Stimulus-Induced Changes in 1/f-like Background Activity in EEG

Abstract

Research into the nature of 1/f-like, nonoscillatory electrophysiological activity has grown exponentially in recent years in cognitive neuroscience. The shape of this activity has been linked to the balance between excitatory and inhibitory neural circuits, which is thought to be important for information processing. However, to date, it is not known whether the presentation of a stimulus induces changes in the parameters of 1/f activity in scalp recordings, separable from event-related potentials (ERPs). Here, we analyzed event-related broadband changes in human EEG both before and after removing ERPs to demonstrate their confounding effect, and to establish whether there are genuine stimulus-induced changes in 1/f. Using data from a passive and an active auditory task (n = 23, 61% female), we found that the shape of the post-event spectra between 2 and 25 Hz differed significantly from the pre-event spectra even after removing the frequency-content of ERPs. Further, a significant portion of this difference could be accounted for by a rotational shift in 1/f activity, manifesting as an increase in low and a decrease in high frequencies. Importantly, the magnitude of this rotational shift was related to the attentional demands of the task. This change in 1/f is consistent with increased inhibition following stimulus onset, and likely reflects a disruption of ongoing excitatory activity proportional to processing demands. Finally, these findings contradict the central assumption of baseline normalization strategies in time-frequency analyses, namely, that background EEG activity is stationary across time. As such, they have far-reaching consequences relevant for several subfields of neuroscience.

Event-Induced Modulation of Aperiodic Background EEG: Attention-Dependent and Age-Related Shifts in E:I balance, and Their Consequences for Behavior

“…The reported stimulus-induced clockwise spectral rotations are consistent with a decreased E:I ratio (increased inhibition) following stimulus onset and likely reflect a disruption of ongoing excitatory activity proportional to processing demands (Gratton, 2018; see also Zhang et al, 2023). However, the Gyurkovics et al (2022) study was conducted using simple paradigms with minimal quantification of the participants' performance, thus making it difficult to determine the behavioral consequences, if any, of the stimulus-induced spectral exponent shifts. Moreover, event-related spectrograms were quantified using a time window extending more than 1,000 ms, which precludes the detection of rapid changes in aperiodic activity accompanying information processing over time.…”

“…p-values for Ftests were based on permutations for mixed ANOVA (Frossard & Renaud, 2021;Kherad-Pajouh & Renaud, 2015). We used 10,000 permutations, and the sign for a given parameter was reversed for a random half of the data points in each iteration (an equivalent approach was adopted in our previous work, Gyurkovics et al, 2022). Only planned comparisons were tested.…”

“…Despite accounting for a substantial portion of the neural signal, the aperiodic component has, until recently, received limited attention in cognitive neuroscience, often being considered "noise" devoid of any functional significance. Recent theoretical and methodological advances, however, have begun to provide evidence in support of the functional relevance of the aperiodic component in explaining brain dynamics and human behavior (Donoghue et al, 2020;Gyurkovics et al, 2022;Waschke et al, 2021). A significant breakthrough in this research is the observation of a reduction in the exponent of the aperiodic activity (i.e., a flatter spectrum) in older adults, consistent with the idea of increasing neural noise in aging (Cremer & Zeef, 1987;Salthouse, 2010;Salthouse & Lichty, 1985;, and suggesting an age-related shift in the balance between excitation and inhibition (E:I balance, Gao et al, 2017).…”

“…However, a serious challenge to this endeavor is the need to separate the task-induced (non-phase-locked) aperiodic component from other task-evoked (phaselocked) EEG activity (i.e., event-related potentials, ERPs, in the time domain), both of which display a broadband distribution in the frequency domain. Gyurkovics et al (2022) were the first to address this methodological issue using scalp EEG data collected from young adults. Their study showed reliable and systematic stimulus-induced changes in the aperiodic component, which were independent of the concurrent ERPs and scaled with the attentional demands of the task.…”

Dynamics of alpha suppression index both modality specific and general attention processes

“…It is also worth noting that these effects could reflect, in part, variability in non-oscillatory, broadband (1/f) activity. The steepness of 1/f activity has been reported to vary after presentation of attentionally relevant auditory stimuli (Gyurkovics et al, 2022). However, an in-depth investigation of broadband activity is beyond the scope of this paper.…”