Layer-Specific GABAergic Control of Distinct Gamma Oscillations in the CA1 Hippocampus

The temporary interaction of distinct gamma oscillators effects binding, association, and information routing. How independent gamma oscillations are generated and maintained by pyramidal cells and interneurons within a cortical circuit remains unknown. We recorded the spike timing of identified parvalbumin-expressing basket cells in the CA1 hippocampus of anesthetized rats and simultaneously detected layer-specific gamma oscillations using current-source-density analysis. Spike timing of basket cells tuned the phase and amplitude of gamma oscillations generated around stratum pyramidale, where basket cells selectively innervate pyramidal cells with GABAergic synapses. Basket cells did not contribute to gamma oscillations generated at the apical tuft of pyramidal cells. This gamma oscillation was selectively modulated by a subset of local GABAergic interneurons and by medial entorhinal cortex layer 3 neurons. The generation of independent and layer-specific gamma oscillations, implemented onto hippocampal pyramidal cells along their somato-dendritic axis, can be explained by selective axonal targeting and precisely controlled temporal firing of GABAergic interneurons.

[1]  G. Buzsáki,et al.  Intrinsic Circuit Organization and Theta–Gamma Oscillation Dynamics in the Entorhinal Cortex of the Rat , 2010, The Journal of Neuroscience.

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

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

[4]  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.

[5]  Fabian Kloosterman,et al.  Recording and marking with silicon multichannel electrodes. , 2002, Brain research. Brain research protocols.

[6]  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.

[7]  D. Pinault,et al.  A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin , 1996, Journal of Neuroscience Methods.

[8]  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.

[9]  Thomas Klausberger,et al.  Distinct Dendritic Arborization and In Vivo Firing Patterns of Parvalbumin-Expressing Basket Cells in the Hippocampal Area CA3 , 2013, The Journal of Neuroscience.

[10]  U. Eysel,et al.  Functional and Structural Topography of Horizontal Inhibitory Connections in Cat Visual Cortex , 1993, The European journal of neuroscience.

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

[12]  G. Buzsáki,et al.  Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells , 1995, Hippocampus.

[13]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  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.

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

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

[17]  Brendon O. Watson,et al.  Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease. , 2012, Dialogues in clinical neuroscience.

[18]  J. Lisman,et al.  The θ-γ neural code. , 2013, Neuron.

[19]  Adriano B L Tort,et al.  Theta phase modulates multiple layer-specific oscillations in the CA1 region. , 2012, Cerebral cortex.

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

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

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

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

[24]  Iris Oren,et al.  Feedforward Inhibition Underlies the Propagation of Cholinergically Induced Gamma Oscillations from Hippocampal CA3 to CA1 , 2013, The Journal of Neuroscience.

[25]  R. Schmidt,et al.  Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus , 2012, The Journal of Neuroscience.

[26]  Edward O. Mann,et al.  Perisomatic Feedback Inhibition Underlies Cholinergically Induced Fast Network Oscillations in the Rat Hippocampus In Vitro , 2005, Neuron.

[27]  Dimitri M. Kullmann,et al.  Oscillations and Filtering Networks Support Flexible Routing of Information , 2010, Neuron.

[28]  G. Buzsáki,et al.  Gamma Oscillations in the Entorhinal Cortex of the Freely Behaving Rat , 1998, The Journal of Neuroscience.

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

[30]  T. Freund,et al.  Differences between Somatic and Dendritic Inhibition in the Hippocampus , 1996, Neuron.

[31]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

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

[33]  J. Csicsvari,et al.  Massively parallel recording of unit and local field potentials with silicon-based electrodes. , 2003, Journal of neurophysiology.

[34]  J E Lisman,et al.  Storage of 7 +/- 2 short-term memories in oscillatory subcycles , 1995, Science.

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

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

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

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

[39]  Menno P. Witter,et al.  Entorhinal projections to the hippocampal CA1 region in the rat: An underestimated pathway , 1988, Neuroscience Letters.

[40]  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.

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

[42]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[43]  Hannah Monyer,et al.  NMDA Receptor Ablation on Parvalbumin-Positive Interneurons Impairs Hippocampal Synchrony, Spatial Representations, and Working Memory , 2010, Neuron.

[44]  Ivan Cohen,et al.  Unitary inhibitory field potentials in the CA3 region of rat hippocampus , 2010, The Journal of physiology.

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

[46]  C. Schroeder,et al.  How Local Is the Local Field Potential? , 2011, Neuron.

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

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

[49]  M. Deschenes,et al.  Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. , 1993, Journal of neurophysiology.

[50]  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.

[51]  Oscar Herreras,et al.  Schaffer-Specific Local Field Potentials Reflect Discrete Excitatory Events at Gamma Frequency That May Fire Postsynaptic Hippocampal CA1 Units , 2012, The Journal of Neuroscience.

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

[53]  R. Anwyl,et al.  Stimulation on the Positive Phase of Hippocampal Theta Rhythm Induces Long-Term Potentiation That Can Be Depotentiated by Stimulation on the Negative Phase in Area CA1 In Vivo , 1997, The Journal of Neuroscience.

[54]  E. Moser,et al.  Gamma oscillations in the hippocampus. , 2010, Physiology.

[55]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[56]  Peter Somogyi,et al.  Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis , 2009, Nature Neuroscience.

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

[58]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[59]  István Ulbert,et al.  Supplementary material to : Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus , 2010 .

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

[61]  J. Lisman,et al.  The Theta-Gamma Neural Code , 2013, Neuron.

[62]  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.

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

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

[65]  N. Burgess,et al.  Evidence for Encoding versus Retrieval Scheduling in the Hippocampus by Theta Phase and Acetylcholine , 2013, The Journal of Neuroscience.

[66]  R. Llinás,et al.  The Entorhinal Cortex Entrains Fast CA1 Hippocampal Oscillations in the Anaesthetized Guinea‐pig: Role of the Monosynaptic Component of the Perforant Path , 1995, The European journal of neuroscience.

[67]  T. Freund,et al.  Total Number and Ratio of Excitatory and Inhibitory Synapses Converging onto Single Interneurons of Different Types in the CA1 Area of the Rat Hippocampus , 1999, The Journal of Neuroscience.

[68]  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.

[69]  C. Stumpf THE FAST COMPONENT IN THE ELECTRICAL ACTIVITY OF RABBIT'S HIPPOCAMPUS. , 1965, Electroencephalography and clinical neurophysiology.

[70]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[71]  O. Paulsen,et al.  Identification of the current generator underlying cholinergically induced gamma frequency field potential oscillations in the hippocampal CA3 region , 2010, The Journal of physiology.

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

[73]  Thomas Klausberger,et al.  Terminal Field and Firing Selectivity of Cholecystokinin-Expressing Interneurons in the Hippocampal CA3 Area , 2011, The Journal of Neuroscience.