Can the causal role of brain oscillations be studied through rhythmic brain stimulation?

Many studies have investigated the causal relevance of brain-oscillations using rhythmic stimulation, either through direct-brain-stimulation or sensory stimulation. Yet, how intrinsic rhythms interact with the externally generated rhythm is largely unknown. We either presented a flickered visual grating or its correspondent unflickered stimulus in a psychophysical change-detection-task to humans, during simultaneous MEG-recordings, to test the effect of visual entrainment on induced gamma- oscillations. Notably, we generally observed a co-existence of the broadband induced gamma-rhythm with the entrained flicker-rhythm (reliably measured in each participant), with the peak frequency of the induced response remaining unaltered in approximately half of participants - relatively independently of their native frequency. However, flicker increased broadband induced-gamma-power, and this was stronger in participants with a native frequency closer to the flicker-frequency (resonance), and led to strong phase-entrainment. Presence of flicker did not change behaviour itself, but profoundly altered brain-behaviour correlates across the sample: whilst broadband induced gamma-oscillations correlated with reaction-times for unflickered stimuli (as known previously), for the flicker, the amplitude of the entrained flicker-rhythm (but no more the induced oscillation) correlated with reaction-times. This, however, strongly depended on whether a participants peak frequency shifted to the entrained rhythm. Our results suggests that rhythmic brain-stimulation leads to a coexistence of two partially independent oscillations with heterogeneous effects across participants on the downstream relevance of these rhythms for behaviour. This may explain the inconsistency of findings related to external entrainment of brain-oscillations and poses further questions towards causal manipulations of brain-oscillations in general.

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Spectral Properties of Induced and Evoked Gamma Oscillations in Human Early Visual Cortex to Moving and Stationary Stimuli

Journal of Neurophysiology ◽

10.1152/jn.91044.2008 ◽

2009 ◽

Vol 102 (2) ◽

pp. 1241-1253 ◽

Cited By ~ 85

Author(s):

J. B. Swettenham ◽

S. D. Muthukumaraswamy ◽

K. D. Singh

Keyword(s):

Visual Cortex ◽

Stimulus Presentation ◽

Gamma Oscillations ◽

Induced Response ◽

Stimulus Motion ◽

Time Frequency ◽

Beta Power ◽

Visual Areas ◽

Gamma Power ◽

Early Visual Cortex

In two experiments, magnetoencephalography (MEG) was used to investigate the effects of motion on gamma oscillations in human early visual cortex. When presented centrally, but not peripherally, stationary and moving gratings elicited several evoked and induced response components in early visual cortex. Time-frequency analysis revealed two nonphase locked gamma power increases—an initial, rapidly adapting response and one sustained throughout stimulus presentation and varying in frequency across observers from 28 to 64 Hz. Stimulus motion raised the sustained gamma oscillation frequency by a mean of ∼10 Hz. The largest motion-induced frequency increases were in those observers with the lowest gamma response frequencies for stationary stimuli, suggesting a possible saturation mechanism. Moderate gamma amplitude increases to moving versus stationary stimuli were also observed but were not correlated with the magnitude of the frequency increase. At the same site in visual cortex, sustained alpha/beta power reductions and an onset evoked response were observed, but these effects did not change significantly with the presence of motion and did not correlate with the magnitude of gamma power changes. These findings suggest that early visual areas encode moving and stationary percepts via activity at higher and lower gamma frequencies, respectively.

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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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Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area

Journal of Neurophysiology ◽

10.1152/jn.00323.2012 ◽

2012 ◽

Vol 108 (5) ◽

pp. 1392-1402 ◽

Cited By ~ 15

Author(s):

Elsie Premereur ◽

Wim Vanduffel ◽

Pieter R. Roelfsema ◽

Peter Janssen

Keyword(s):

Spatial Attention ◽

Field Potential ◽

Gamma Oscillations ◽

Oculomotor Control ◽

Saccade Target ◽

Frontal Eye Field ◽

Alpha Power ◽

Lateral Intraparietal Area ◽

Electrical Microstimulation ◽

Gamma Power

Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention.

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Orientation and color tuning of the human visual gamma rhythm

10.1101/2021.04.23.441193 ◽

2021 ◽

Author(s):

Ye Li ◽

William Bosking ◽

Michael S Beauchamp ◽

Sameer A Sheth ◽

Daniel Yoshor ◽

...

Keyword(s):

Visual Cortex ◽

Large Scale ◽

Brain Activity ◽

Population Level ◽

Gamma Oscillations ◽

Cell Orientation ◽

Population Activity ◽

Color Tuning ◽

Human Visual Cortex ◽

Gamma Rhythm

Narrowband gamma oscillations (NBG: ~20-60Hz) in visual cortex reflect rhythmic fluctuations in population activity generated by underlying circuits tuned for stimulus location, orientation, and color. Consequently, the amplitude and frequency of induced NBG activity is highly sensitive to these stimulus features. For example, in the non-human primate, NBG displays biases in orientation and color tuning at the population level. Such biases may relate to recent reports describing the large-scale organization of single-cell orientation and color tuning in visual cortex, thus providing a potential bridge between measurements made at different scales. Similar biases in NBG population tuning have been predicted to exist in the human visual cortex, but this has yet to be fully examined. Using intracranial recordings from human visual cortex, we investigated the tuning of NBG to orientation and color, both independently and in conjunction. NBG was shown to display a cardinal orientation bias (horizontal) and also an end- and mid-spectral color bias (red/blue and green). When jointly probed, the cardinal bias for orientation was attenuated and an end-spectral preference for red and blue predominated. These data both elaborate on the close, yet complex, link between the population dynamics driving NBG oscillations and known feature selectivity biases in visual cortex, adding to a growing set of stimulus dependencies associated with the genesis of NBG. Together, these two factors may provide a fruitful testing ground for examining multi-scale models of brain activity, and impose new constraints on the functional significance of the visual gamma rhythm.

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Coherent and intermittent ensemble oscillations emerge from networks of irregular spiking neurons

Journal of Neurophysiology ◽

10.1152/jn.00578.2015 ◽

2016 ◽

Vol 115 (1) ◽

pp. 457-469 ◽

Cited By ~ 6

Author(s):

Mahmood S. Hoseini ◽

Ralf Wessel

Keyword(s):

Single Neuron ◽

Experimental Studies ◽

Field Potential ◽

Gamma Oscillations ◽

Peak Frequency ◽

Spiking Neurons ◽

Network Activity ◽

Cortical Circuits ◽

Model Network ◽

Low Rate

Local field potential (LFP) recordings from spatially distant cortical circuits reveal episodes of coherent gamma oscillations that are intermittent, and of variable peak frequency and duration. Concurrently, single neuron spiking remains largely irregular and of low rate. The underlying potential mechanisms of this emergent network activity have long been debated. Here we reproduce such intermittent ensemble oscillations in a model network, consisting of excitatory and inhibitory model neurons with the characteristics of regular-spiking (RS) pyramidal neurons, and fast-spiking (FS) and low-threshold spiking (LTS) interneurons. We find that fluctuations in the external inputs trigger reciprocally connected and irregularly spiking RS and FS neurons in episodes of ensemble oscillations, which are terminated by the recruitment of the LTS population with concurrent accumulation of inhibitory conductance in both RS and FS neurons. The model qualitatively reproduces experimentally observed phase drift, oscillation episode duration distributions, variation in the peak frequency, and the concurrent irregular single-neuron spiking at low rate. Furthermore, consistent with previous experimental studies using optogenetic manipulation, periodic activation of FS, but not RS, model neurons causes enhancement of gamma oscillations. In addition, increasing the coupling between two model networks from low to high reveals a transition from independent intermittent oscillations to coherent intermittent oscillations. In conclusion, the model network suggests biologically plausible mechanisms for the generation of episodes of coherent intermittent ensemble oscillations with irregular spiking neurons in cortical circuits.

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Reward-Associated Gamma Oscillations in Ventral Striatum Are Regionally Differentiated and Modulate Local Firing Activity

Journal of Neurophysiology ◽

10.1152/jn.00432.2009 ◽

2010 ◽

Vol 103 (3) ◽

pp. 1658-1672 ◽

Cited By ~ 50

Author(s):

Tobias Kalenscher ◽

Carien S. Lansink ◽

Jan V. Lankelma ◽

Cyriel M. A. Pennartz

Keyword(s):

Ventral Striatum ◽

Phase Locking ◽

Gamma Oscillations ◽

Brain Regions ◽

Reward Processing ◽

Temporal Organization ◽

Gamma Activity ◽

Neural Ensembles ◽

Gamma Range ◽

Gamma Power

Oscillations of local field potentials (LFPs) in the gamma range are found in many brain regions and are supposed to support the temporal organization of cognitive, perceptual, and motor functions. Even though gamma oscillations have also been observed in ventral striatum, one of the brain's most important structures for motivated behavior and reward processing, their specific function during ongoing behavior is unknown. Using a movable tetrode array, we recorded LFPs and activity of neural ensembles in the ventral striatum of rats performing a reward-collection task. Rats were running along a triangle track and in each round collected one of three different types of rewards. The gamma power of LFPs on subsets of tetrodes was modulated by reward-site visits, discriminated between reward types, between baitedness of reward locations and was different before versus after arrival at a reward site. Many single units in ventral striatum phase-locked their discharge pattern to the gamma oscillations of the LFPs. Phase-locking occurred more often in reward-related than in reward-unrelated neurons and LFPs. A substantial number of simultaneously recorded LFPs correlated poorly with each other in terms of gamma rhythmicity, indicating that the expression of gamma activity was heterogeneous and regionally differentiated. The orchestration of LFPs and single-unit activity by way of gamma rhythmicity sheds light on the functional architecture of the ventral striatum and the temporal coordination of ventral striatal activity for modulating downstream areas and regulating synaptic plasticity.

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Gamma Oscillations Index Sustained Attention in a Brief Vigilance Task

Proceedings of the Human Factors and Ergonomics Society Annual Meeting ◽

10.1177/1071181321651122 ◽

2021 ◽

Vol 65 (1) ◽

pp. 546-550

Author(s):

Lorraine Borghetti ◽

Megan B. Morris ◽

L. Jack Rhodes ◽

Ashley R. Haubert ◽

Bella Z. Veksler

Keyword(s):

Sustained Attention ◽

Gamma Oscillations ◽

Time On Task ◽

Potential Candidate ◽

Theta Power ◽

High Performers ◽

Beta Power ◽

Study Results ◽

Gamma Power ◽

Compensatory Effort

Sustained attention is an essential behavior in life, but often leads to performance decrements with time. Computational accounts of sustained attention suggest this is due to brief disruptions in goal-directed processing, or microlapses. Decreases in gamma spectral power are a potential candidate for indexing microlapses and discriminating between low and high performers in sustained attention tasks, while increases in beta, alpha, and theta power are expected to exhibit compensatory effort to offset fatigue. The current study tests these hypotheses in a 10-minute Psychomotor Vigilance Test, a context that eliminates confounds with measuring gamma frequencies. 34 participants ( Mage = 22.60; SDage = 4.08) volunteered in the study. Results suggested frontal gamma power declined with time-on-task, indicating reduction in central cognition. Beta power increased with time-on-task, suggesting compensatory effort; however, alpha and theta power did not increase. Additionally, gamma power discriminated between low and high performers, potentially suggesting motivational differences between the groups.

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Cortical oscillations to measure anti-epileptic drug activity in clinical trials

10.21203/rs.3.rs-121959/v1 ◽

2021 ◽

Author(s):

Andrea Biondi ◽

Lorenzo Rocchi ◽

Viviana Santoro ◽

Gregory Beatch ◽

Pierre Rossini ◽

...

Keyword(s):

Clinical Trials ◽

Brain Activity ◽

Systematic Evaluation ◽

Alpha Power ◽

Brain Oscillations ◽

Cortical Oscillations ◽

Anti Epileptic Drug ◽

Beta Power ◽

Gamma Power

Abstract The frequency analysis of electroencephalographic (EEG) activity, either spontaneous or evoked by transcranial magnetic stimulation (TMS-EEG), is a powerful tool to investigate changes in brain activity and excitability following the administration of antiepileptic drugs (AEDs). However, a systematic evaluation of the effect of AEDs on spontaneous and TMS-induced brain oscillations has not yet been provided. We studied the effects of lamotrigine, levetiracetam, and of a novel potassium channel opener (XEN1101) on TMS-induced and spontaneous brain oscillations in a group of healthy volunteers. Levetiracetam suppressed TMS-induced theta, alpha and beta power, whereas lamotrigine increased TMS-induced alpha power. XEN1101 decreased TMS-induced delta, theta and beta power. Resting-state EEG showed a decrease of theta band power after lamotrigine intake. Levetiracetam increased theta, beta and gamma power, while XEN1101 produced an increase of delta, theta, beta and gamma power. Different AEDs induce specific patterns of power changes in spontaneous and TMS-induced brain oscillations. Spontaneous and TMS-induced cortical oscillations represent a powerful tool to characterize the effect of AEDs on in vivo brain activity. Spectral fingerprints of specific AEDs should be further investigated to provide robust and objective biomarkers of biological effect in human clinical trials.

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Noninvasive brain stimulation and brain oscillations

10.1016/b978-0-12-819410-2.00013-8 ◽

2022 ◽

pp. 239-247

Author(s):

Simone Rossi ◽

Emiliano Santarnecchi ◽

Matteo Feurra

Keyword(s):

Brain Stimulation ◽

Brain Oscillations ◽

Noninvasive Brain Stimulation

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Probing the Link Between Perception and Oscillations: Lessons from Transcranial Alternating Current Stimulation

The Neuroscientist ◽

10.1177/1073858419828646 ◽

2019 ◽

Vol 26 (1) ◽

pp. 57-73 ◽

Cited By ~ 4

Author(s):

Yuranny Cabral-Calderin ◽

Melanie Wilke

Keyword(s):

Time Windows ◽

Gamma Oscillations ◽

Alternating Current ◽

Brain Regions ◽

Causal Link ◽

Brain Oscillations ◽

Promising Tool ◽

Transcranial Alternating Current Stimulation ◽

Close Time ◽

Auditory Cortices

Brain oscillations are regarded as important for perception as they open and close time windows for neural spiking to enable the effective communication within and across brain regions. In the past, studies on perception primarily relied on the use of electrophysiological techniques for probing a correlative link between brain oscillations and perception. The emergence of noninvasive brain stimulation techniques such as transcranial alternating current stimulation (tACS) provides the possibility to study the causal contribution of specific oscillatory frequencies to perception. Here, we review the studies on visual, auditory, and somatosensory perception that employed tACS to probe the causality of brain oscillations for perception. The current literature is consistent with a causal role of alpha and gamma oscillations in parieto-occipital regions for visual perception and theta and gamma oscillations in auditory cortices for auditory perception. In addition, the sensory gating by alpha oscillations applies not only to the visual but also to the somatosensory domain. We conclude that albeit more refined perceptual paradigms and individualized stimulation practices remain to be systematically adopted, tACS is a promising tool for establishing a causal link between neural oscillations and perception.

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