Slow and Fast Inhibition and an H-Current Interact to Create a Theta Rhythm in a Model of CA1 Interneuron Network

Rotstein, Horacio G.; Pervouchine, Dmitri D.; Acker, Corey D.; Gillies, Martin J.; White, John A.; Buhl, Eberhardt H.; Whittington, Miles A.; Kopell, Nancy

doi:10.1152/jn.00957.2004

Cited by 162 publications

(188 citation statements)

References 67 publications

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“…Rate variability can occur because assembly oscillation is a cooperative product where timing of spikes remains robust despite the variation of individual firing rates (51)(52)(53). In addition, the oscillating cell assembly hypothesis can also account for the observation that spikes of single place cells can switch assembly membership even within a single cycle (24).…”

Section: Distance Representation By Time Compression Is Speed-dependentmentioning

confidence: 99%

Hippocampal place cell assemblies are speed-controlled oscillators

Geisler

Robbe

Zugaro

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

249

321

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The phase of spikes of hippocampal pyramidal cells relative to the local field oscillation shifts forward (''phase precession'') over a full cycle as the animal crosses the cell's receptive field (''place field''). The linear relationship between the phase of the spikes and the travel distance within the place field is independent of the animal's running speed. This invariance of the phase-distance relationship is likely to be important for coordinated activity of hippocampal cells and space coding, yet the mechanism responsible for it is not known. Here we show that at faster running speeds place cells are active for fewer cycles but oscillate at a higher frequency and emit more spikes per cycle. As a result, the phase shift of spikes from cycle to cycle (i.e., temporal precession slope) is faster, yet spatial-phase precession stays unchanged. Interneurons can also show transient-phase precession and contribute to the formation of coherently precessing assemblies. We hypothesize that the speed-correlated acceleration of place cell assembly oscillation is responsible for the phase-distance invariance of hippocampal place cells.cell assembly ͉ interneurons ͉ phase locking ͉ phase precession ͉ oscillations W hile animals navigate in an environment, the hippocampal local field potential (LFP) is characterized by a highly regular oscillation (8-10 Hz). Principal cells in the hippocampus show place-specific firing by two criteria. First, the firing is tuned to a particular location (''place field''), showing a bellshaped tuning curve centered around its preferred location (1). Second, the timing of spikes within subsequent cycles systematically shifts forward (''phase precession''), Ϸ1 full cycle in total, as the rat runs through the place field of the neuron (2, 3) (see also Fig. 1 A and B). Both the firing rate and discharge phase within a cycle are correlated with the rat's position. However, how the rate change and -phase precession of spikes are related is poorly understood. The available experiments support both a rate-phase interdependence (4-6) and independence (7).Several explanations for the place-phase relationship were put forward (4)(5)(6)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18). To confront these models, we examined the relationship among running speed, oscillation frequency of place cells and LFP , and timing of spikes within the cycle. We show that principal cells oscillate at a frequency faster than the simultaneously recorded LFP oscillation, and that this oscillation frequency depends on the rat's running speed. Together with the place-and speed-dependent oscillation frequencies of interneurons, the findings support the hypothesis that place coding results from coordinated network activity. We propose that the locomotion speed-dependent oscillation of place cell assemblies may underlie the mechanisms responsible for distance encoding in the hippocampus. ResultsWe recorded the firing patterns of pyramidal cells, interneurons, and the LFP from the CA1 pyramidal layer of rats as they ran on a U-shap...

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Section: Distance Representation By Time Compression Is Speed-dependentmentioning

confidence: 99%

Hippocampal place cell assemblies are speed-controlled oscillators

Geisler

Robbe

Zugaro

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

249

321

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“…To better understand possible field effects at the network level, we have developed a twodimensional spiking model of the hippocampal CA3 which includes pyramidal and OLM neurons as well as basket cells (based on [4,10,15]). Extending these models, we implement an orthogonal arrangement of theta and gamma rhythm-generating circuits with OLM axons arborizing anisotropically in a septotemporal orientation and CA3 collaterals and basket cell axons extending in a lamellar orientation (Fig.2, left).…”

Section: Computational Modelmentioning

confidence: 99%

“…Basket and OLM cells were implemented as one-compartment and pyramidal cells as fourcompartment neurons with fast Na, K, and leak currents, as well as excitatory (AMPA) and inhibitory (GABA A ) synaptic currents. Additionally, pyramidal cells included NMDA excitatory channels and an afterhyperpolarizing current, while OLM neurons included persistent Na and h-currents [15].…”

Section: Computational Modelmentioning

confidence: 99%

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Switching between gamma and theta: Dynamic network control using subthreshold electric fields

Berzhanskaya

Gorchetchnikov

2007

Neurocomputing

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We implemented an experimentally observed orthogonal arrangement of theta and gamma generation circuitry in septotemporal and lamellar dimensions is a two-dimensional model of hippocampus. The model includes three types of cells: pyramidal, basket, and oriens lacunosum-moleculare (OLM) neurons. In this reduced model, application of continuous electric fields allowed us to switch between theta, gamma and mixed theta-gamma regimes without additional pharmacological manipulation. Electric field effects on individual neurons were modeled based on experimental data. Network simulation results predict a flexible experimental technique, which would employ adaptive subthreshold electric fields to continuously modulate neuronal ensemble activity, and can be used for testing cognitive correlates of oscillatory rhythms as well as for suppressing epileptiform activity.

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“…γ oscillation is associated with the activation of fastfiring basket cell inhibitory interneurons [28,29] that act on fast GABA A receptors [30][31][32] , whereas, θ oscillation involves slow stellate cell inhibitory interneurons [33] that act on slow GABA A receptors [30] . Our results suggest that the γ oscillation induced by nicotine and DHPG may be involved in the activation of the fast firing inhibitory interneuron in the MSDB.…”

Section: Discussionmentioning

confidence: 99%

Co-activation of nAChR and mGluR induces γ oscillation in rat medial septum diagonal band of Broca slices

Wang

Ouyang

et al. 2014

Acta Pharmacol Sin

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Aim: To examine whether co-activation of nAChR and mGluR1 induced γ oscillation (20-60 Hz) in rat medial septum diagonal band of Broca (MSDB) slices. Methods: Rat brain sagittal slices containing the MSDB were prepared. Extracellular field potentials were recorded with glass microelectrodes. The nAChR and mGluR1 agonists were applied to the slices to induce network activity. Data analysis was performed off-line using software Spike 2. Results: Co-application of the nAChR agonist nicotine (1 µmol/L) and the mGluR1 agonist dihydroxyphenylglycine (DHPG, 25 µmol/L) was able to induce γ oscillation in MSDB slices. The intensity of nAChR and mGluR1 activation was critical for induction of network oscillation at a low (θ oscillation) or high frequency (γ oscillation): co-application of low concentrations of the two agonists only increased the power and frequency of oscillation within the range of θ, whereas γ oscillation mostly appeared when high concentrations of the two agonists were applied. Conclusion: Activation of mGluR1 and nAChR is able to program slow or fast network oscillation by altering the intensity of receptor activation, which may provide a mechanism for modulation of learning and memory.

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Slow and Fast Inhibition and an H-Current Interact to Create a Theta Rhythm in a Model of CA1 Interneuron Network

Cited by 162 publications

References 67 publications

Hippocampal place cell assemblies are speed-controlled oscillators

Hippocampal place cell assemblies are speed-controlled oscillators

Switching between gamma and theta: Dynamic network control using subthreshold electric fields

Co-activation of nAChR and mGluR induces γ oscillation in rat medial septum diagonal band of Broca slices

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