Contribution of a single CA3 neuron to network synchrony

doi:10.1016/J.NEUROIMAGE.2006.01.007

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Contribution of a single CA3 neuron to network synchrony

Journal Article•DOI•

Contribution of a single CA3 neuron to network synchrony

Jarno E. Mikkonen¹, Joanna K. Huttunen¹, Markku Penttonen¹•Institutions (1)

University of Eastern Finland¹

01 Jul 2006-NeuroImage (Academic Press)-Vol. 31, Iss: 3, pp 1222-1227

TL;DR: It is reported that an individual CA3 pyramidal cell can activate the CA1 neuronal network in vivo in rat hippocampus using electrical stimulations with simultaneous intracellular gamma and extracellular theta and slow and slow frequencies.

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About: This article is published in NeuroImage.The article was published on 2006-07-01. It has received 9 citations till now. The article focuses on the topics: Pyramidal cell & Biological neural network.

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Journal Article•DOI•

Propagation of specific network patterns through the mouse hippocampus.

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Martin Both¹, Florian Bähner¹, Oliver von Bohlen und Halbach¹, Andreas Draguhn¹•Institutions (1)

Heidelberg University¹

01 Sep 2008-Hippocampus

TL;DR: Propagation of ripples through the hippocampal loop maintained precise temporal relationships at the network and cellular level, as indicated by coupling of field potentials, multiunit and single cell activity between major portions of CA3 and CA1.

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Abstract: Network oscillations bind neurons into transient assemblies with coherent activity, enabling temporal coding. In the mammalian hippocampus, spatial relationships are represented by sequences of action potentials of place cells. Such patterns are established during memory acquisition and are re-played during sharp wave-ripple complexes in CA1 in subsequent sleep episodes. These events originate in CA3 and travel towards CA1 and downstream cortical areas. It is unclear, however, whether specific sequences of ripple-associated firing are solely defined within the CA1 network or whether these patterns are directly entrained by preceding activities of neurons within CA3. Using a model of sharp wave-ripple oscillations (SPW-R) in mouse hippocampal slices we analyzed the propagation of these signals between CA3 and CA1. We found tight coupling between high-frequency network activity in CA3 and CA1. Propagation of ripples through the hippocampal loop maintained precise temporal relationships at the network and cellular level, as indicated by coupling of field potentials, multiunit and single cell activity between major portions of CA3 and CA1. Moreover, SPW-R-like activity in CA1 could be elicited by electrical stimulation within area CA3 while antidromic activation of CA1 failed to induce organized high-frequency oscillations. Our data show that the specificity of neuronal assemblies is maintained with cell-to-cell precision while SPW-R propagate along the hippocampal loop.

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60 citations

Journal Article•DOI•

Field Potential Signature of Distinct Multicellular Activity Patterns in the Mouse Hippocampus

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Susanne Reichinnek¹, Thomas Künsting, Andreas Draguhn, Martin Both•Institutions (1)

Heidelberg University¹

17 Nov 2010-The Journal of Neuroscience

TL;DR: Application of unbiased sorting algorithms to sharp wave–ripple complexes in mouse hippocampal slices did indeed reveal the reliable recurrence of defined waveforms that were robust over prolonged recording periods and may be important for cognition-related physiological studies in humans and behaving animals.

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Abstract: Cognitive functions go along with complex patterns of distributed activity in neuronal networks, thereby forming assemblies of selected neurons. To support memory processes, such assemblies have to be stabilized and reactivated in a highly reproducible way. The rodent hippocampus provides a well studied model system for network mechanisms underlying spatial memory formation. Assemblies of place-encoding cells are repeatedly activated during sleep-associated network states called sharp wave–ripple complexes (SPW-Rs). Behavioral studies suggest that at any time the hippocampus harbors a limited number of different assemblies that are transiently stabilized for memory consolidation. We hypothesized that the corresponding field potentials (sharp wave–ripple complexes) contain a specific signature of the underlying neuronal activity patterns. Hence, they should fall into a limited number of different waveforms. Application of unbiased sorting algorithms to sharp wave–ripple complexes in mouse hippocampal slices did indeed reveal the reliable recurrence of defined waveforms that were robust over prolonged recording periods. Single-unit discharges tended to fire selectively with certain SPW-R classes and were coupled above chance level. Thus, field SPW-Rs of different waveforms are directly related to the underlying multicellular activity patterns that recur with high fidelity. This direct relationship between the coordinated activity of distinct groups of neurons and macroscopic electrographic signals may be important for cognition-related physiological studies in humans and behaving animals.

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57 citations

Cites background from "Contribution of a single CA3 neuron..."

...Action potentials of one or few neurons can have significant impact on the local field, either by their direct contribution (Rasch et al., 2009) or by synaptically mediated effects on multiple target cells (Mikkonen et al., 2006; Huttunen et al., 2008)....
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...A similar strong influence of few neurons in CA3 on network patterns in CA1 has previously been shown for theta and gamma oscillations in vivo (Mikkonen et al., 2006)....
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Journal Article•DOI•

Characterization of synchronized bursts in cultured hippocampal neuronal networks with learning training on microelectrode arrays.

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Yanling Li¹, Wei Zhou¹, Xiangning Li¹, Shaoqun Zeng¹, Man Liu¹, Qingming Luo¹ - Show less +2 more•Institutions (1)

Huazhong University of Science and Technology¹

15 Jun 2007-Biosensors and Bioelectronics

TL;DR: Results indicate that firing, association and synchrony of spontaneous bursts in neuronal networks were promoted by learning, and are encouraged to think of a more engineered system based on in vitro hippocampal neurons, as a novel sensitive system for electrophysiological evaluations.

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43 citations

Journal Article•DOI•

The limits of brain determinacy

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Peter G.H. Clarke¹•Institutions (1)

University of Lausanne¹

07 May 2012-Proceedings of The Royal Society B: Biological Sciences

TL;DR: Developmental stochasticity is sufficiently low to make neurobehavioural defects uncommon, but a chance component of neural development remains, indicating that the authors' brains and behaviour are not entirely determined by a combination of genes-plus-environment.

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Abstract: The genes do not control everything that happens in a cell or an organism, because thermally induced molecular movements and conformation changes are beyond genetic control. The importance of uncontrolled events has been argued from the differences between isogenic organisms reared in virtually identical environments, but these might alternatively be attributed to subtle, undetected differences in the environment. The present review focuses on the uncontrolled events themselves in the context of the developing brain. These are considered at cellular and circuit levels because even if cellular physiology was perfectly controlled by the genes (which it is not), the interactions between different cells might still be uncoordinated. A further complication is that the brain contains mechanisms that buffer noise and others that amplify it. The final resultant of the battle between these contrary mechanisms is that developmental stochasticity is sufficiently low to make neurobehavioural defects uncommon, but a chance component of neural development remains. Thus, our brains and behaviour are not entirely determined by a combination of genes-plus-environment.

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15 citations

Journal Article•DOI•

The Effect of Neural Noise on Spike Time Precision in a Detailed CA3 Neuron Model

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Eduard Kuriscak¹, Petr Marsalek¹, Petr Marsalek², Julius Stroffek¹, Zdenek Wunsch¹ - Show less +1 more•Institutions (2)

Charles University in Prague¹, Czech Technical University in Prague²

24 Jun 2012-Computational and Mathematical Methods in Medicine

TL;DR: This study investigates the spike time precision of a multicompartmental pyramidal neuron model of the CA3 region of the hippocampus under the influence of various sources of neuronal noise, and describes differences in the contribution to noise originating from voltage-gated ion channels, synaptic vesicles release, and vesicle quantal size.

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Abstract: Experimental and computational studies emphasize the role of the millisecond precision of neuronal spike times as an important coding mechanism for transmitting and representing information in the central nervous system. We investigate the spike time precision of a multicompartmental pyramidal neuron model of the CA3 region of the hippocampus under the influence of various sources of neuronal noise. We describe differences in the contribution to noise originating from voltage-gated ion channels, synaptic vesicle release, and vesicle quantal size. We analyze the effect of interspike intervals and the voltage course preceding the firing of spikes on the spike-timing jitter. The main finding of this study is the ranking of different noise sources according to their contribution to spike time precision. The most influential is synaptic vesicle release noise, causing the spike jitter to vary from 1 ms to 7 ms of a mean value 2.5 ms. Of second importance was the noise incurred by vesicle quantal size variation causing the spike time jitter to vary from 0.03 ms to 0.6 ms. Least influential was the voltage-gated channel noise generating spike jitter from 0.02 ms to 0.15 ms.

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9 citations

Cites methods from "Contribution of a single CA3 neuron..."

...Although hippocampal cells’ discharge frequency is closer to the theta regimes and even lower [25], the frequencies around the gamma band were also observed in CA3 neurons [75] and were simulated in our model as well, allowing us to measure the spiking precision for shorter ISI intervals....
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References

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Journal Article•DOI•

Neuronal Oscillations in Cortical Networks

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György Buzsáki¹, Andreas Draguhn²•Institutions (2)

Rutgers University¹, Heidelberg University²

25 Jun 2004-Science

TL;DR: Recent findings indicate that network oscillations bias input selection, temporally link neurons into assemblies, and facilitate synaptic plasticity, mechanisms that cooperatively support temporal representation and long-term consolidation of information.

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Abstract: Clocks tick, bridges and skyscrapers vibrate, neuronal networks oscillate. Are neuronal oscillations an inevitable by-product, similar to bridge vibrations, or an essential part of the brain’s design? Mammalian cortical neurons form behavior-dependent oscillating networks of various sizes, which span five orders of magnitude in frequency. These oscillations are phylogenetically preserved, suggesting that they are functionally relevant. Recent findings indicate that network oscillations bias input selection, temporally link neurons into assemblies, and facilitate synaptic plasticity, mechanisms that cooperatively support temporal representation and long-term consolidation of information.

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5,512 citations

"Contribution of a single CA3 neuron..." refers background or methods in this paper

..., 2003), yet responding to multiple coexisting spike patterns (Penttonen and Buzsaki, 2003; Buzsaki and Draguhn, 2004), in neuronal networks....
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...In essence, we combined intracellular CA3 gamma stimulation with extrahippocampal theta stimulation in order to create ‘‘local’’ fast gamma oscillations with ‘‘global’’ theta oscillations in the background (Buzsaki and Draguhn, 2004)....
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...This indicates that more widely spread theta frequencies may be considered as a prerequisite for local hippocampal gamma frequencies (Buzsaki and Draguhn, 2004) and that different frequency ranges serve different functions within intact neuronal networks (Steriade, 2001)....
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...local hippocampal gamma frequencies (Buzsaki and Draguhn, 2004) and that different frequency ranges serve different functions within intact neuronal networks (Steriade, 2001)....
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...…emerge from distinct populations of neurons in the CA1 neuronal network (Izhikevich et al., 2003), the CA1 neuronal population response to the single CA3 pyramidal cell input suggests that in vivo neuronal network can self organize to meet the demands of its inputs (Buzsaki and Draguhn, 2004)....
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Journal Article•DOI•

Dynamic predictions: Oscillations and synchrony in top–down processing

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Andreas K. Engel, Pascal Fries¹, Pascal Fries², Wolf Singer³•Institutions (3)

National Institutes of Health¹, F.C. Donders Centre for Cognitive Neuroimaging², Max Planck Society³

01 Oct 2001-Nature Reviews Neuroscience

TL;DR: It is argued that coherence among subthreshold membrane potential fluctuations could be exploited to express selective functional relationships during states of expectancy or attention, and these dynamic patterns could allow the grouping and selection of distributed neuronal responses for further processing.

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Abstract: Classical theories of sensory processing view the brain as a passive, stimulus-driven device. By contrast, more recent approaches emphasize the constructive nature of perception, viewing it as an active and highly selective process. Indeed, there is ample evidence that the processing of stimuli is controlled by top-down influences that strongly shape the intrinsic dynamics of thalamocortical networks and constantly create predictions about forthcoming sensory events. We discuss recent experiments indicating that such predictions might be embodied in the temporal structure of both stimulus-evoked and ongoing activity, and that synchronous oscillations are particularly important in this process. Coherence among subthreshold membrane potential fluctuations could be exploited to express selective functional relationships during states of expectancy or attention, and these dynamic patterns could allow the grouping and selection of distributed neuronal responses for further processing.

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3,330 citations

"Contribution of a single CA3 neuron..." refers background in this paper

...Gamma and theta frequencies have been shown to participate in information transfer in neuronal networks (O’Keefe and Recce, 1993; Chrobak and Buzsaki, 1998; Engel et al., 2001; Jensen and Lisman, 2005)....
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..., 2004; Jensen and Lisman, 2005), and binding (Nowak et al., 1997; Engel et al., 2001)....
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...Thereby, these frequencies coincide with brain states that promote cognitive processes such as learning (Wallenstein and Hasselmo, 1997), memory (Herrmann et al., 2004; Jensen and Lisman, 2005), and binding (Nowak et al., 1997; Engel et al., 2001)....
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Journal Article•DOI•

Phase relationship between hippocampal place units and the EEG theta rhythm

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John O'Keefe¹, Michael Recce¹•Institutions (1)

University College London¹

01 Jul 1993-Hippocampus

TL;DR: The phase was highly correlated with spatial location and less well correlated with temporal aspects of behavior, such as the time after place field entry, and the characteristics of the phase shift constrain the models that define the construction of place fields.

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Abstract: Many complex spike cells in the hippocampus of the freely moving rat have as their primary correlate the animal's location in an environment (place cells). In contrast, the hippocampal electroencephalograph theta pattern of rhythmical waves (7-12 Hz) is better correlated with a class of movements that change the rat's location in an environment. During movement through the place field, the complex spike cells often fire in a bursting pattern with an interburst frequency in the same range as the concurrent electroencephalograph theta. The present study examined the phase of the theta wave at which the place cells fired. It was found that firing consistently began at a particular phase as the rat entered the field but then shifted in a systematic way during traversal of the field, moving progressively forward on each theta cycle. This precession of the phase ranged from 100 degrees to 355 degrees in different cells. The effect appeared to be due to the fact that individual cells had a higher interburst rate than the theta frequency. The phase was highly correlated with spatial location and less well correlated with temporal aspects of behavior, such as the time after place field entry. These results have implications for several aspects of hippocampal function. First, by using the phase relationship as well as the firing rate, place cells can improve the accuracy of place coding. Second, the characteristics of the phase shift constrain the models that define the construction of place fields. Third, the results restrict the temporal and spatial circumstances under which synapses in the hippocampus could be modified.

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2,434 citations

"Contribution of a single CA3 neuron..." refers background in this paper

...Gamma and theta frequencies have been shown to participate in information transfer in neuronal networks (O’Keefe and Recce, 1993; Chrobak and Buzsaki, 1998; Engel et al., 2001; Jensen and Lisman, 2005)....
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...Hippocampal gamma and theta frequencies have been mainly encompassed with learning and memory (O’Keefe and Recce, 1993; Lisman and Idiart, 1995; Mikkonen et al., 2002; Kobayashi and Poo, 2004; Jensen and 1053-8119/$ - see front matter D 2006 Elsevier Inc....
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Journal Article•DOI•

Storage of 7 +/- 2 short-term memories in oscillatory subcycles

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John E. Lisman¹, Marco Idiart¹•Institutions (1)

Brandeis University¹

10 Mar 1995-Science

TL;DR: It is shown that activity patterns associated with multiple memories can be stored in a single neural network that exhibits nested oscillations similar to those recorded from the brain.

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Abstract: Psychophysical measurements indicate that human subjects can store approximately seven short-term memories. Physiological studies suggest that short-term memories are stored by patterns of neuronal activity. Here it is shown that activity patterns associated with multiple memories can be stored in a single neural network that exhibits nested oscillations similar to those recorded from the brain. Each memory is stored in a different high-frequency ("40 hertz") subcycle of a low-frequency oscillation. Memory patterns repeat on each low-frequency (5 to 12 hertz) oscillation, a repetition that relies on activity-dependent changes in membrane excitability rather than reverberatory circuits. This work suggests that brain oscillations are a timing mechanism for controlling the serial processing of short-term memories.

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1,421 citations

"Contribution of a single CA3 neuron..." refers background in this paper

...Hippocampal gamma and theta frequencies have been mainly encompassed with learning and memory (O’Keefe and Recce, 1993; Lisman and Idiart, 1995; Mikkonen et al., 2002; Kobayashi and Poo, 2004; Jensen and 1053-8119/$ - see front matter D 2006 Elsevier Inc....
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...Similar recruitment can be achieved also with hippocampal gamma frequency field stimulations that induce timed recurrent activity in the CA3 (Fujisawa et al., 2004) and CA1 (Lisman and Idiart, 1995) networks....
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Journal Article•DOI•

Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat

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Jozsef Csicsvari¹, Brian Jamieson², Kensall D. Wise², György Buzsáki¹•Institutions (2)

Rutgers University¹, University of Michigan²

23 Jan 2003-Neuron

TL;DR: This work examines the generation of gamma oscillation currents in the hippocampus, using two-dimensional, 96-site silicon probes and identifies two gamma generators, one in the dentate gyrus and another in the CA3-CA1 regions.

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985 citations

"Contribution of a single CA3 neuron..." refers background in this paper

...Thereby, our results emphasize the specific role of individual neurons working at gamma frequencies (Henze et al., 2002; Csicsvari et al., 2003), yet responding to multiple coexisting spike patterns (Penttonen and Buzsaki, 2003; Buzsaki and Draguhn, 2004), in neuronal networks....
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