NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex

doi:10.1073/PNAS.0809302105

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NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex

Journal Article•DOI•

NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex

Steven J. Middleton¹, Jozsi Jalics, Tilman J. Kispersky, Fiona E. N. LeBeau, Anita K. Roopun, Nancy Kopell, Miles A. Whittington, Mark O. Cunningham - Show less +4 more•Institutions (1)

Newcastle University¹

25 Nov 2008-Proceedings of the National Academy of Sciences of the United States of America (National Academy of Sciences)-Vol. 105, Iss: 47, pp 18572-18577

TL;DR: The two different gamma frequencies matched the different intrinsic frequencies in hippocampal areas CA3 and CA1, suggesting that NMDA receptor activation may control the nature of temporal interactions between mEC and hippocampus, thus influencing the pathway for information transfer between the two regions.

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Abstract: Local circuits in the medial entorhinal cortex (mEC) and hippocampus generate gamma frequency population rhythms independently. Temporal interaction between these areas at gamma frequencies is implicated in memory—a phenomenon linked to activity of NMDA-subtype glutamate receptors. While blockade of NMDA receptors does not affect frequency of gamma rhythms in hippocampus, it exposes a second, lower frequency (25–35 Hz) gamma rhythm in mEC. In experiment and model, NMDA receptor-dependent mEC gamma rhythms were mediated by basket interneurons, but NMDA receptor-independent gamma rhythms were mediated by a novel interneuron subtype—the goblet cell. This cell was distinct from basket cells in morphology, intrinsic membrane properties and synaptic inputs. The two different gamma frequencies matched the different intrinsic frequencies in hippocampal areas CA3 and CA1, suggesting that NMDA receptor activation may control the nature of temporal interactions between mEC and hippocampus, thus influencing the pathway for information transfer between the two regions.

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Journal Article•DOI•

Driving fast-spiking cells induces gamma rhythm and controls sensory responses

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Jessica A. Cardin¹, Marie Carlén², Marie Carlén³, Konstantinos Meletis², Konstantinos Meletis³, Ulf Knoblich¹, Feng Zhang⁴, Karl Deisseroth⁴, Li-Huei Tsai³, Li-Huei Tsai², Li-Huei Tsai⁵, Christopher I. Moore¹ - Show less +8 more•Institutions (5)

McGovern Institute for Brain Research¹, Massachusetts Institute of Technology², Picower Institute for Learning and Memory³, Stanford University⁴, Howard Hughes Medical Institute⁵

04 Jun 2009-Nature

TL;DR: The timing of a sensory input relative to a gamma cycle determined the amplitude and precision of evoked responses and provided the first causal evidence that distinct network activity states can be induced in vivo by cell-type-specific activation.

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Abstract: Corticalgammaoscillations(20280Hz)predictincreasesinfocusedattention,andfailureingammaregulationisahallmark of neurological and psychiatric disease. Current theory predicts that gamma oscillations are generated by synchronous activity of fast-spiking inhibitory interneurons, with the resulting rhythmic inhibition producing neural ensemble synchrony by generating a narrow window for effective excitation. We causally tested these hypotheses in barrel cortex in vivo by targeting optogenetic manipulation selectively to fast-spiking interneurons. Here we show that light-driven activation of fast-spiking interneurons atvariedfrequencies (82200Hz) selectivelyamplifies gamma oscillations. Incontrast, pyramidal neuron activation amplifies only lower frequency oscillations, a cell-type-specific double dissociation. We found that the timing of a sensory input relative to a gamma cycle determined the amplitude and precision of evoked responses. Our data directly support the fast-spiking-gamma hypothesis and provide the first causal evidence that distinct network activity states can be induced in vivo by cell-type-specific activation.

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2,453 citations

Journal Article•DOI•

Neurophysiological and Computational Principles of Cortical Rhythms in Cognition

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Xiao Jing Wang¹•Institutions (1)

Yale University¹

01 Jul 2010-Physiological Reviews

TL;DR: A plethora of studies will be reviewed on the involvement of long-distance neuronal coherence in cognitive functions such as multisensory integration, working memory, and selective attention, and implications of abnormal neural synchronization are discussed as they relate to mental disorders like schizophrenia and autism.

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Abstract: Synchronous rhythms represent a core mechanism for sculpting temporal coordination of neural activity in the brain-wide network. This review focuses on oscillations in the cerebral cortex that occur during cognition, in alert behaving conditions. Over the last two decades, experimental and modeling work has made great strides in elucidating the detailed cellular and circuit basis of these rhythms, particularly gamma and theta rhythms. The underlying physiological mechanisms are diverse (ranging from resonance and pacemaker properties of single cells to multiple scenarios for population synchronization and wave propagation), but also exhibit unifying principles. A major conceptual advance was the realization that synaptic inhibition plays a fundamental role in rhythmogenesis, either in an interneuronal network or in a reciprocal excitatory-inhibitory loop. Computational functions of synchronous oscillations in cognition are still a matter of debate among systems neuroscientists, in part because the notion of regular oscillation seems to contradict the common observation that spiking discharges of individual neurons in the cortex are highly stochastic and far from being clocklike. However, recent findings have led to a framework that goes beyond the conventional theory of coupled oscillators and reconciles the apparent dichotomy between irregular single neuron activity and field potential oscillations. From this perspective, a plethora of studies will be reviewed on the involvement of long-distance neuronal coherence in cognitive functions such as multisensory integration, working memory, and selective attention. Finally, implications of abnormal neural synchronization are discussed as they relate to mental disorders like schizophrenia and autism.

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1,774 citations

Cites background from "NMDA receptor-dependent switching b..."

...The slower frequency may be determined by a mixture of cellular and synaptic properties, including voltage- and calcium-gated potassium currents in pyramidal cells and the strength of recurrent excitatory connections (817, 1052, 1054), perhaps also involving specific subtypes of interneurons (667, 682, 758)....
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Journal Article•DOI•

Hippocampal GABAergic Inhibitory Interneurons.

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Kenneth A. Pelkey¹, Ramesh Chittajallu², Michael T. Craig³, Ludovic Tricoire², Ludovic Tricoire¹, Jason C. Wester², Jason C. Wester¹, Chris J. McBain¹, Chris J. McBain² - Show less +5 more•Institutions (3)

National Institutes of Health¹, University of Exeter², University of Paris³

01 Oct 2017-Physiological Reviews

TL;DR: An overview of the current state of the field of interneuron research, focusing largely on the hippocampus, discusses recent advances related to the various cell types, including their development and maturation, expression of subtype-specific voltage- and ligand-gated channels, and their roles in network oscillations.

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Abstract: In the hippocampus GABAergic local circuit inhibitory interneurons represent only ~10–15% of the total neuronal population; however, their remarkable anatomical and physiological diversity allows them to regulate virtually all aspects of cellular and circuit function. Here we provide an overview of the current state of the field of interneuron research, focusing largely on the hippocampus. We discuss recent advances related to the various cell types, including their development and maturation, expression of subtype-specific voltage- and ligand-gated channels, and their roles in network oscillations. We also discuss recent technological advances and approaches that have permitted high-resolution, subtype-specific examination of their roles in numerous neural circuit disorders and the emerging therapeutic strategies to ameliorate such pathophysiological conditions. The ultimate goal of this review is not only to provide a touchstone for the current state of the field, but to help pave the way for future research by highlighting where gaps in our knowledge exist and how a complete appreciation of their roles will aid in future therapeutic strategies.

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545 citations

Journal Article•DOI•

Beyond the connectome: the dynome.

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Nancy Kopell¹, Howard J. Gritton¹, Miles A. Whittington², Mark A. Kramer¹•Institutions (2)

Boston University¹, Hull York Medical School²

17 Sep 2014-Neuron

TL;DR: A framework for studying the brain's "dynome" and its relationship to cognition is described, which links brain connectivity with brain dynamics, as well as the biological details that relate this connectivity more directly to function.

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301 citations

Cites background from "NMDA receptor-dependent switching b..."

...…in different cortical layers (Oke et al., 2010; Ainsworth et al., 2012), different effects of neuromodulators on rhythms in different brain areas (Middleton et al., 2008; Roopun et al., 2008a), switches in temporal structure with changes in activation (Roopun et al., 2008b), fast rhythms nested…...
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Journal Article•DOI•

Feedback Inhibition Enables Theta-Nested Gamma Oscillations and Grid Firing Fields

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Hugh Pastoll¹, Lukas Solanka¹, Mark C. W. van Rossum¹, Matthew F. Nolan¹•Institutions (1)

University of Edinburgh¹

09 Jan 2013-Neuron

TL;DR: This work establishes with optogenetic activation of layer II of the medial entorhinal cortex that theta frequency drive to this circuit is sufficient to generate nested gamma frequency oscillations in synaptic activity and indicates that grid cells communicate primarily via inhibitory interneurons.

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266 citations

Cites background from "NMDA receptor-dependent switching b..."

...(G) Schematic indicates the slice cut to separate layers II and III (left)....
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...…of nested gamma activity reported in the MEC of behaving animals (Chrobak and Buzsáki, 1998; Colgin et al., 2009) and much higher than the frequency of pharmacologically induced gamma oscillations (Cunningham et al., 2003; Dickson et al., 2000; Middleton et al., 2008; van Der Linden et al., 1999)....
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...Examples of synaptic currents (row 2), corresponding scalograms (row 3), and the mean scalograms for all experiments (row 4), each plotted as a function of the phase of theta stimulation, demonstrate that nested gamma is maintained when connections between layers II and III are cut (control) and after subsequent block of NMDA receptors with 50 mM D-APV but is abolished by complete block of iGluRs....
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...…pharmacological models of gamma activity in the MEC in which the frequency of excitatory drive to interneurons is less than the network gamma frequency (Cunningham et al., 2003) and in which NMDA receptor activation is required for oscillations generatedwithin layer II (Middleton et al., 2008)....
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...Blocking NMDA receptors abolishes pharmacologically induced gamma activity generated locally in layer II of the MEC and reveals lower-frequency activity that originates from layer III (Middleton et al., 2008)....
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References

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Journal Article•DOI•

Organization of the entorhinal—hippocampal system: A review of current anatomical data

[...]

Menno P. Witter¹•Institutions (1)

VU University Amsterdam¹

01 Oct 1993-Hippocampus

542 citations

Journal Article•DOI•

Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells.

[...]

John O'Keefe¹, Neil Burgess¹•Institutions (1)

University College London¹

01 Jan 2005-Hippocampus

TL;DR: The hypothesis that hippocampal pyramidal cells encode information by their phase of firing relative to the theta rhythm of the EEG is reviewed and a model of the firing of the recently discovered “grid cells” in entorhinal cortex as part of a path‐integration system is proposed.

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Abstract: We review the ideas and data behind the hypothesis that hippocampal pyramidal cells encode information by their phase of firing relative to the theta rhythm of the EEG. Particular focus is given to the further hypothesis that variations in firing rate can encode information independently from that encoded by firing phase. We discuss possible explanation of the phase-precession effect in terms of interference between two independent oscillatory influences on the pyramidal cell membrane potential, and the extent to which firing phase reflects internal dynamics or external (environmental) variables. Finally, we propose a model of the firing of the recently discovered "grid cells" in entorhinal cortex as part of a path-integration system, in combination with place cells and head-direction cells.

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517 citations

"NMDA receptor-dependent switching b..." refers background in this paper

...Interestingly, combining two different gamma frequencies with values around 30 Hz (from area CA3) and 40 Hz (directly from mEC)—as would be expected at the level of area CA1—produces a pattern of frequency beating within the hippocampal theta range (7–13 Hz), a mode of frequency interaction proposed, for theta frequencies, to underlie phase precession in hippocampus (32)....
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Journal Article•DOI•

Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice.

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Sheriar G. Hormuzdi, Isabel Pais¹, Fiona E. N. LeBeau¹, Stephen K. Towers¹, Andrei Rozov², Eberhard H. Buhl¹, Miles A. Whittington¹, Hannah Monyer² - Show less +4 more•Institutions (2)

University of Leeds¹, Max Planck Society²

16 Aug 2001-Neuron

TL;DR: It is shown that the loss of this protein disrupts gamma frequency network oscillations in vitro but leaves high frequency rhythms, which may involve gap junctions between principal cells (Schmitz et al., 2001), unaffected.

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509 citations

"NMDA receptor-dependent switching b..." refers background in this paper

...During persistent gamma rhythms in intact hippocampal slices, the gamma rhythm is seen to be generated in area CA3 with frequencies between 30–40 Hz (2, 22), a generally lower frequency than that seen in control conditions in comparable mEC slice preparations (15, 17) (see above)....
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Journal Article•DOI•

Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro

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Miles A. Whittington¹, Roger D. Traub²•Institutions (2)

University of Leeds¹, SUNY Downstate Medical Center²

01 Dec 2003-Trends in Neurosciences

TL;DR: This review concentrates on recent in vitro evidence revealing a division of labour among different subclasses of interneurons with respect to the frequency of persistent rhythms, and the crucial dependence on gap-junction-mediated intercellular communication for the generation and maintenance of these rhythms.

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496 citations

"NMDA receptor-dependent switching b..." refers background in this paper

...The latter study demonstrated gamma frequency outputs not only from perisomatic targeting basket cells (the accepted source of gamma frequency inhibitory inputs to principal cells (13), but also from trilaminar and bistratified interneurons with terminals predominantly in dendrite-containing laminae....
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Journal Article•DOI•

Transgenic Inhibition of Synaptic Transmission Reveals Role of CA3 Output in Hippocampal Learning

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Toshiaki Nakashiba¹, Jennie Z. Young¹, Thomas J. McHugh¹, Derek L. Buhl¹, Susumu Tonegawa¹ - Show less +1 more•Institutions (1)

Picower Institute for Learning and Memory¹

29 Feb 2008-Science

TL;DR: A generally applicable tetanus toxin–based method for transgenic mice that permits inducible and reversible inhibition of synaptic transmission and applied it to the trisynaptic pathway is developed and it is found that synaptic output from CA3 in the transexual pathway is dispensable and the short monosynaptic pathways is sufficient for incremental spatial learning.

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Abstract: The hippocampus is an area of the brain involved in learning and memory. It contains parallel excitatory pathways referred to as the trisynaptic pathway (which carries information as follows: entorhinal cortex --> dentate gyrus --> CA3 --> CA1 --> entorhinal cortex) and the monosynaptic pathway (entorhinal cortex --> CA1 --> entorhinal cortex). We developed a generally applicable tetanus toxin-based method for transgenic mice that permits inducible and reversible inhibition of synaptic transmission and applied it to the trisynaptic pathway while preserving transmission in the monosynaptic pathway. We found that synaptic output from CA3 in the trisynaptic pathway is dispensable and the short monosynaptic pathway is sufficient for incremental spatial learning. In contrast, the full trisynaptic pathway containing CA3 is required for rapid one-trial contextual learning, for pattern completion-based memory recall, and for spatial tuning of CA1 cells.

...read moreread less

475 citations

"NMDA receptor-dependent switching b..." refers background in this paper

...Fast, one-trial contextual learning is critically dependent on the trisynaptic circuit but the direct mEC-CA1 pathway is sufficient for slower, multitrial learning (45)....
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