Enhanced Stimulus-Induced Gamma Activity in Humans during Propofol-Induced Sedation

Saxena, Neeraj; Muthukumaraswamy, Suresh; Diukova, Ana; Singh, Krish Devi; Hall, Judith Elizabeth; Wise, Richard G.

doi:10.1371/journal.pone.0057685

Cited by 50 publications

(59 citation statements)

References 64 publications

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“…More recently, comparable results were obtained with the NMDA receptor antagonist ketamine [Shaw et al, 2015]. In addition to the frequency modulation, these studies found increased amplitude of gamma responses with GABAergic enhancement, replicating previous results obtained with administration of the GABA A agonist propofol [Saxena et al, 2013]. Increased gamma amplitude accompanying a shift toward lower gamma frequencies may be related to the recruitment of larger pyramidal cell populations achieved under longer periods of inhibition [Gonzalez‐Burgos and Lewis, 2012].…”

Section: Discussionsupporting

confidence: 83%

“…For example, the GABA A positive allosteric modulator propofol was found to increase gamma amplitude, but left gamma frequency unchanged [Saxena et al, 2013]. More surprisingly, a recent study reported that neither the amplitude nor the frequency of visual gamma responses were modulated by tiagabine [Muthukumaraswamy et al, 2013a], a drug that prolongs IPSC duration by selectively inhibiting the re‐uptake of GABA from the synapse.…”

Section: Introductionmentioning

confidence: 99%

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Significant reductions in human visual gamma frequency by the gaba reuptake inhibitor tiagabine revealed by robust peak frequency estimation

Magazzini

Muthukumaraswamy

Campbell

et al. 2016

Human Brain Mapping

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The frequency of visual gamma oscillations is determined by both the neuronal excitation–inhibition balance and the time constants of GABAergic processes. The gamma peak frequency has been linked to sensory processing, cognitive function, cortical structure, and may have a genetic contribution. To disentangle the intricate relationship among these factors, accurate and reliable estimates of peak frequency are required. Here, a bootstrapping approach that provides estimates of peak frequency reliability, thereby increasing the robustness of the inferences made on this parameter was developed. The method using both simulated data and real data from two previous pharmacological MEG studies of visual gamma with alcohol and tiagabine was validated. In particular, the study by Muthukumaraswamy et al. [2013a] (Neuropsychopharmacology 38(6):1105–1112), in which GABAergic enhancement by tiagabine had previously demonstrated a null effect on visual gamma oscillations, contrasting with strong evidence from both animal models and very recent human studies was re‐evaluated. After improved peak frequency estimation and additional exclusion of unreliably measured data, it was found that the GABA reuptake inhibitor tiagabine did produce, as predicted, a marked decrease in visual gamma oscillation frequency. This result demonstrates the potential impact of objective approaches to data quality control, and provides additional translational evidence for the mechanisms of GABAergic transmission generating gamma oscillations in humans. Hum Brain Mapp 37:3882–3896, 2016. © 2016 Wiley Periodicals, Inc.

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Section: Discussionsupporting

confidence: 83%

Section: Introductionmentioning

confidence: 99%

Significant reductions in human visual gamma frequency by the gaba reuptake inhibitor tiagabine revealed by robust peak frequency estimation

Magazzini

Muthukumaraswamy

Campbell

et al. 2016

Human Brain Mapping

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“…Muthukumaraswamy and colleagues (26) found that elevation of extracellular GABA levels by tiagabine, which blocks GABA reuptake, did not modulate gamma oscillations in either visual or motor cortex. Finally, Saxena and colleagues (27), using GABA-A agonist propofol, observed an increase in stimulus-induced gamma amplitude only. Taken together, none of these studies provides support for a measurable relationship between GABA levels and visual gamma frequency in the human brain.…”

Section: Discussionmentioning

confidence: 96%

Resting GABA and glutamate concentrations do not predict visual gamma frequency or amplitude

Cousijn

Haegens

Wallis

et al. 2014

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

100

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Gamma band oscillations arise in neuronal networks of interconnected GABAergic interneurons and excitatory pyramidal cells. A previous study found a correlation between visual gamma peak frequency, as measured with magnetoencephalography, and resting GABA levels, as measured with magnetic resonance spectroscopy (MRS), in 12 healthy volunteers. If true, this would allow studies in clinical populations testing modulation of this relationship, but this finding has not been replicated. We addressed this important question by measuring gamma oscillations and GABA, as well as glutamate, in 50 healthy volunteers. Visual gamma activity was evoked using an established gratings paradigm, and we applied a beamformer spatial filtering technique to extract source-reconstructed gamma peak frequency and amplitude from the occipital lobe. We determined gamma peak frequency and amplitude from the location with maximal activation and from the location of the MRS voxel to assess the relationship of GABA with gamma. Gamma peak frequency was estimated from the highest value of the raw spectra and by a Gaussian fit to the spectra. MRS data were acquired from occipital cortex. We did not replicate the previously found correlation between gamma peak frequency and GABA concentration. Calculation of a Bayes factor provided strong evidence in favor of the null hypothesis. We also did not find a correlation between gamma activity and glutamate or between gamma and the ratio of GABA/glutamate. Our results suggest that cortical gamma oscillations do not have a consistent, demonstrable relationship to excitatory/inhibitory network activity as proxied by MRS measurements of GABA and glutamate. G amma band oscillations (30-90 Hz) are found in many cortical areas and are thought to play an important role in cognitive processing (1). Both experimental and modeling studies have shown that the gamma rhythm is inextricably linked to synaptic inhibition (2-4). GABA-mediated inhibition is both necessary and sufficient for the generation of gamma oscillations, and mutually connected inhibitory interneuron networks are major generators of gamma oscillations (4-6). In addition, fast recurrent excitation followed by slower feedback inhibitions can give rise to gamma oscillations (3, 7). Most likely, excitation-inhibition and inhibition-inhibition hybrid gamma networks work together to generate gamma frequency oscillations (2, 8).In vitro and modeling studies have clearly shown the importance of GABA for the generation of gamma oscillations, but the relationship between GABA and gamma is not easily assessed in the human brain. Muthukumaraswamy and colleagues (9) attempted to assess this relationship by correlating resting GABA concentrations as measured by magnetic resonance spectroscopy (MRS) with visual gamma oscillations as measured by magnetoencephalography (MEG). MRS provides a noninvasive method of quantifying metabolite concentrations in discrete regions of the human brain, but it can only detect the total concentration of a neurochemical and cannot...

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“…In line with the role of inhibitory interneurons in generating gamma band activity, a positive correlation between GABA levels in superior temporal sulcus (measured using MRS) and the power of induced gamma band oscillations has been reported (Balz et al, 2016), suggesting that increased induced gamma band power is associated with higher GABA levels. This position is also supported by pharmalogical manipulations of GABA, as administration of propofol (a GABA agonist) leads to an increase in induced gamma band power (Saxena, Muthukumaraswamy, & Diukova, 2013). However, other studies have not found any association between GABA levels (in occipital cortex) and induced gamma band power (Cousijn et al, 2014;Muthukumaraswamy, Edden, Jones, Swettenham, & Singh, 2009).…”

Section: High Frequency Neural Oscillations (Gamma-band Activity)mentioning

confidence: 92%

“…Peak gamma frequency has been shown to be stable over time, and also to be highly heritable (van Pelt, Boomsma, & Fries, 2012), therefore peak gamma frequency may represent a more useful way to investigate E/I balance in human participants. Some studies have shown that visuallyinduced peak gamma frequency is correlated with resting GABA levels in occipital cortex Gaetz, Edgar, Wang, & Roberts, 2011;Muthukumaraswamy et al, 2009) although others have failed to replicate this relationship (Cousijn et al, 2014;Saxena et al, 2013). The technical difficulty in measuring GABA concentration in vivo with MRS and the different scan parameters used in these studies may contribute to the lack of convergence in results, Nevertheless, peak gamma frequency elicited by visual stimuli has been found to be higher in ASD (Dickinson et al, 2016), and correlated with autistic traits in the neurotypical population (Dickinson, Bruyns-Haylett, Jones, & Milne, 2015).…”

Section: High Frequency Neural Oscillations (Gamma-band Activity)mentioning

confidence: 99%

Measuring neural excitation and inhibition in autism: Different approaches, different findings and different interpretations

2016

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The balance of neural excitation and inhibition (E/I balance) is often hypothesised to be altered in autism spectrum disorder (ASD). One widely held view is that excitation levels are elevated relative to inhibition in ASD. Understanding whether, and how, E/I balance may be altered in ASD is important given the recent interest in trialling pharmacological interventions for ASD which target inhibitory neurotransmitter function.Here we provide a critical review of evidence for E/I balance in ASD. We conclude that data from a number of domains provides support for alteration in excitation and inhibitory neurotransmission in ASD, but when considered collectively, the available literature provide little evidence to support claims for either a net increase in excitation or a net increase in inhibition. Strengths and limitations of available techniques are considered, and directions for future research discussed.3

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Enhanced Stimulus-Induced Gamma Activity in Humans during Propofol-Induced Sedation

Cited by 50 publications

References 64 publications

Significant reductions in human visual gamma frequency by the gaba reuptake inhibitor tiagabine revealed by robust peak frequency estimation

Significant reductions in human visual gamma frequency by the gaba reuptake inhibitor tiagabine revealed by robust peak frequency estimation

Resting GABA and glutamate concentrations do not predict visual gamma frequency or amplitude

Measuring neural excitation and inhibition in autism: Different approaches, different findings and different interpretations

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