Instantaneous Modulation of Gamma Oscillation Frequency by Balancing Excitation with Inhibition

Atallah, Bassam V.; Scanziani, Massimo

doi:10.1016/j.neuron.2009.04.027

Cited by 553 publications

(614 citation statements)

References 57 publications

(82 reference statements)

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“…3C). Given that prior experiments suggest cycle-by-cycle recruitment of inhibition after excitation in orchestrating high-frequency rhythms (20), it is likely that the origin of the observed fast rhythms in our experiment was either distal to the recorded region/layer or included a mixture of distal and focal elements. These possible distal contributions could be conveyed through afferents from different layers of the involved column or from neighboring areas.…”

Section: Discussionmentioning

confidence: 88%

“…Mechanistically, it has been shown that the temporal interplay of synaptic excitation and inhibition (15) and the dynamic balance of ensemble excitation and inhibition (13) shape the neocortical network activity during different states [wakefulness, SWS, and rapid eye movement (REM)]. Specifically, studies of hippocampal and entorhinal cortex point to a link between phasic discharge of fast-spiking (FS) interneurons and the γ-cycle (16)(17)(18)(19), and show how the excitation/inhibition balance modulates γ-oscillations (20). Both experimental and simulation studies frame β-oscillations as inhibition-based rhythms as well (21,22).…”

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confidence: 99%

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High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

Quyen

Muller

Teleńczuk

et al. 2016

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

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Beta (β)-and gamma (γ)-oscillations are present in different cortical areas and are thought to be inhibition-driven, but it is not known if these properties also apply to γ-oscillations in humans. Here, we analyze such oscillations in high-density microelectrode array recordings in human and monkey during the wake-sleep cycle. In these recordings, units were classified as excitatory and inhibitory cells. We find that γ-oscillations in human and β-oscillations in monkey are characterized by a strong implication of inhibitory neurons, both in terms of their firing rate and their phasic firing with the oscillation cycle. The β-and γ-waves systematically propagate across the array, with similar velocities, during both wake and sleep. However, only in slow-wave sleep (SWS) β-and γ-oscillations are associated with highly coherent and functional interactions across several millimeters of the neocortex. This interaction is specifically pronounced between inhibitory cells. These results suggest that inhibitory cells are dominantly involved in the genesis of β-and γ-oscillations, as well as in the organization of their large-scale coherence in the awake and sleeping brain. The highest oscillation coherence found during SWS suggests that fast oscillations implement a highly coherent reactivation of wake patterns that may support memory consolidation during SWS.excitation | inhibition | state-dependent firing | wave propagation | synchrony N eocortical beta (β)-and gamma (γ)-oscillations have been largely studied in the context of action/cognition during wakefulness (1-3). Although numerous studies have focused intensely on the information-processing role of β and γ during wakefulness, these rhythms do also occur during deep anesthesia and natural sleep (4-6). Additionally, although very-high-frequency allocortical oscillations (e.g., ripples at 80-200 Hz and fast ripples at 200-500 Hz in rodent/human hippocampus) have been thoroughly implicated in sleep-dependent memory consolidation (ref. 7 and reviewed in refs. 8 and 9), the occurrence and role of neocortical β-and γ-oscillations during sleep remain largely unexplored and related studies have been limited to macroscopic (whole-brain) scales (e.g., ref. 10). A recent study using microwires and intracranial electroencephalography (iEEG) recordings in the neocortex of epileptics has verified the strong presence of γ-oscillations during slow-wave sleep (SWS) (11). That study also showed a marked increase of spiking during γ, a suggestive indicator of association with cortical UP states. Here, we evaluate the presence of neocortical β-and γ-oscillations during the wake-sleep cycle at the level of local circuitry using dense 2D multielectrode recordings with identified excitatory and inhibitory cells (12, 13).Experimental and theoretical studies suggest that thalamocortical oscillations (including β and γ) are generated through a combination of intrinsic mechanisms involving the interplay between different ionic currents and extrinsic interaction of inhibitory and excitatory c...

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Section: Discussionmentioning

confidence: 88%

mentioning

confidence: 99%

High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

Quyen

Muller

Teleńczuk

et al. 2016

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

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“…Third, GABA A receptors opposite PV cell terminals produce very rapid rising and decaying IPSCs. Loss of PV immunoreactivity because of a reduction in PV expression and actual loss of PV-positive cells has been implicated in a number of neuropsychiatric diseases and models associated with schizophrenia (65)(66)(67)(68). Although both are considered markers for loss of appropriate inhibition, it remains a matter of contention whether loss of PV protein or loss of the PV cells themselves generates the decreased immunoreactivity observed in the disease state.…”

Section: Role Of Disrupted Fast-phasic Inhibition In Reduced γ-Power mentioning

confidence: 99%

Dysbindin-1 mutant mice implicate reduced fast-phasic inhibition as a final common disease mechanism in schizophrenia

Carlson

Talbot²,

Halene³

et al. 2011

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

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DTNBP1 (dystrobrevin binding protein 1) is a leading candidate susceptibility gene in schizophrenia and is associated with working memory capacity in normal subjects. In schizophrenia, the encoded protein dystrobrevin-binding protein 1 (dysbindin-1) is often reduced in excitatory cortical limbic synapses. We found that reduced dysbindin-1 in mice yielded deficits in auditory-evoked response adaptation, prepulse inhibition of startle, and evoked γ-activity, similar to patterns in schizophrenia. In contrast to the role of dysbindin-1 in glutamatergic transmission, γ-band abnormalities in schizophrenia are most often attributed to disrupted inhibition and reductions in parvalbumin-positive interneuron (PV cell) activity. To determine the mechanism underlying electrophysiological deficits related to reduced dysbindin-1 and the potential role of PV cells, we examined PV cell immunoreactivity and measured changes in net circuit activity using voltage-sensitive dye imaging. The dominant circuit impact of reduced dysbindin-1 was impaired inhibition, and PV cell immunoreactivity was reduced. Thus, this model provides a link between a validated candidate gene and an auditory endophenotypes. Furthermore, these data implicate reduced fast-phasic inhibition as a common underlying mechanism of schizophrenia-associated intermediate phenotypes.GABAergic | γ-oscillation | hippocampus | evoked response spectral perturbation | Sandy mouse P atients with schizophrenia have reduced amplitude and gating of auditory event-related potentials (ERPs) (1, 2). Recent clinical studies also show abnormal γ-band oscillations (30-100 Hz) as an endophenotype of the illness that is associated with reduced cognitive function (3-7). Work in animal models shows a prominent role of cortical inhibitory networks in generating γ-oscillations (8, 9), which in turn, supports the role of aberrant GABAergic inhibition as an important potential component of schizophrenia (4,7,10,11). The GABA-producing enzyme glutamic acid decarboxylase is dysregulated in schizophrenia, and postsynaptic GABA A receptors are dysregulated as well (4). Risk alleles for GABA A receptor subunits are also associated with the disease (12, 13), although linkage is weaker than the linkage found with dysbindin-1 and other candidate genes such as DISC1 (14). At the anatomical level, there is a loss of immunoreactivity for parvalbumin (PV) in schizophrenia. PV is a calcium-binding protein marker for a class of fast-spiking GABAergic neurons. It is debated whether reduced PV in postmortem studies is caused by reduction in cell number or merely loss of protein expression. In either case, reduced PV immunoreactivity suggests disruption of an important source of local circuit inhibition (4, 15).Although clinical electrophysiological and postmortem anatomical findings support the role of GABA dysfunction in schizophrenia, a larger set of schizophrenia risk haplotypes are thought to confer reduced NMDA receptor-mediated function and changes in glutamatergic transmission [e.g., DISC1; Neuregu...

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“…The frequency of gamma oscillation depends on the surrounding circuitry and its behavior (Atallah and Scanziani, 2009;Mann and Mody, 2010). Therefore, pair-by-pair variability of the peak frequencies might be expected to be larger in SUA-SUA coherence than those between MUAs or between MUA and LFP, since the variability of the surrounding circuit would be larger in the case of single-unit pairs compared with other configurations.…”

Section: Coherence and Granger Causalitymentioning

confidence: 99%

Triphasic Dynamics of Stimulus-Dependent Information Flow between Single Neurons in Macaque Inferior Temporal Cortex

Hirabayashi¹,

Takeuchi²,

Tamura³

et al. 2010

J. Neurosci.

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The functional connectivity between cortical neurons is not static and is known to exhibit contextual modulations in terms of the coupling strength. Here we hypothesized that the information flow in a cortical local circuit exhibits complex forward-and-back dynamics, and conducted Granger causality analysis between the neuronal spike trains that were simultaneously recorded from macaque inferior temporal (IT) cortex while the animals performed a visual object discrimination task. Spikes from neuron pairs with a displaced peak on the cross-correlogram (CCG) showed Granger causality in the gamma-frequency range (30 -80 Hz) with the dominance in the direction consistent with the CCG peak (forward direction). Although, in a classical view, the displaced CCG peak has been interpreted as an indicative of a pauci-synaptic serial linkage, temporal dynamics of the gamma Granger causality after stimulus onset exhibited a more complex triphasic pattern,withatransientforwardcomponentfollowedbyaslowlydevelopingbackwardcomponentandsubsequentreappearanceoftheforward component. These triphasic dynamics of causality were not explained by the firing rate dynamics and were not observed for cell pairs that exhibited a center peak on the CCG. Furthermore, temporal dynamics of Granger causality depended on the feature configuration within the presented object. Together, these results demonstrate that the classical view of functional connectivity could be expanded to incorporate more complex forward-and-back dynamics and also imply that multistage processing in the recognition of visual objects might be implemented by multiphasic dynamics of directional information flow between single neurons in a local circuit in the IT cortex.

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Instantaneous Modulation of Gamma Oscillation Frequency by Balancing Excitation with Inhibition

Cited by 553 publications

References 57 publications

High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

Dysbindin-1 mutant mice implicate reduced fast-phasic inhibition as a final common disease mechanism in schizophrenia

Triphasic Dynamics of Stimulus-Dependent Information Flow between Single Neurons in Macaque Inferior Temporal Cortex

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