Fast Gamma Oscillations Are Generated Intrinsically in CA1 without the Involvement of Fast-Spiking Basket Cells

Information processing in neuronal networks relies on the precise synchronization of ensembles of neurons, coordinated by the diverse family of inhibitory interneurons. Cortical interneurons can be usefully parsed by embryonic origin, with the vast majority arising from either the caudal or medial ganglionic eminences (CGE and MGE). Here, we examine the activity of hippocampal interneurons during gamma oscillations in mouse CA1, using an in vitro model where brief epochs of rhythmic activity were evoked by local application of kainate. We found that this CA1 KA-evoked gamma oscillation was faster than that in CA3 and, crucially, did not appear to require the involvement of fast-spiking basket cells. In contrast to CA3, we also found that optogenetic inhibition of pyramidal cells in CA1 did not significantly affect the power of the oscillation, suggesting that excitation may not be essential for gamma genesis in this region. We found that MGE-derived interneurons were generally more active than CGE interneurons during CA1 gamma, although a group of CGE-derived interneurons, putative trilaminar cells, were strongly phase-locked with gamma oscillations and, together with MGE-derived axo-axonic and bistratified cells, provide attractive candidates for being the driver of this locally generated, predominantly interneuron-driven model of gamma oscillations.

[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]  J. Lisman Working Memory: The Importance of Theta and Gamma Oscillations , 2010, Current Biology.

[3]  E. Southam,et al.  A comparison of possible markers for chandelier cartridges in rat medial prefrontal cortex and hippocampus , 2005, Brain Research.

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

[5]  Jesse Jackson,et al.  Fast and Slow Gamma Rhythms Are Intrinsically and Independently Generated in the Subiculum , 2011, The Journal of Neuroscience.

[6]  R. Traub,et al.  Distinct Roles for the Kainate Receptor Subunits GluR5 and GluR6 in Kainate-Induced Hippocampal Gamma Oscillations , 2004, The Journal of Neuroscience.

[7]  Allan R. Jones,et al.  A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing , 2012, Nature Neuroscience.

[8]  Fiona E. N. LeBeau,et al.  Beta rhythms (15-20 Hz) generated by nonreciprocal communication in hippocampus. , 2007, Journal of neurophysiology.

[9]  P. Sprent,et al.  Statistical Analysis of Circular Data. , 1994 .

[10]  M. Whittington,et al.  Segregation of Axonal and Somatic Activity During Fast Network Oscillations , 2012, Science.

[11]  U. Heinemann,et al.  First and second generation antipsychotics influence hippocampal gamma oscillations by interactions with 5‐HT3 and D3 receptors , 2012, British journal of pharmacology.

[12]  J. O’Neill,et al.  Gamma Oscillatory Firing Reveals Distinct Populations of Pyramidal Cells in the CA1 Region of the Hippocampus , 2008, The Journal of Neuroscience.

[13]  G. Buzsáki,et al.  Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. , 1996, The Journal of physiology.

[14]  Pablo Fuentealba,et al.  Cell Type-Specific Tuning of Hippocampal Interneuron Firing during Gamma Oscillations In Vivo , 2007, The Journal of Neuroscience.

[15]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

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

[17]  A. Fisahn,et al.  5‐Hydroxytryptamine1A receptor‐activation hyperpolarizes pyramidal cells and suppresses hippocampal gamma oscillations via Kir3 channel activation , 2014, The Journal of physiology.

[18]  Nicholas I. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[19]  G. Buzsáki,et al.  Hippocampal CA1 interneurons: an in vivo intracellular labeling study , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[21]  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.

[22]  Norbert Hájos,et al.  Network mechanisms of gamma oscillations in the CA3 region of the hippocampus , 2009, Neural Networks.

[23]  C. McBain,et al.  Dual embryonic origins of functionally distinct hippocampal O-LM cells revealed by differential 5-HT3AR expression , 2013, Nature Neuroscience.

[24]  Chris J. McBain,et al.  Interneurons unbound , 2001, Nature Reviews Neuroscience.

[25]  Babak Tahvildari,et al.  Selective Functional Interactions between Excitatory and Inhibitory Cortical Neurons and Differential Contribution to Persistent Activity of the Slow Oscillation , 2012, The Journal of Neuroscience.

[26]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[27]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

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

[29]  P. Somogyi,et al.  Metabotropic Glutamate Receptor 8-Expressing Nerve Terminals Target Subsets of GABAergic Neurons in the Hippocampus , 2005, The Journal of Neuroscience.

[30]  Luis Puelles,et al.  Cortical Excitatory Neurons and Glia, But Not GABAergic Neurons, Are Produced in the Emx1-Expressing Lineage , 2002, The Journal of Neuroscience.

[31]  M. Vreugdenhil,et al.  Transition between fast and slow gamma modes in rat hippocampus area CA1 in vitro is modulated by slow CA3 gamma oscillations , 2014, The Journal of physiology.

[32]  Jozsi Z. Jalics,et al.  NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex , 2008, Proceedings of the National Academy of Sciences.

[33]  Chris J. McBain,et al.  A Blueprint for the Spatiotemporal Origins of Mouse Hippocampal Interneuron Diversity , 2011, The Journal of Neuroscience.

[34]  N. Ropert,et al.  Serotonin facilitates GABAergic transmission in the CA1 region of rat hippocampus in vitro. , 1991, The Journal of physiology.

[35]  Fiona E. N. LeBeau,et al.  GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Hannah Monyer,et al.  Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro , 2005, The Journal of physiology.

[37]  G. Fishell,et al.  The Largest Group of Superficial Neocortical GABAergic Interneurons Expresses Ionotropic Serotonin Receptors , 2010, The Journal of Neuroscience.

[38]  I. Módy,et al.  Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons , 2009, Nature Neuroscience.

[39]  T. Freund,et al.  GABAergic Interneurons are the Major Postsynaptic Targets of Median Raphe Afferents in the Rat Dentate Gyrus , 1992, The European journal of neuroscience.

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

[41]  J. Csicsvari,et al.  Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat , 2003, Neuron.

[42]  Ole Paulsen,et al.  Hippocampal gamma‐frequency oscillations: from interneurones to pyramidal cells, and back , 2005, The Journal of physiology.

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

[44]  O. Paulsen,et al.  Spike Timing of Distinct Types of GABAergic Interneuron during Hippocampal Gamma Oscillations In Vitro , 2004, The Journal of Neuroscience.

[45]  E. Callaway,et al.  Previously Published Works Uc Irvine Title: Cell-type-specific Circuit Connectivity of Hippocampal Ca1 Revealed through Cre-dependent Rabies Tracing Cell-type Specific Circuit Connectivity of Hippocampal Ca1 Revealed through Cre-dependent Rabies Tracing Nih Public Access Author Manuscript , 2022 .

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

[47]  P. Somogyi,et al.  Neuronal Diversity in GABAergic Long-Range Projections from the Hippocampus , 2007, The Journal of Neuroscience.

[48]  C. McBain,et al.  Developmental origin dictates interneuron AMPA and NMDA receptor subunit composition and plasticity , 2013, Nature Neuroscience.