NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex
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.
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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TL;DR: It is found that human resting-state functional connectivity was better predicted by transitions between brain activity patterns rather than any specific pattern per se, suggesting that functional connectivity underscores transitions between alternative patterns of activity in the brain—even more than the patterns themselves.
Abstract: The brain is a complex, nonlinear system, exhibiting ever-evolving patterns of activities even without external inputs or tasks. Such intrinsic or resting neural dynamics has been found to play critical roles in the normal functioning of the brain and psychiatric disorders. It remains a challenge, however, to link the intrinsic dynamics to the underlying structure, in part, due to the nonlinearity. Here we use a nonlinear-dynamical model to examine how the complexity of intrinsic neural dynamics, in terms of multistability and temporal diversity, is sculpted by structural properties across scales. Our model combines a population-level model (Wilson-Cowan) with additional biophysical constraints (from the Wong-Wang-Deco model). We show that multistability can emerge at the whole-brain level even when individual brain regions are by themselves monostable. The multi-functionality and memory capacity associated with multistability are thus synergistic properties of the whole-brain, irreducible to properties of its parts. The exact size of the functional repertoire and memory capacity is a joint product of the nonlinearity in the local dynamics and the topology of the large-scale network. Similarly, temporal diversity of the brain is determined by both local structural differences and the topology of the global network. Together, this work unravels an intertwined and circular relationship between local and global properties in defining the intrinsic dynamic organization of the brain. Looking forward, the model can be used to probe the multiscale mechanisms underlying psychiatric disorders and the effective scales for treatment.
3 citations
01 Jan 2014
TL;DR: The contributions of rhythms to basic cognitive computations and to major cognitive functions (such as attention and multi-modal coordination) are investigated and the premise that the physiology underlying brain rhythms plays an essential role in how these rhythms facilitate some cognitive operations is offered.
Abstract: Neuronal rhythms are ubiquitous features of brain dynamics, and are highly correlated with cognitive processing. However, the relationship between the physiological mechanisms producing these rhythms and the functions associated with the rhythms remains mysterious. This article investigates the contributions of rhythms to basic cognitive computations (such as filtering signals by coherence and/or frequency) and to major cognitive functions (such as attention and multi-modal coordination). We offer support to the premise that the physiology underlying brain rhythms plays an essential role in how these rhythms facilitate some cognitive operations.
2 citations
01 Jan 2012
2 citations
Cites background from "NMDA receptor-dependent switching b..."
...Furthermore, an NMDAR-dependent switch between fast (here: ~40 Hz) and low (~30 Hz) gamma rhythms has also been found in EC but this could not be replicated in hippocampus (Middleton et al., 2008)....
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Dissertation•
01 Oct 2018
TL;DR: Systemic infection alters neuronal communication by changes to oscillatory activity, but does not change synaptic plasticity levels, which is corroborated in a mouse model of Leishmaniasis.
Abstract: During wakefulness, synapses are strengthened to enable memory formation. Whereas, during sleep, weaker connections are ‘pruned’ to help consolidate memories. These synaptic alterations are related to cortical oscillations, which are generally faster during wakefulness (30-80Hz, gamma), and slower during deep sleep (1-4Hz, delta). Synaptic strength is thought to decrease during delta rhythms (compared to gamma rhythms). Neuroinflammation can disturb these brain rhythms and lead to a decline in cognitive function, which may result from aberrations in synaptic plasticity.
To test the laminar and cellular changes in synaptic plasticity during sleep- and wake-related oscillations, in vitro electrophysiology and immunofluorescence were employed using acute rat neocortical slices. To examine the effect of neuroinflammation on these brain states, systemic infection was induced using synthetic analogues of pathogenic bacterial and viral material, and a biological parasitic disease model.
The expression of an immediate early gene (IEG) marker of neuronal plasticity (Arc) was higher during delta oscillations compared to gamma oscillations and was concentrated to mid-apical dendrite bundles from layer V intrinsically bursting cells. These bundles represented cortical microcolumns which are known to exhibit synchronous activity, allowing parallel processing of information. Increased Arc expression in these columns during delta oscillations may promote synaptic rescaling and highlights the role of cortical microcolumns in memory consolidation.
A balance of pro- and anti-inflammatory cytokines was found after short term systemic infection which gave way to a predominately pro-inflammatory state when the infection was longer term. The oscillatory activity also changed, with a continued decline in gamma power. However, delta power increased short term but decreased with a longer infection. The systemic infection had no effect on cortical plasticity. These results were corroborated in a mouse model of Leishmaniasis and show that systemic infection alters neuronal communication by changes to oscillatory activity, but does not change synaptic plasticity levels.
2 citations
TL;DR: The interactions among different ion channels and receptors regulate neuronal excitability; frequency and pattern of firing of action potentials (AP); propagation of the AP along the axon; neurotransmitter release at synaptic terminals; AP backpropagation from theAxon initial segment to the somatodendritic domain; dendritic integration of synaptic signals; and use-dependent plasticity.
Abstract: Ion channels and receptors are the fundamental basis for neuronal communication in the nervous system and are important targets of autoimmunity. The different neuronal domains contain a unique repertoire of voltage-gated Na+ (Nav), Ca2 + (Cav), and K+ (Kv), as well as other K+ channels and hyperpolarization-gated cyclic nucleotide-regulated channels. The distinct ion channel distribution defines the electrophysiologic properties of different subtypes of neurons. The different neuronal compartments also express neurotransmitter-gated ion channels, or ionotropic receptors, as well as G protein-coupled receptors. Of particular relevance in the central nervous system are excitatory glutamate receptors and inhibitory γ-aminobutyric acid and glycine receptors. The interactions among different ion channels and receptors regulate neuronal excitability; frequency and pattern of firing of action potentials (AP); propagation of the AP along the axon; neurotransmitter release at synaptic terminals; AP backpropagation from the axon initial segment to the somatodendritic domain; dendritic integration of synaptic signals; and use-dependent plasticity.
2 citations
Cites background from "NMDA receptor-dependent switching b..."
...These GABAergic interneurons are critical for cortical network oscillations at gamma (g) frequency, which allows the precise timing of spiking of functionally linked pyramidal neurons during a variety of cognitive tasks (Bannerman et al., 2008; Middleton et al., 2008; Wang et al., 2008); impaired NMDA receptor-mediated activation of these GABAergic neurons in the prefrontal or anterior cingulate cortex has been implicated in the cognitive manifestations of schizophrenia (Woo et al....
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References
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TL;DR: The results indicate that transient coupling between low- and high-frequency brain rhythms coordinates activity in distributed cortical areas, providing a mechanism for effective communication during cognitive processing in humans.
Abstract: We observed robust coupling between the high- and low-frequency bands of ongoing electrical activity in the human brain. In particular, the phase of the low-frequency theta (4 to 8 hertz) rhythm modulates power in the high gamma (80 to 150 hertz) band of the electrocorticogram, with stronger modulation occurring at higher theta amplitudes. Furthermore, different behavioral tasks evoke distinct patterns of theta/high gamma coupling across the cortex. The results indicate that transient coupling between low- and high-frequency brain rhythms coordinates activity in distributed cortical areas, providing a mechanism for effective communication during cognitive processing in humans.
2,404 citations
"NMDA receptor-dependent switching b..." refers background in this paper
...This mechanism can underlie gamma rhythms in a broad range of frequencies from around 20 Hz up to 70 Hz in the hippocampus (8) but cannot support higher frequencies such as those labeled as ‘‘high gamma’’ previously (9)....
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TL;DR: It is proposed that interneuron network oscillations, in conjunction with intrinsic membrane resonances and long-loop (such as thalamocortical) interactions, contribute to 40-Hz rhythms in vivo.
Abstract: Partially synchronous 40-Hz oscillations of cortical neurons have been implicated in cognitive function. Specifically, coherence of these oscillations between different parts of the cortex may provide conjunctive properties to solve the 'binding problem': associating features detected by the cortex into unified perceived objects. Here we report an emergent 40-Hz oscillation in networks of inhibitory neurons connected by synapses using GABAA (gamma-aminobutyric acid) receptors in slices of rat hippocampus and neocortex. These network inhibitory postsynaptic potential oscillations occur in response to the activation of metabotropic glutamate receptors. The oscillations can entrain pyramidal cell discharges. The oscillation frequency is determined both by the net excitation of interneurons and by the kinetics of the inhibitory postsynaptic potentials between them. We propose that interneuron network oscillations, in conjunction with intrinsic membrane resonances and long-loop (such as thalamocortical) interactions, contribute to 40-Hz rhythms in vivo.
1,625 citations
"NMDA receptor-dependent switching b..." refers background in this paper
...The basic mechanism of generation of population gamma rhythms by local neuronal circuits reveals an absolute dependence on the influence of fast spiking inhibitory interneurons at the level of principal cell somata (5, 6),with the frequency dependent on the magnitude and kinetics of gamma aminobutyric acid (GABAA) receptor-mediated synaptic events (7)....
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TL;DR: It is suggested that gamma oscillation emerges from an interaction between intrinsic oscillatory properties of interneurons and the network properties of the dentate gyrus and that Gamma oscillation in the CA3-CA1 circuitry is suppressed by either the hilar region or the entorhinal cortex.
Abstract: The cellular generation and spatial distribution of gamma frequency (40-100 Hz) activity was examined in the hippocampus of the awake rat. Field potentials and unit activity were recorded by multiple site silicon probes (5- and 16-site shanks) and wire electrode arrays. Gamma waves were highly coherent along the long axis of the dentate hilus, but average coherence decreased rapidly in the CA3 and CA1 directions. Analysis of short epochs revealed large fluctuations in coherence values between the dentate and CA1 gamma waves. Current source density analysis revealed large sinks and sources in the dentate gyrus with spatial distribution similar to the dipoles evoked by stimulation of the perforant path. The frequency changes of gamma and theta waves positively correlated (40-100 Hz and 5-10 Hz, respectively). Putative interneurons in the dentate gyrus discharged at gamma frequency and were phase-locked to the ascending part of the gamma waves recorded from the hilus. Following bilateral lesion of the entorhinal cortex the power and frequency of hilar gamma activity significantly decreased or disappeared. Instead, a large amplitude but slower gamma pattern (25-50 Hz) emerged in the CA3-CA1 network. We suggest that gamma oscillation emerges from an interaction between intrinsic oscillatory properties of interneurons and the network properties of the dentate gyrus. We also hypothesize that under physiological conditions the hilar gamma oscillation may be entrained by the entorhinal rhythm and that gamma oscillation in the CA3-CA1 circuitry is suppressed by either the hilar region or the entorhinal cortex.
1,529 citations
"NMDA receptor-dependent switching b..." refers background in this paper
...For example, removal of entorhinal cortex in vivo produces a slower gamma rhythm (39), whose origins appear to be in area CA3 (40)....
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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.
985 citations
"NMDA receptor-dependent switching b..." refers background in this paper
...For example, removal of entorhinal cortex in vivo produces a slower gamma rhythm (39), whose origins appear to be in area CA3 (40)....
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TL;DR: In this paper, the authors used high-resolution (1.5-millimeter isotropic voxels) functional magnetic resonance imaging to measure brain activity during incidental memory encoding.
Abstract: Pattern separation, the process of transforming similar representations or memories into highly dissimilar, nonoverlapping representations, is a key component of many functions ascribed to the hippocampus. Computational models have stressed the role of the hippocampus and, in particular, the dentate gyrus and its projections into the CA3 subregion in pattern separation. We used high-resolution (1.5-millimeter isotropic voxels) functional magnetic resonance imaging to measure brain activity during incidental memory encoding. Although activity consistent with a bias toward pattern completion was observed in CA1, the subiculum, and the entorhinal and parahippocampal cortices, activity consistent with a strong bias toward pattern separation was observed in, and limited to, the CA3/dentate gyrus. These results provide compelling evidence of a key role of the human CA3/dentate gyrus in pattern separation.
899 citations