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 highdimensional neural states.auditory perception | psychophysics | neuroscience L ow-frequency neural oscillations have recently been proposed to play a crucial role in perception (1-4). This is because lowfrequency neural oscillations reflect fluctuations in local neuronal excitability, meaning they influence the likelihood of neuronal firing in a periodic fashion (4-6). The result is that the probability that a (near-threshold) stimulus will elicit a neuronal response is not a uniform function of time but, instead, depends on the phase of the neural oscillation into which the stimulation falls. Indeed, the dependence of behavioral performance on neural oscillatory phase has been demonstrated in the visual (7-11) and auditory (12-15) domains.The role of neural oscillatory phase in perception is suggested to be of particular importance when stimuli possess temporal regularity (1,11,16,17). Precise alignment of neural oscillations with rhythmic stimuli is accomplished via entrainment, which is a process by which two oscillations become synchronized, or phaselocked, through phase and/or period adjustments (18). Through entrainment, perception of rhythmic stimuli is optimized when high-energy portions of a signal are aligned with periods of high excitab...

Natural asynchronies in audiovisual communication signals regulate neuronal multisensory interactions in voice-sensitive cortex

“…Evidence supporting this possibility in human studies shows that the phase of entrained or cross-modally reset cortical oscillations can have subtle effects on auditory perception (24,45,46), behavioral response times (26), and visual detection thresholds (23,40,47,48). Previous work has also shown both that the degree of multisensory perceptual binding is modulated by stimulus type (5), task (49), and prior experience (50), and that oscillatory entrainment adjusts as a function of selective attention to visual or auditory stimuli (51,52).…”

Prefrontal cortex modulates posterior alpha oscillations during top-down guided visual perception

“…Previous studies in the auditory domain had localized the origin of the low-frequency activity to sensory areas and not frontal regions (13,14,35) but were confounded by the presentation rate, which likely evoked activity (14,35,36). Given that exogenous stimulation induces a strong phase alignment (Fig.…”

“…It has been argued that lowfrequency neuronal oscillations might reflect a cortical mechanism for sensory selection, attentional allocation, and evidence updating during decision making (9,11,13,14,32). If the underlying functional brain architecture is inherently rhythmic, then we should be able to observe rhythmic patterns in behavior.…”

“…It has been suggested that slow-frequency activity in the delta range (<5 Hz) might reflect a mechanism for endogenous attentional selection and predictions (9, 10). In particular, endogenous low-frequency entrainment is thought to reflect a substrate of top-down processing (11)(12)(13)(14). Importantly, endogenous entrainment does not require rhythmicity in the input stream but reflects an intrinsic mechanism to enable predictions (15).…”

Studying Effects of Transcranial Alternating Current Stimulation on Hearing and Auditory Scene Analysis

“…They found that detection performance varied as a function of phase lag and that this function resembled well the tACS waveform. Henry (2012;Henry et al 2014) used a periodic 3-or 5-Hz modulation applied to an interrupted tone carrier as entraining stimulus. They manipulated the relative timing of the gap and the ongoing modulation and found that this influences gap detection in the phase-dependent manner described above for the tACS study.…”