Neural gain control measured through cortical gamma oscillations is associated with sensory sensitivity

Orekhova, Elena V.; Stroganova, Tatiana A.; Schneiderman, Justin F.; Lundström, Staffan; Riaz, Bushra; Sarovic, Darko; Sysoeva, Olga; Brant, Georg; Gillberg, Christopher; Hadjikhani, Nouchine

doi:10.1002/hbm.24469

Cited by 23 publications

(46 citation statements)

References 63 publications

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“…In a majority of these clinically oriented studies, the parameters of gamma oscillations (power, frequency) were investigated in a single experimental condition. Our present and previous [18,71,76] results suggest that changes of gamma parameters caused by changes in sensory input intensity may be particularly informative for detecting E-I balance abnormalities in neuro-psychiatric disorders.…”

Section: Gr Suppression Transition Point and E-i Balance In The Visuasupporting

confidence: 67%

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Additive effect of contrast and velocity suggests the role of strong excitatory drive in suppression of visual gamma response

et al. 2020

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It is commonly acknowledged that gamma-band oscillations arise from interplay between neural excitation and inhibition; however, the neural mechanisms controlling the power of stimulus-induced gamma responses (GR) in the human brain remain poorly understood. A moderate increase in velocity of drifting gratings results in GR power enhancement, while increasing the velocity beyond some 'transition point' leads to GR power attenuation. We tested two alternative explanations for this nonlinear input-output dependency in the GR power. First, the GR power can be maximal at the preferable velocity/temporal frequency of motion-sensitive V1 neurons. This 'velocity tuning' hypothesis predicts that lowering contrast either will not affect the transition point or shift it to a lower velocity. Second, the GR power attenuation at high velocities of visual motion can be caused by changes in excitation/inhibition balance with increasing excitatory drive. Since contrast and velocity both add to excitatory drive, this 'excitatory drive' hypothesis predicts that the 'transition point' for lowcontrast gratings would be reached at a higher velocity, as compared to high-contrast gratings. To test these alternatives, we recorded magnetoencephalography during presentation of low (50%) and high (100%) contrast gratings drifting at four velocities. We found that lowering contrast led to a highly reliable shift of the GR suppression transition point to higher velocities, thus supporting the excitatory drive hypothesis. No effects of contrast or velocity were found in the alpha-beta range. The results have implications for understanding the mechanisms of gamma oscillations and developing gamma-based biomarkers of disturbed excitation/inhibition balance in brain disorders.

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Section: Gr Suppression Transition Point and E-i Balance In The Visuasupporting

confidence: 67%

“…In indirect support of this assumption, we have recently described a lack of velocity-related gamma suppression in a subject with epilepsy and occipital spikes [18]. A link between reduced velocityrelated GR suppression and sensory hypersensitivity [71] further supports this conjecture.…”

Section: Gr Suppression Transition Point and E-i Balance In The Visuamentioning

confidence: 62%

Additive effect of contrast and velocity suggests the role of strong excitatory drive in suppression of visual gamma response

et al. 2020

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“…To better quantify this effect, we separated the gamma response into three frequency bands -low (25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40), mid (40-70 Hz) and high (70-100 Hz)-based on the data from Experiment 1. We then calculated the average amplitude for each condition within a time window of 0-16 s (Fig 10) and analysed this data as a two-factor repeated-measures design for each frequency band ( Table 5).…”

Section: Plos Onementioning

confidence: 99%

“…Visual stimulus induced gamma oscillations are a prominent feature of the local field potential in the visual cortex, and have been observed in humans [1][2][3], non-human primates [4][5][6], cats [7,8] and rodents [9,10], suggesting that they represent a fundamental aspect of the operation of the visual cortex that has been preserved across species. Gamma oscillations are sensitive to the presence of luminance contrast in the visual field [2,5,[11][12][13][14][15] and are tuned to properties of luminance-defined gratings, such as their size [16][17][18], orientation [13,19] and spatial and temporal frequency [1,[20][21][22][23][24][25]. However there is some debate about the extent to which they are generated by more naturalistic stimuli [26,27].…”

Section: Introductionmentioning

confidence: 99%

The gamma response to colour hue in humans: Evidence from MEG

et al. 2020

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It has recently been demonstrated through invasive electrophysiology that visual stimulation with extended patches of uniform colour generates pronounced gamma oscillations in the visual cortex of both macaques and humans. In this study we sought to discover if this oscillatory response to colour can be measured non-invasively in humans using magnetoencephalography. We were able to demonstrate increased gamma (40–70 Hz) power in response to full-screen stimulation with four different colour hues and found that the gamma response is particularly strong for long wavelength (i.e. red) stimulation, as was found in previous studies. However, we also found that gamma power in response to colour was generally weaker than the response to an identically sized luminance-defined grating. We also observed two additional responses in the gamma frequency: a lower frequency response around 25–35 Hz that showed fewer clear differences between conditions than the gamma response, and a higher frequency response around 70–100 Hz that was present for red stimulation but not for other colours. In a second experiment we sought to test whether differences in the gamma response between colour hues could be explained by their chromatic separation from the preceding display. We presented stimuli that alternated between each of the three pairings of the three primary colours (red, green, blue) at two levels of chromatic separation defined in the CIELUV colour space. We observed that the gamma response was significantly greater to high relative to low chromatic separation, but that at each level of separation the response was greater for both red-blue and red-green than for blue-green stimulation. Our findings suggest that the stronger gamma response to red stimulation cannot be wholly explained by the chromatic separation of the stimuli.

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“…A weak suppression of gamma oscillations at high stimulation intensities may then result in a stronger impact of the sensory stimulation on the neural network, and lead to sensory overload. Indeed, in a recent study, we have found that a weaker suppression of gamma response at fast motion velocities (of high-contrast gratings) correlated with enhanced sensory sensitivity, especially in the visual domain (Orekhova et al, 2018a).…”

Section: Discussionmentioning

confidence: 87%

Additive effect of contrast and velocity proves the role of strong excitatory drive in suppression of visual gamma response

Orekhova

Prokofyev

Nikolaeva

et al. 2018

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Visual gamma oscillations are generated through interactions of excitatory and inhibitory neurons and are strongly modulated by sensory input. A moderate increase in excitatory drive to the visual cortex via increasing contrast or motion velocity of drifting gratings results in strengthening of the gamma response (GR). However, increasing the velocity beyond some ‘transition point’ leads to the suppression of the GR. There are two theoretical models that can explain such suppression. The ‘excitatory drive’ model infers that, at high drifting rates, GR suppression is caused by excessive excitation of inhibitory neurons. Since contrast and velocity have an additive effect on excitatory drive, this model predicts that the GR ‘transition point’ for low-contrast gratings would be reached at a higher velocity, as compared to high-contrast gratings. The alternative ‘velocity tuning’ model implies that the GR is maximal when the drifting rate of the grating corresponds to the preferable velocity of the motion-sensitive V1 neurons. This model predicts that lowering contrast either will not affect the transition point or will shift it to a lower drifting rate. We tested these models with magnetoencephalography-based recordings of the GR during presentation of low (50%) and high (100%) contrast gratings drifting at four velocities. We found that lowering contrast led to a highly reliable shift of the GR suppression transition point to higher velocities, thus supporting the excitatory drive model. No effects of contrast or velocity were found for the alpha-beta response power. The results have important implications for the understanding of the neural mechanisms underlying gamma oscillations and the development of gamma-based biomarkers of brain disorders.

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Neural gain control measured through cortical gamma oscillations is associated with sensory sensitivity

Cited by 23 publications

References 63 publications

Additive effect of contrast and velocity suggests the role of strong excitatory drive in suppression of visual gamma response

Additive effect of contrast and velocity suggests the role of strong excitatory drive in suppression of visual gamma response

The gamma response to colour hue in humans: Evidence from MEG

Additive effect of contrast and velocity proves the role of strong excitatory drive in suppression of visual gamma response

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