Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks
TL;DR: Experimental analysis in the hippocampus and the neocortex and computational analysis suggests that synaptic specialization turns interneuron networks into robust gamma frequency oscillators.
Abstract: Gamma frequency oscillations are thought to provide a temporal structure for information processing in the brain. They contribute to cognitive functions, such as memory formation and sensory processing, and are disturbed in some psychiatric disorders. Fast-spiking, parvalbumin-expressing, soma-inhibiting interneurons have a key role in the generation of these oscillations. Experimental analysis in the hippocampus and the neocortex reveals that synapses among these interneurons are highly specialized. Computational analysis further suggests that synaptic specialization turns interneuron networks into robust gamma frequency oscillators.
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TL;DR: High-density recordings of field activity in animals and subdural grid recordings in humans can provide insight into the cooperative behaviour of neurons, their average synaptic input and their spiking output, and can increase the understanding of how these processes contribute to the extracellular signal.
Abstract: Neuronal activity in the brain gives rise to transmembrane currents that can be measured in the extracellular medium. Although the major contributor of the extracellular signal is the synaptic transmembrane current, other sources — including Na+ and Ca2+ spikes, ionic fluxes through voltage- and ligand-gated channels, and intrinsic membrane oscillations — can substantially shape the extracellular field. High-density recordings of field activity in animals and subdural grid recordings in humans, combined with recently developed data processing tools and computational modelling, can provide insight into the cooperative behaviour of neurons, their average synaptic input and their spiking output, and can increase our understanding of how these processes contribute to the extracellular signal.
3,366 citations
TL;DR: It is proposed that information is gated by inhibiting task-irrelevant regions, thus routing information to task-relevant regions and the empirical support for this framework is discussed.
Abstract: In order to understand the working brain as a network, it is essential to identify the mechanisms by which information is gated between regions. We here propose that information is gated by inhibiting task-irrelevant regions, thus routing information to task-relevant regions. The functional inhibition is reflected in oscillatory activity in the alpha band (8-13 Hz). From a physiological perspective the alpha activity provides pulsed inhibition reducing the processing capabilities of a given area. Active processing in the engaged areas is reflected by neuronal synchronization in the gamma band (30-100 Hz) accompanied by an alpha band decrease. According to this framework the brain should be studied as a network by investigating cross-frequency interactions between gamma and alpha activity. Specifically the framework predicts that optimal task performance will correlate with alpha activity in task-irrelevant areas. In this review we will discuss the empirical support for this framework. Given that alpha activity is by far the strongest signal recorded by EEG and MEG, we propose that a major part of the electrophysiological activity detected from the working brain reflects gating by inhibition.
2,448 citations
Cites background from "Synaptic mechanisms of synchronized..."
...It should be mentioned that GABAergic interneurons also have been strongly implicated in the generation of the much faster 30–100 Hz gamma rhythm (Traub et al., 1999; Bartos et al., 2007; Mann and Paulsen, 2007; Cardin et al., 2009; Sohal et al., 2009)....
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...• While extensive work has been devoted to understanding the physiological mechanism generating for instance the gamma rhythm and spindle oscillations (Destexhe et al., 1998; Traub et al., 1999; Bartos et al., 2007; Mann and Paulsen, 2007; Cardin et al., 2009; Sohal et al., 2009) less is known about how the alpha rhythm is generated....
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...…to understanding the physiological mechanism generating for instance the gamma rhythm and spindle oscillations (Destexhe et al., 1998; Traub et al., 1999; Bartos et al., 2007; Mann and Paulsen, 2007; Cardin et al., 2009; Sohal et al., 2009) less is known about how the alpha rhythm is generated....
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TL;DR: The cellular and synaptic mechanisms underlying gamma oscillations are reviewed and empirical questions and controversial conceptual issues are outlined, finding that gamma-band rhythmogenesis is inextricably tied to perisomatic inhibition.
Abstract: Gamma rhythms are commonly observed in many brain regions during both waking and sleep states, yet their functions and mechanisms remain a matter of debate. Here we review the cellular and synaptic mechanisms underlying gamma oscillations and outline empirical questions and controversial conceptual issues. Our main points are as follows: First, gamma-band rhythmogenesis is inextricably tied to perisomatic inhibition. Second, gamma oscillations are short-lived and typically emerge from the coordinated interaction of excitation and inhibition, which can be detected as local field potentials. Third, gamma rhythm typically concurs with irregular firing of single neurons, and the network frequency of gamma oscillations varies extensively depending on the underlying mechanism. To document gamma oscillations, efforts should be made to distinguish them from mere increases of gamma-band power and/or increased spiking activity. Fourth, the magnitude of gamma oscillation is modulated by slower rhythms. Such cross-frequency coupling may serve to couple active patches of cortical circuits. Because of their ubiquitous nature and strong correlation with the "operational modes" of local circuits, gamma oscillations continue to provide important clues about neuronal population dynamics in health and disease.
2,168 citations
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.
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.
1,774 citations
Cites background from "Synaptic mechanisms of synchronized..."
...Given such input variations, and the high heterogeneity of both cellular and synaptic properties in interneurons (887), how can synchronous oscillations be maintained robustly? Modeling studies suggest that synchrony can be more robustly realized in spite of heterogeneity when GABAA receptor-mediated synaptic inhibition is strong (53, 54, 947, 1008)....
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TL;DR: CFC might serve as a mechanism to transfer information from large-scale brain networks operating at behavioral timescales to the fast, local cortical processing required for effective computation and synaptic modification, thus integrating functional systems across multiple spatiotemporal scales.
1,701 citations
References
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TL;DR: This work aims to understand how an enormous network of interacting dynamical systems — be they neurons, power stations or lasers — will behave collectively, given their individual dynamics and coupling architecture.
Abstract: The study of networks pervades all of science, from neurobiology to statistical physics. The most basic issues are structural: how does one characterize the wiring diagram of a food web or the Internet or the metabolic network of the bacterium Escherichia coli? Are there any unifying principles underlying their topology? From the perspective of nonlinear dynamics, we would also like to understand how an enormous network of interacting dynamical systems-be they neurons, power stations or lasers-will behave collectively, given their individual dynamics and coupling architecture. Researchers are only now beginning to unravel the structure and dynamics of complex networks.
7,665 citations
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.
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.
5,512 citations
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...jpg" NDATA ITEM> ]> Oscillatory activity is a hallmark of neuronal network function in various brain regions, including the olfactory bulb, thalamus, hippocampus and neocorte...
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3,359 citations
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.
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.
2,434 citations
TL;DR: The results demonstrate that local neuronal populations in the visual cortex engage in stimulus-specific synchronous oscillations resulting from an intracortical mechanism, and may provide a general mechanism by which activity patterns in spatially separate regions of the cortex are temporally coordinated.
Abstract: In areas 17 and 18 of the cat visual cortex the firing probability of neurons, in response to the presentation of optimally aligned light bars within their receptive field, oscillates with a peak frequency near 40 Hz. The neuronal firing pattern is tightly correlated with the phase and amplitude of an oscillatory local field potential recorded through the same electrode. The amplitude of the local field-potential oscillations are maximal in response to stimuli that match the orientation and direction preference of the local cluster of neurons. Single and multiunit recordings from the dorsal lateral geniculate nucleus of the thalamus showed no evidence of oscillations of the neuronal firing probability in the range of 20-70 Hz. The results demonstrate that local neuronal populations in the visual cortex engage in stimulus-specific synchronous oscillations resulting from an intracortical mechanism. The oscillatory responses may provide a general mechanism by which activity patterns in spatially separate regions of the cortex are temporally coordinated.
2,404 citations
"Synaptic mechanisms of synchronized..." refers background in this paper
...Within this spectrum, gamma oscillations have received particular attention, because their relationship to higher brain functions is most eviden...
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