Frequency of gamma oscillations in humans is modulated by velocity of visual motion

Abstract

Gamma oscillations are generated in networks of inhibitory fast-spiking (FS) parvalbumin-positive (PV) interneurons and pyramidal cells. In animals, gamma frequency is modulated by the velocity of visual motion; the effect of velocity has not been evaluated in humans. In this work, we have studied velocity-related modulations of gamma frequency in children using MEG/EEG. We also investigated whether such modulations predict the prominence of the "spatial suppression" effect (Tadin D, Lappin JS, Gilroy LA, Blake R. Nature 424: 312-315, 2003) that is thought to depend on cortical center-surround inhibitory mechanisms. MEG/EEG was recorded in 27 normal boys aged 8-15 yr while they watched high-contrast black-and-white annular gratings drifting with velocities of 1.2, 3.6, and 6.0°/s and performed a simple detection task. The spatial suppression effect was assessed in a separate psychophysical experiment. MEG gamma oscillation frequency increased while power decreased with increasing velocity of visual motion. In EEG, the effects were less reliable. The frequencies of the velocity-specific gamma peaks were 64.9, 74.8, and 87.1 Hz for the slow, medium, and fast motions, respectively. The frequency of the gamma response elicited during slow and medium velocity of visual motion decreased with subject age, whereas the range of gamma frequency modulation by velocity increased with age. The frequency modulation range predicted spatial suppression even after controlling for the effect of age. We suggest that the modulation of the MEG gamma frequency by velocity of visual motion reflects excitability of cortical inhibitory circuits and can be used to investigate their normal and pathological development in the human brain.

Input-dependent modulation of MEG gamma oscillations reflects gain control in the visual cortex

“…Developmental changes of excitatory and inhibitory neurotransmission [26][27][28] leave a possibility that our previous observation of motion-velocity modulation of MEG gamma oscillations in children 25 is age-specific. To clarify this issue, we investigated a large group of subjects spanning ages from 7 to 40 years.…”

“…The procedure used herein is similar to that used previously 25,43 . The stimuli were generated using Presentation software (Neurobehavioral Systems Inc., USA) and consisted of black and white sinusoidally modulated annular gratings with a spatial frequency of 1.66 cycles per degree of visual angle with an outer diameter of 18 degrees of visual angle (Fig.…”

Peak visual gamma frequency is modified across the healthy menstrual cycle

“…There is promising translation of this cellular model to noninvasive human studies via induction of gamma oscillations in the visual cortex. Visual gamma oscillations appear to be a highly robust biological trait marker (Muthukumaraswamy, Singh, Swettenham, & Jones, ; Tan, Gross, & Uhlhaas, ) that varies across age (Gaetz, Roberts, Singh, & Muthukumaraswamy, ; Orekhova et al, ), and is strongly genetically determined (van Pelt, Boomsma, & Fries, ). A number of pharmaco‐MEG studies have been able to show that they are consistently and predictably modulated by changes in GABAergic inhibition (Muthukumaraswamy, ).…”

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

“…The peak frequency of visual gamma responses is modulated by properties of the visual stimulus such as size [Gieselmann and Thiele, 2008; Jia et al, 2013; Ray and Maunsell, 2011; van Pelt and Fries, 2013], contrast [Hadjipapas et al, 2015; Jia et al, 2013; Lowet et al, 2015; Perry et al, 2015; Ray and Maunsell, 2010; Roberts et al, 2013], motion [Friedman‐Hill, 2000; Muthukumaraswamy and Singh, 2013; Swettenham et al, 2009], motion velocity [Gray et al, 1990; Gray and Viana Di Prisco, 1997; Orekhova et al, 2015], eccentricity [van Pelt and Fries, 2013], noise masking [Jia et al, 2013], and cross‐orientation masking [Lima et al, 2010; Perry, 2015]. Across individuals, peak gamma frequency correlates with psychophysical performance in visual discrimination tasks [Dickinson et al, 2015; Edden et al, 2009].…”