Deciphering the role of CA1 inhibitory circuits in sharp wave-ripple complexes

Sharp wave-ripples (SWRs) are population oscillatory patterns in hippocampal LFPs during deep sleep and immobility, involved in the replay of memories acquired during wakefulness. SWRs have been extensively studied, but their exact generation mechanism is still unknown. A computational model has suggested that fast perisomatic inhibition may generate the high frequency ripples (~200 Hz). Another model showed how replay of memories can be controlled by various classes of inhibitory interneurons targeting specific parts of pyramidal cells (PC) and firing at particular SWR phases. Optogenetic studies revealed new roles for interneuronal classes and rich dynamic interplays between them, shedding new light in their potential role in SWRs. Here, we integrate these findings in a conceptual model of how dendritic and somatic inhibition may collectively contribute to the SWR generation. We suggest that sharp wave excitation and basket cell (BC) recurrent inhibition synchronises BC spiking in ripple frequencies. This rhythm is imposed on bistratified cells which prevent pyramidal bursting. Axo-axonic and stratum lacunosum/moleculare interneurons are silenced by inhibitory inputs originating in the medial septum. PCs receiving rippling inhibition in both dendritic and perisomatic areas and excitation in their apical dendrites, exhibit sparse ripple phase-locked spiking.

[1]  José R. Donoso,et al.  Recruitment of oriens-lacunosum-moleculare interneurons during hippocampal ripples , 2013, Proceedings of the National Academy of Sciences.

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

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

[4]  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.

[5]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[6]  廣瀬雄一,et al.  Neuroscience , 2019, Workplace Attachments.

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

[8]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

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

[10]  G. Buzsáki,et al.  Dendritic Spikes Are Enhanced by Cooperative Network Activity in the Intact Hippocampus , 1998, The Journal of Neuroscience.

[11]  B. McNaughton,et al.  Replay of Neuronal Firing Sequences in Rat Hippocampus During Sleep Following Spatial Experience , 1996, Science.

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

[13]  David J. Foster,et al.  Reverse replay of behavioural sequences in hippocampal place cells during the awake state , 2006, Nature.

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

[15]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

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

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

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

[19]  Jozsef Csicsvari,et al.  Ivy Cells: A Population of Nitric-Oxide-Producing, Slow-Spiking GABAergic Neurons and Their Involvement in Hippocampal Network Activity , 2008, Neuron.

[20]  Frances S. Chance,et al.  Erratum: Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex , 2013, Nature Neuroscience.

[21]  K. Rockland,et al.  Rhythmically Active Enkephalin-Expressing GABAergic Cells in the CA1 Area of the Hippocampus Project to the Subiculum and Preferentially Innervate Interneurons , 2008, The Journal of Neuroscience.

[22]  Thomas Wennekers,et al.  Hippocampus, microcircuits and associative memory , 2009, Neural Networks.

[23]  D. Amaral,et al.  The three-dimensional organization of the hippocampal formation: A review of anatomical data , 1989, Neuroscience.

[24]  G. Buzsáki,et al.  Forward and reverse hippocampal place-cell sequences during ripples , 2007, Nature Neuroscience.

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

[26]  G. Buzsáki.  Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[27]  A. Losonczy,et al.  Regulation of neuronal input transformations by tunable dendritic inhibition , 2012, Nature Neuroscience.

[28]  Michael E. Hasselmo,et al.  Bio-inspired models of memory capacity, recall performance and theta phase precession in the hippocampus , 2011, The 2011 International Joint Conference on Neural Networks.

[29]  Menno P. Witter,et al.  Connectivity of the Hippocampus , 2010 .

[30]  P. Somogyi,et al.  Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons , 1995, Nature.

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

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

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

[34]  Kenji Mizuseki,et al.  Influence of slow oscillation on hippocampal activity and ripples through cortico-hippocampal synaptic interactions, analyzed by a cortical-CA3-CA1 network model , 2013, Front. Comput. Neurosci..

[35]  P. Somogyi,et al.  Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo , 2004, Nature Neuroscience.

[36]  Vassilis Cutsuridis,et al.  Encoding and retrieval in a model of the hippocampal CA1 microcircuit , 2009, Hippocampus.

[37]  Christof Koch,et al.  The Spiking Component of Oscillatory Extracellular Potentials in the Rat Hippocampus , 2012, The Journal of Neuroscience.

[38]  T. Freund,et al.  GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus , 1988, Nature.

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

[40]  P. Somogyi,et al.  Defined types of cortical interneurone structure space and spike timing in the hippocampus , 2005, The Journal of physiology.

[41]  G Buzsáki,et al.  Interactions between Hippocampus and Medial Septum during Sharp Waves and Theta Oscillation in the Behaving Rat , 1999, The Journal of Neuroscience.

[42]  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.

[43]  M. Capogna.  Neurogliaform cells and other interneurons of stratum lacunosum‐moleculare gate entorhinal–hippocampal dialogue , 2011, The Journal of physiology.