carson C. Chow,et al.  Frequency Control in Synchronized Networks of Inhibitory Neurons , 1998, Journal of Computational Neuroscience.

[69]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[70]  Oscar Herreras,et al.  Sustained increase of spontaneous input and spike transfer in the CA3-CA1 pathway following long-term potentiation in vivo , 2012, Front. Neural Circuits.

[71]  J. Hobson,et al.  Visual discrimination learning requires sleep after training , 2000, Nature Neuroscience.

[72]  E. Izhikevich,et al.  Weakly connected neural networks , 1997 .

[73]  M. Khamassi,et al.  Replay of rule-learning related neural patterns in the prefrontal cortex during sleep , 2009, Nature Neuroscience.

[74]  Raoul-Martin Memmesheimer,et al.  Quantitative prediction of intermittent high-frequency oscillations in neural networks with supralinear dendritic interactions , 2010, Proceedings of the National Academy of Sciences.

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

[76]  Vassilis Cutsuridis,et al.  Deciphering the role of CA1 inhibitory circuits in sharp wave-ripple complexes , 2013, Front. Syst. Neurosci..

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

[78]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  Wulfram Gerstner,et al.  Firing patterns in the adaptive exponential integrate-and-fire model , 2008, Biological Cybernetics.

[80]  J. Born,et al.  Sleep forms memory for finger skills , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[81]  Jonathan Touboul,et al.  Dynamics and bifurcations of the adaptive exponential integrate-and-fire model , 2008, Biological Cybernetics.

[82]  Denise J. Cai,et al.  Synaptic tagging during memory allocation , 2014, Nature Reviews Neuroscience.