Comparison between spontaneous and kainate‐induced gamma oscillations in the mouse hippocampus <i>in vitro</i>

Pietersen, Alexander N.J.; Patel, Nisha; Jefferys, John G. R.; Vreugdenhil, Martin

doi:10.1111/j.1460-9568.2009.06771.x

Cited by 26 publications

(25 citation statements)

References 54 publications

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“…The results from our simulations are consistent with experiments in vitro showing that NMDAR blockade does not affect gamma oscillations that are, however, abolished by AMPAR antagonists (Traub et al, 1996;Buhl et al, 1998;Fisahn et al, 1998;LeBeau et al, 2002;Cunningham et al, 2006;Roopun et al, 2008). Moreover, in some in vivo and in vitro studies NMDAR blockade increased the gamma oscillation power (Roopun et al, 2008;Pinault, 2008;Hakami et al, 2009;Pietersen et al, 2009;Hong et al, 2010), consistent with the effect of lowering g ni in our simulations.…”

Section: Resultssupporting

confidence: 90%

“…Conversely, decreases in the slow NMDA conductance at pyramidal-FS neuron synapses increased gamma power in the network model. Similarly, NMDAR antagonists enhance gamma power in animal models (Pinault, 2008;Roopun et al, 2008;Hakami et al, 2009;Pietersen et al, 2009) or human subjects (Hong et al, 2010). Our simulations therefore suggest that rapid FS neuron activation (Jonas et al, 2004;Hu et al, 2010) is crucial for the production of gamma oscillations.…”

Section: Discussionmentioning

confidence: 99%

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Glutamate Receptor Subtypes Mediating Synaptic Activation of Prefrontal Cortex Neurons: Relevance for Schizophrenia

Rotaru¹,

Yoshino²,

Lewis³

et al. 2011

J. Neurosci.

139

159

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Schizophrenia may involve hypofunction of NMDAR-mediated signaling, and alterations in parvalbumin-positive fast-spiking (FS) GABA neurons that may cause abnormal gamma oscillations. It was recently hypothesized that prefrontal cortex (PFC) FS neuron activity is highly dependent on NMDAR activation and that, consequently, FS neuron dysfunction in schizophrenia is secondary to NMDAR hypofunction. However, NMDARs are abundant in synapses onto PFC pyramidal neurons, thus a key question is whether FS neuron or pyramidal cell activation is more dependent on NMDARs. We examined the AMPAR and NMDAR contribution to synaptic activation of FS neurons and pyramidal cells in the PFC of adult mice. In FS neurons, EPSCs had fast decay and weak NMDAR contribution whereas in pyramidal cells EPSCs were significantly prolonged by NMDAR-mediated currents. Moreover, the AMPAR/NMDAR EPSC ratio was higher in FS cells. NMDAR antagonists decreased EPSPs and EPSP-spike coupling more strongly in pyramidal cells than in FS neurons, showing that FS neuron activation is less NMDAR-dependent than pyramidal cell excitation. The precise EPSP-spike coupling produced by fast-decaying EPSCs in FS cells may be important for network mechanisms of gamma oscillations based on feedback inhibition. To test this possibility, we used simulations in a computational network of reciprocally-connected FS neurons and pyramidal cells and found that brief AMPAR-mediated FS neuron activation is crucial to synchronize, via feedback inhibition, pyramidal cells in the gamma frequency band. Our results raise interesting questions about the mechanisms that might link NMDAR hypofunction to alterations of FS neurons in schizophrenia.

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Section: Resultssupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Glutamate Receptor Subtypes Mediating Synaptic Activation of Prefrontal Cortex Neurons: Relevance for Schizophrenia

Rotaru¹,

Yoshino²,

Lewis³

et al. 2011

J. Neurosci.

139

159

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“…Gamma oscillations in CA3 show the strongest sink–source sequence at the stratum pyramidale–stratum lucidum (Pietersen et al . ). In isolated CA1 slices (cut like in Fig.…”

Section: Resultsmentioning

confidence: 97%

Transition between fast and slow gamma modes in rat hippocampus area CA1 in vitro is modulated by slow CA3 gamma oscillations

Pietersen

Ward

Hagger-Vaughan

et al. 2014

The Journal of Physiology

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Key pointsr The synchronisation of neuronal activity at gamma frequencies (30-100 Hz) could determine the effectiveness of neuronal communication.r Gamma oscillations in the CA1 region of the hippocampus in vitro was thought to be dependent on gamma oscillations generated in area CA3, but in vivo CA1 can generate gamma oscillations independently.r In this study we found that activating acetylcholine receptors induced stable gamma oscillations in the CA1 local network isolated in slices in vitro that were faster than those in CA3, but relied on similar neuronal circuitry involving feedback inhibition.r Gamma frequency inputs from CA3 (spontaneous in intact hippocampal slices or stimulated in isolated CA1) can suppress the local fast gamma oscillation in CA1 and force it to adopt the slower CA3 oscillation through feed-forward inhibition.r This modulation could allow CA1 to alternate between effective communication with the entorhinal cortex and CA3, which may regulate memory encoding and memory recall phases.Abstract Hippocampal gamma oscillations have been associated with cognitive functions including navigation and memory encoding/retrieval. Gamma oscillations in area CA1 are thought to depend on the oscillatory drive from CA3 (slow gamma) or the entorhinal cortex (fast gamma). Here we show that the local CA1 network can generate its own fast gamma that can be suppressed by slow gamma-paced inputs from CA3. Moderate acetylcholine receptor activation induces fast (45 ± 1 Hz) gamma in rat CA1 minislices and slow (33 ± 1 Hz) gamma in CA3 minislices in vitro. Using pharmacological tools, current-source density analysis and intracellular recordings from pyramidal cells and fast-spiking stratum pyramidale interneurons, we demonstrate that fast gamma in CA1 is of the pyramidal-interneuron network gamma (PING) type, with the firing of principal cells paced by recurrent perisomal IPSCs. The oscillation frequency was only weakly dependent on IPSC amplitude, and decreased to that of CA3 slow gamma by reducing IPSC decay rate or reducing interneuron activation through tonic inhibition of interneurons. Fast gamma in CA1 was replaced by slow CA3-driven gamma in unlesioned slices, which could be mimicked in CA1 minislices by sub-threshold 35 Hz Schaffer collateral stimulation that activated fast-spiking interneurons but hyperpolarised pyramidal cells, suggesting that slow gamma frequency CA3 outputs can suppress the CA1 fast gamma-generating network by feed-forward inhibition and replaces it with a slower gamma oscillation driven by feed-forward inhibition. The transition between the two gamma oscillation modes in CA1 might allow it to alternate between effective communication with the medial entorhinal cortex and CA3, which have different roles in encoding and recall of memory.

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“…The lack of the rest of the brain and of blood supply obviously has a major impact, and indeed reduced activity can be an advantage for reductionist studies of the properties of single neurons and synaptic connections. However, the low levels of activity mean that population activities including coherent oscillations usually (but not always, Pietersen et al, 2009) need sustained chemical or other stimulation, such as mGluR agonists, kainic acid or carbachol (Bartos et al, 2007;Fisahn et al, 1998;Whittington et al, 1995). Such models, combined with computational models in silico (see Section 6 below), have told us much on how neuronal networks can sustain coherent oscillations, and especially on the important roles of inhibitory interneurons in γ oscillations (Bartos et al, 2007).…”

Section: Preparations and Physiological Oscillationsmentioning

confidence: 99%

Mechanisms of physiological and epileptic HFO generation

Jefferys

Prida

Wendling

et al. 2012

Progress in Neurobiology

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268

238

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High frequency oscillations (HFO) have a variety of characteristics: band-limited or broad-band, transient burst-like phenomenon or steady-state. HFOs may be encountered under physiological or under pathological conditions (pHFO). Here we review the underlying mechanisms of oscillations, at the level of cells and networks, investigated in a variety of experimental in vitro and in vivo models. Diverse mechanisms are described, from intrinsic membrane oscillations to network processes involving different types of synaptic interactions, gap junctions and ephaptic coupling. HFOs with similar frequency ranges can differ considerably in their physiological mechanisms. The fact that in most cases the combination of intrinsic neuronal membrane oscillations and synaptic circuits are necessary to sustain network oscillations is emphasized. Evidence for pathological HFOs, particularly fast ripples, in experimental models of epilepsy and in human epileptic patients is scrutinized. The underlying mechanisms of fast ripples are examined both in the light of animal observations, in vivo and in vitro, and in epileptic patients, with emphasis on single cell dynamics. Experimental observations and computational modeling have led to hypotheses for these mechanisms, several of which are considered here, namely the role of out-ofphase firing in neuronal clusters, the importance of strong excitatory AMPA-synaptic currents and recurrent inhibitory connectivity in combination with the fast time scales of IPSPs, ephaptic coupling and the contribution of interneuronal coupling through gap junctions. The statistical behaviour of fast ripple events can provide useful information on the underlying mechanism and can help to further improve classification of the diverse forms of HFOs.

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Comparison between spontaneous and kainate‐induced gamma oscillations in the mouse hippocampus in vitro

Cited by 26 publications

References 54 publications

Glutamate Receptor Subtypes Mediating Synaptic Activation of Prefrontal Cortex Neurons: Relevance for Schizophrenia

Glutamate Receptor Subtypes Mediating Synaptic Activation of Prefrontal Cortex Neurons: Relevance for Schizophrenia

Transition between fast and slow gamma modes in rat hippocampus area CA1 in vitro is modulated by slow CA3 gamma oscillations

Mechanisms of physiological and epileptic HFO generation

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