Steady-state BOLD Response to Higher-order Cognition Modulates Low-Frequency Neural Oscillations

Abstract

Steady-state responses (SSRs) reflect the synchronous neural oscillations evoked by noninvasive and consistently repeated stimuli at the fundamental or harmonic frequencies. The steady-state evoked potentials (SSEPs; the representative form of the SSRs) have been widely used in the cognitive and clinical neurosciences and brain-computer interface research. However, the steady-state evoked potentials have limitations in examining high-frequency neural oscillations and basic cognition. In addition, synchronous neural oscillations in the low frequency range (<1 Hz) and in higher-order cognition have received a little attention. Therefore, we examined the SSRs in the low frequency range using a new index, the steady-state BOLD responses (SSBRs) evoked by semantic stimuli. Our results revealed that the significant SSBRs were induced at the fundamental frequency of stimuli and the first harmonic in task-related regions, suggesting the enhanced variability of neural oscillations entrained by exogenous stimuli. The SSBRs were independent of neurovascular coupling and characterized by sensorimotor bias, an indication of regional-dependent neuroplasticity. Furthermore, the amplitude of SSBRs may predict behavioral performance and show the psychophysiological relevance. Our findings provide valuable insights into the understanding of the SSRs evoked by higher-order cognition and how the SSRs modulate low-frequency neural oscillations.

Low frequency steady-state brain responses modulate large scale functional networks in a frequency-specific means

“…Post hoc analysis for both the fundamental frequency and the first harmonic showed that the power was different between task conditions and the resting‐state rather than among task conditions, indicating that the modulation of brain states by lfSSBRs overwhelms the modulation of different attention conditions. Meanwhile, it is consistent with previous results of sensorimotor bias [Wang et al, ]. That is to say, the lfSSBRs modulate sensorimotor network much more that task‐related regions.…”

“…Furthermore, the lfSSBRs measure the variability of BOLD signal, and are different from the activation that measures the mean value of BOLD signal [Wang et al ]. In prior studies, Garrett et al [], [2014] found that task‐related regions assessed by the BOLD signal variability are dispersive and distinctive from those measured by the mean BOLD signal.…”

“…The visual and sensorimotor networks were also expected to be modulated in the ANT because these networks are involved in all visual tasks that require motor responses, i.e., stimulus–response (S–R) tasks. Considering the sensorimotor bias of lfSSBRs [Wang et al, ], the attention networks may be modulated more weakly than the sensory‐motor system and triple network system. Therefore, we hypothesized that the triple network system and the sensory‐motor system would be effectively modulated by lfSSBRs in a frequency‐specific pattern.…”

Multiscale energy reallocation during low‐frequency steady‐state brain response

“…Accordingly, we hypothesize that the lfSSBR may reflect brain signal variability (BSV) at particular frequencies. Previous studies have shown enhanced power, functional connectivity, and coherence at resonant frequencies (the fundamental frequency and its harmonics) and a reduction in power at lower frequency range (Fransson, ; He, ; Wang et al, ), suggesting frequency‐specific characteristics of lfSSBR. The BSV, on the other hand, is usually measured at broad frequency range (Garrett et al, ; Guitart‐Masip et al, ), leaving its frequency characteristics largely unknown.…”

“…In lfSSBR, we assess the amplitude of regular fluctuations in a relative long time series rather than transient signal change (Figure ), indicating that it cannot be delineated using traditional hemodynamic response function (Lewis, Setsompop, Rosen, & Polimeni, ; Wang et al, ). Additionally, the lfSSBR represents brain network in frequency‐ and phase‐dependent means (Wang, Liu, Jing, Long, & Chen, ; Wang et al, ), and is associated with particular psychophysiological activity (Wang et al, ). Recent studies have suggested that task‐evoked blood oxygen level dependent (BOLD) signals and ongoing BOLD signal fluctuations have negative and phase‐dependent interaction, challenging the linear superposition model (He, ; Huang et al, ).…”