Theta activity paradoxically boosts gamma and ripple frequency sensitivity in prefrontal interneurons

Fast oscillations in cortical circuits critically depend on GABAergic interneurons. Which interneuron types and populations can drive different cortical rhythms, however, remains unresolved and may depend on brain state. Here, we measured the sensitivity of different GABAergic interneurons in prefrontal cortex under conditions mimicking distinct brain states. While fast-spiking neurons always exhibited a wide bandwidth of around 400 Hz, the response properties of spike-frequency adapting interneurons switched with the background input’s statistics. Slowly fluctuating background activity, as typical for sleep or quiet wakefulness, dramatically boosted the neurons’ sensitivity to gamma and ripple frequencies. We developed a time-resolved dynamic gain analysis and revealed rapid sensitivity modulations that enable neurons to periodically boost gamma oscillations and ripples during specific phases of ongoing low-frequency oscillations. This mechanism predicts these prefrontal interneurons to be exquisitely sensitive to high-frequency ripples, especially during brain states characterized by slow rhythms, and to contribute substantially to theta-gamma cross-frequency coupling.

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Background correlations selectively boost the gamma-sensitivity of cortical GABAergic neurons

10.1101/2019.12.19.882639 ◽

2019 ◽

Author(s):

Ricardo Martins Merino ◽

Carolina Leon-Pinzon ◽

Walter Stühmer ◽

Martin Möck ◽

Jochen F. Staiger ◽

...

Keyword(s):

High Frequency ◽

Background Activity ◽

Dynamic Control ◽

Gamma Oscillations ◽

Gabaergic Neurons ◽

Brain State ◽

Gabaergic Interneurons ◽

Cortical Circuits ◽

Frequency Coupling ◽

Cross Frequency Coupling

SUMMARYGamma oscillations in cortical circuits critically depend on GABAergic interneurons. Precisely which interneuron types and populations can drive cortical gamma, however, remains unresolved and may depend on brain state. Here we show that spike-frequency adapting interneurons dramatically boost their gamma-sensitivity in the presence of slowly fluctuating background activity. This mechanism allows the dynamic control of gamma oscillations, induces cross-frequency coupling and predicts these interneurons to be exquisitely sensitive to high-frequency ripples.

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Short-term effects on brain functional network caused by focused-attention meditation revealed by Tucker3 clustering on graph theoretical metrics

10.1101/765693 ◽

2019 ◽

Author(s):

Takuma Miyoshi ◽

Kensuke Tanioka ◽

Shoko Yamamoto ◽

Hiroshi Yadohisa ◽

Tomoyuki Hiroyasu ◽

...

Keyword(s):

Low Frequency ◽

Brain Regions ◽

Brain State ◽

Focused Attention ◽

Functional Magnetic Resonance ◽

Short Term ◽

Functional Brain ◽

Brain States ◽

The Given ◽

Short Term Effects

AbstractThis study examines the short-term effects of focused-attention meditation on functional brain state in novice meditators. There are a number of feature metrics for functional brain states, such as functional connectivity, graph theoretical metrics, and amplitude of low frequency fluctuation (ALFF). It is necessary to choose appropriate metrics and also to specify the region of interests (ROIs) from a number of brain regions. Here, we use a Tucker3 clustering method, which simultaneously selects the feature vectors (graph theoretical metrics and fractional ALFF) and the ROIs that can discriminate between resting and meditative states based on the characteristics of the given data. In this study, breath-counting meditation, one of the most popular forms of focused-attention meditation, was used and brain activities during resting and meditation states were measured by functional magnetic resonance imaging. The results indicated that the clustering coefficients of eight brain regions tended to increase through the meditation. Our results reveal that short-term effects of breath-counting meditation can be explained by network density changes in these eight brain regions.

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Replicating Cortical Signatures May Open the Possibility for “Transplanting” Brain States via Brain Entrainment

Frontiers in Human Neuroscience ◽

10.3389/fnhum.2021.710003 ◽

2021 ◽

Vol 15 ◽

Author(s):

Alexander Poltorak

Keyword(s):

Neural Correlates ◽

Brain State ◽

Transcranial Stimulation ◽

Emotional States ◽

Cortical Function ◽

Cortical Rhythms ◽

Brain States ◽

Psychiatric Conditions ◽

Oscillatory Network ◽

The Brain

Brain states, which correlate with specific motor, cognitive, and emotional states, may be monitored with noninvasive techniques such as electroencephalography (EEG) and magnetoencephalography (MEG) that measure macroscopic cortical activity manifested as oscillatory network dynamics. These rhythmic cortical signatures provide insight into the neuronal activity used to identify pathological cortical function in numerous neurological and psychiatric conditions. Sensory and transcranial stimulation, entraining the brain with specific brain rhythms, can effectively induce desired brain states (such as state of sleep or state of attention) correlated with such cortical rhythms. Because brain states have distinct neural correlates, it may be possible to induce a desired brain state by replicating these neural correlates through stimulation. To do so, we propose recording brain waves from a “donor” in a particular brain state using EEG/MEG to extract cortical signatures of the brain state. These cortical signatures would then be inverted and used to entrain the brain of a “recipient” via sensory or transcranial stimulation. We propose that brain states may thus be transferred between people by acquiring an associated cortical signature from a donor, which, following processing, may be applied to a recipient through sensory or transcranial stimulation. This technique may provide a novel and effective neuromodulation approach to the noninvasive, non-pharmacological treatment of a variety of psychiatric and neurological disorders for which current treatments are mostly limited to pharmacotherapeutic interventions.

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Predicting the fMRI signal fluctuation with echo-state neural networks trained on vascular network dynamics

10.1101/807966 ◽

2019 ◽

Author(s):

Filip Sobczak ◽

Yi He ◽

Terrence J. Sejnowski ◽

Xin Yu

Keyword(s):

Low Frequency ◽

Calcium Oscillations ◽

Brain State ◽

Fmri Signal ◽

Human Connectome Project ◽

Vascular Origin ◽

Signal Fluctuation ◽

Brain States ◽

Human Brains ◽

Global Fluctuations

AbstractResting-state functional MRI (rs-fMRI) studies have revealed specific low-frequency hemodynamic signal fluctuations (<0.1 Hz) in the brain, which could be related to oscillations in neural activity through several mechanisms. Although the vascular origin of the fMRI signal is well established, the neural correlates of global rs-fMRI signal fluctuations are difficult to separate from other confounding sources. Recently, we reported that single-vessel fMRI slow oscillations are directly coupled to brain state changes. Here, we used an echo-state network (ESN) to predict the future temporal evolution of the rs-fMRI slow oscillatory feature from both rodent and human brains. rs-fMRI signals from individual blood vessels that were strongly correlated with neural calcium oscillations were used to train an ESN to predict brain state-specific rs-fMRI signal fluctuations. The ESN-based prediction model was also applied to recordings from the Human Connectome Project (HCP), which classified variance-independent brain states based on global fluctuations of rs-fMRI features. The ESN revealed brain states with global synchrony and decoupled internal correlations within the default-mode network.

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Faculty Opinions recommendation of Disinhibition of somatostatin-positive GABAergic interneurons results in an anxiolytic and antidepressant-like brain state.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.726943368.793540754 ◽

2017 ◽

Author(s):

Hans van Bokhoven

Keyword(s):

Brain State ◽

Gabaergic Interneurons

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Impaired spike-gamma coupling of area CA3 fast-spiking interneurons as the earliest functional impairment in the AppNL-G-F mouse model of Alzheimer’s disease

Molecular Psychiatry ◽

10.1038/s41380-021-01257-0 ◽

2021 ◽

Author(s):

Luis Enrique Arroyo-García ◽

Arturo G. Isla ◽

Yuniesky Andrade-Talavera ◽

Hugo Balleza-Tapia ◽

Raúl Loera-Valencia ◽

...

Keyword(s):

Alzheimer’S Disease ◽

Alzheimer's Disease ◽

Cognitive Impairment ◽

Mouse Model ◽

Functional Impairment ◽

Amyloid Β ◽

Gamma Oscillations ◽

Gamma Oscillation ◽

Gamma Rhythm ◽

Fast Spiking

AbstractIn Alzheimer’s disease (AD) the accumulation of amyloid-β (Aβ) correlates with degradation of cognition-relevant gamma oscillations. The gamma rhythm relies on proper neuronal spike-gamma coupling, specifically of fast-spiking interneurons (FSN). Here we tested the hypothesis that decrease in gamma power and FSN synchrony precede amyloid plaque deposition and cognitive impairment in AppNL-G-F knock-in mice (AppNL-G-F). The aim of the study was to evaluate the amyloidogenic pathology progression in the novel AppNL-G-F mouse model using in vitro electrophysiological network analysis. Using patch clamp of FSNs and pyramidal cells (PCs) with simultaneous gamma oscillation recordings, we compared the activity of the hippocampal network of wild-type mice (WT) and the AppNL-G-F mice at four disease stages (1, 2, 4, and 6 months of age). We found a severe degradation of gamma oscillation power that is independent of, and precedes Aβ plaque formation, and the cognitive impairment reported previously in this animal model. The degradation correlates with increased Aβ1-42 concentration in the brain. Analysis on the cellular level showed an impaired spike-gamma coupling of FSN from 2 months of age that correlates with the degradation of gamma oscillations. From 6 months of age PC firing becomes desynchronized also, correlating with reports in the literature of robust Aβ plaque pathology and cognitive impairment in the AppNL-G-F mice. This study provides evidence that impaired FSN spike-gamma coupling is one of the earliest functional impairment caused by the amyloidogenic pathology progression likely is the main cause for the degradation of gamma oscillations and consequent cognitive impairment. Our data suggests that therapeutic approaches should be aimed at restoring normal FSN spike-gamma coupling and not just removal of Aβ.

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Both ongoing alpha and visually induced gamma oscillations show reliable diversity in their across-site phase-relations

Journal of Neurophysiology ◽

10.1152/jn.00788.2014 ◽

2015 ◽

Vol 113 (5) ◽

pp. 1556-1563 ◽

Cited By ~ 20

Author(s):

Freek van Ede ◽

Stan van Pelt ◽

Pascal Fries ◽

Eric Maris

Keyword(s):

Phase Relation ◽

Visual Stimulation ◽

Low Frequency ◽

Gamma Oscillations ◽

Phase Relations ◽

Neural Oscillations ◽

High Signal ◽

Noninvasive Methods ◽

Healthy Human ◽

Systems Neuroscience

Neural oscillations have emerged as one of the major electrophysiological phenomena investigated in cognitive and systems neuroscience. These oscillations are typically studied with regard to their amplitude, phase, and/or phase coupling. Here we demonstrate the existence of another property that is intrinsic to neural oscillations but has hitherto remained largely unexplored in cognitive and systems neuroscience. This pertains to the notion that these oscillations show reliable diversity in their phase-relations between neighboring recording sites (phase-relation diversity). In contrast to most previous work, we demonstrate that this diversity is restricted neither to low-frequency oscillations nor to periods outside of sensory stimulation. On the basis of magnetoencephalographic (MEG) recordings in humans, we show that this diversity is prominent not only for ongoing alpha oscillations (8–12 Hz) but also for gamma oscillations (50–70 Hz) that are induced by sustained visual stimulation. We further show that this diversity provides a dimension within electrophysiological data that, provided a sufficiently high signal-to-noise ratio, does not covary with changes in amplitude. These observations place phase-relation diversity on the map as a prominent and general property of neural oscillations that, moreover, can be studied with noninvasive methods in healthy human volunteers. This opens important new avenues for investigating how neural oscillations contribute to the neural implementation of cognition and behavior.

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Structural alterations in fast-spiking GABAergic interneurons in a model of posttraumatic neocortical epileptogenesis

Neurobiology of Disease ◽

10.1016/j.nbd.2017.08.008 ◽

2017 ◽

Vol 108 ◽

pp. 100-114 ◽

Cited By ~ 8

Author(s):

Feng Gu ◽

Isabel Parada ◽

Fran Shen ◽

Judith Li ◽

Alberto Bacci ◽

...

Keyword(s):

Gabaergic Interneurons ◽

Structural Alterations ◽

Fast Spiking

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Changes in activity of fast-spiking interneurons of the monkey striatum during reaching at a visual target

Journal of Neurophysiology ◽

10.1152/jn.00566.2016 ◽

2017 ◽

Vol 117 (1) ◽

pp. 65-78 ◽

Cited By ~ 3

Author(s):

Kévin Marche ◽

Paul Apicella

Keyword(s):

Target Location ◽

Visual Target ◽

Movement Speed ◽

Gabaergic Interneurons ◽

Movement Preparation ◽

Movement Initiation ◽

Reaching Task ◽

Advance Information ◽

Fast Spiking ◽

Task Conditions

Recent works highlight the importance of local inhibitory interneurons in regulating the function of the striatum. In particular, fast-spiking interneurons (FSIs), which likely correspond to a subgroup of GABAergic interneurons, have been involved in the control of movement by exerting strong inhibition on striatal output pathways. However, little is known about the exact contribution of these presumed interneurons in movement preparation, initiation, and execution. We recorded the activity of FSIs in the striatum of monkeys as they performed reaching movements to a visual target under two task conditions: one in which the movement target was presented at unsignaled left or right locations, and another in which advance information about target location was available, thus allowing monkeys to react faster. Modulations of FSI activity around the initiation of movement (53% of 55 neurons) consisted mostly of increases reaching maximal firing immediately before or, less frequently, after movement onset. Another subset of FSIs showed decreases in activity during movement execution. Rarely did movement-related changes in FSI firing depend on response direction and movement speed. Modulations of FSI activity occurring relatively early in relation to movement initiation were more influenced by the preparation for movement, compared with those occurring later. Conversely, FSI activity remained unaffected, as monkeys were preparing a movement toward a specific location and instead moved to the opposite direction when the trigger occurred. These results provide evidence that changes in activity of presumed GABAergic interneurons of the primate striatum could make distinct contributions to processes involved in movement generation. NEW & NOTEWORTHY We explored the functional contributions of striatal fast-spiking interneurons (FSIs), presumed GABAergic interneurons, to distinct steps of movement generation in monkeys performing a reaching task. The activity of individual FSIs was modulated before and during the movement, consisting mostly of increased in firing rates. Changes in activity also occurred during movement preparation. We interpret this variety of modulation types at different moments of task performance as reflecting differential FSI control over distinct phases of movement.

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