Entrained neural oscillations in multiple frequency bands comodulate behavior

Abstract

Our sensory environment is teeming with complex rhythmic structure, to which neural oscillations can become synchronized. Neural synchronization to environmental rhythms (entrainment) is hypothesized to shape human perception, as rhythmic structure acts to temporally organize cortical excitability. In the current human electroencephalography study, we investigated how behavior is influenced by neural oscillatory dynamics when the rhythmic fluctuations in the sensory environment take on a naturalistic degree of complexity. Listeners detected near-threshold gaps in auditory stimuli that were simultaneously modulated in frequency (frequency modulation, 3.1 Hz) and amplitude (amplitude modulation, 5.075 Hz); modulation rates and types were chosen to mimic the complex rhythmic structure of natural speech. Neural oscillations were entrained by both the frequency modulation and amplitude modulation in the stimulation. Critically, listeners' target-detection accuracy depended on the specific phase-phase relationship between entrained neural oscillations in both the 3.1-Hz and 5.075-Hz frequency bands, with the best performance occurring when the respective troughs in both neural oscillations coincided. Neural-phase effects were specific to the frequency bands entrained by the rhythmic stimulation. Moreover, the degree of behavioral comodulation by neural phase in both frequency bands exceeded the degree of behavioral modulation by either frequency band alone. Our results elucidate how fluctuating excitability, within and across multiple entrained frequency bands, shapes the effective neural processing of environmental stimuli. More generally, the frequency-specific nature of behavioral comodulation effects suggests that environmental rhythms act to reduce the complexity of high-dimensional neural states.

Keywords: auditory perception; neuroscience; psychophysics.

Fig. 1.

Complex rhythmic stimulation and target placement. Schematic time-frequency representation of a complex rhythmic stimulus generated by simultaneously applying AM (5.075 Hz) and FM (3.1 Hz) to a narrow-band noise carrier. Near-threshold gaps fell randomly with respect to 3.1-Hz FM phase and fell equally often into the rising (magenta) or falling (cyan) phase of the 5.075-Hz AM.

Fig. 2.

Behavioral data for the gap-detection task. Single-participant hit rates as a function of FM stimulus phase for four exemplary listeners (Upper Left), shown separately for the rising (magenta) and falling (cyan) AM stimulus phases. All listeners showed quasi-periodic modulation of behavior by FM stimulus phase, as indicated by significant circular–linear correlations, for both AM stimulus phases (Upper Right; error bars indicate SEM). Asterisks denote significance at P ≤ 0.005. The periodicity present in the behavioral modulation was specific to the FM rate (3.1 Hz) and its harmonic (6.2 Hz; Lower).

Fig. 3.

Neural oscillations were entrained by simultaneous FM and AM. Normalized grand-average total amplitude (black), FM-evoked amplitude (red), and AM-evoked amplitude (blue) plotted as a function of frequency. All amplitude peaks for which topographies are shown were statistically significant (P ≤ 0.001). The FFT data are plotted for electrode Cz.

Fig. 4.

Entrained neural phase in multiple frequency bands comodulates behavior. (A) Toroidal representation of hit-rate modulation. 3.1-Hz neural phase is plotted on the larger, outer circle, and 5.075-Hz neural phase is plotted on the smaller, inner circle. (B) Schematic illustration of joint phase effects on behavioral performance. The red arrow indicates the combination of 3.1-Hz phase (dark gray) and 5.075-Hz phase (light gray) that yielded peak performance. (C) Analysis of single-participant hit-rate data for estimation of dependent measures. Single-trial hit rates as a function of 3.1-Hz neural phase were fit with cosine functions separately for each 5.075-Hz phase bin. (D) Dependent measures from cosine fits described in C. The 3.1-Hz driven mean performance (Left), performance range (Center), and optimal 3-Hz neural phase (Right), plotted as a function of 5.075-Hz neural phase. Plots of mean performance and performance range show mean ± SEM; plot of optimal 3.1-Hz neural phase shows mean ± circular SD.

Fig. 5.

Behavioral comodulation was interactive and frequency-specific. (A) The behavioral modulation index was significantly larger for the combination of the 3.1-Hz and 5.075-Hz frequency bands than for either frequency band alone. Error bars indicate SEM. (B) Interaction strength (shown here normalized with respect to SD across participants) showed a peak at the combination of 3.1-Hz and 5.075-Hz frequency bands that was specific to the frequencies entrained by the stimulation.