Abstract
Over the past decades, numerous studies have linked cortical gamma oscillations (∼30–100 Hz) to neurocomputational mechanisms. Their functional relevance, however, is still passionately debated. Here, we asked whether endogenous gamma oscillations in the human brain can be entrained by a rhythmic photic drive >50 Hz. Such a noninvasive modulation of endogenous brain rhythms would allow conclusions about their causal involvement in neurocognition. To this end, we systematically investigated oscillatory responses to a rapid sinusoidal flicker in the absence and presence of endogenous gamma oscillations using magnetoencephalography (MEG) in combination with a high-frequency projector. The photic drive produced a robust response over visual cortex to stimulation frequencies of up to 80 Hz. Strong, endogenous gamma oscillations were induced using moving grating stimuli as repeatedly done in previous research. When superimposing the flicker and the gratings, there was no evidence for phase or frequency entrainment of the endogenous gamma oscillations by the photic drive. Unexpectedly, we did not observe an amplification of the flicker response around participants' individual gamma frequencies (IGFs); rather, the magnitude of the response decreased monotonically with increasing frequency. Source reconstruction suggests that the flicker response and the gamma oscillations were produced by separate, coexistent generators in visual cortex. The presented findings challenge the notion that cortical gamma oscillations can be entrained by rhythmic visual stimulation. Instead, the mechanism generating endogenous gamma oscillations seems to be resilient to external perturbation.SIGNIFICANCE STATEMENT We aimed to investigate to what extent ongoing, high-frequency oscillations in the gamma-band (30–100 Hz) in the human brain can be entrained by a visual flicker. Gamma oscillations have long been suggested to coordinate neuronal firing and enable interregional communication. Our results demonstrate that rhythmic visual stimulation cannot hijack the dynamics of ongoing gamma oscillations; rather, the flicker response and the endogenous gamma oscillations coexist in different visual areas. Therefore, while a visual flicker evokes a strong neuronal response even at high frequencies in the gamma-band, it does not entrain endogenous gamma oscillations in visual cortex. This has important implications for interpreting studies investigating the causal and neuroprotective effects of rhythmic sensory stimulation in the gamma-band.
Highlights
Cortical gamma oscillations have been repeatedly linked to the formation of neuronal ensembles through synchronization of spiking activity in rodents and primates (Eckhorn et al, 1988; Gray and Singer, 1989; Gray et al, 1992; Wehr and Laurent, 1996; Brosch et al, 2002), including humans (Tallon et al, 1995; Müller et al, 1997; Rodriguez et al, 1999; Hoogenboom et al, 2006)
The linearity of the flicker response power indicating a change in the peak frequency of the gamma oscilas a function of flicker frequency, i.e., evidence for the H0 as observed in the results reported below, was corroborated using linear regression models implemented in the R base package
We considered the relative power change induced by the moving gratings in the 0.5to 1.5-s interval (T1) before the flicker onset and in the 2.5- to 3.5-s interval (T2) in which both the moving gratings and the photic drive were present
Summary
Cortical gamma oscillations have been repeatedly linked to the formation of neuronal ensembles through synchronization of spiking activity in rodents and primates (Eckhorn et al, 1988; Gray and Singer, 1989; Gray et al, 1992; Wehr and Laurent, 1996; Brosch et al, 2002), including humans (Tallon et al, 1995; Müller et al, 1997; Rodriguez et al, 1999; Hoogenboom et al, 2006). The ability to non-invasively modulate gamma rhythms would allow to study their causal role in neuronal processing and cognition, as well as their therapeutic potential, as recently proposed by (Iaccarino et al, 2016; Adaikkan et al, 2019)
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