Frequency selectivity of persistent cortical oscillatory responses to auditory rhythmic stimulation

Abstract

Cortical oscillations have been proposed to play a functional role in speech and music perception, attentional selection and working memory, via the mechanism of neural entrainment. One of the most compelling arguments for neural entrainment is that its modulatory effect on ongoing oscillations outlasts rhythmic stimulation. We tested the existence of this phenomenon by studying cortical neural oscillations during and after presentation of melodic stimuli in a passive perception paradigm. Melodies were composed of [~]60 and [~]80 Hz tones embedded in a 2.5 Hz stream. Using intracranial and surface recordings in humans, we reveal consistent neural response properties throughout the cortex, well beyond the auditory regions. Persistent oscillatory activity in the high-gamma band was observed in response to the tones. By contrast, in response to the 2.5 Hz stream, no persistent activity in any frequency band was observed. We further show that our data are well-captured by a model of damped harmonic oscillator and can be classified into three classes of neural dynamics, with distinct damping properties and eigenfrequencies. This model provides a mechanistic and quantitative explanation of the frequency selectivity of auditory neural entrainment in the human cortex. Significance statementIt has been proposed that the functional role of cortical oscillations is subtended by a mechanism of entrainment, the synchronisation in phase or amplitude of neural oscillations to a periodic stimulation. We tested whether the modulatory effect on ongoing oscillations outlasts the rhythmic stimulation, a phenomenon considered to be one of the most compelling arguments for entrainment. Using intracranial and surface recordings of human listening to rhythmic auditory stimuli, we reveal consistent oscillatory responses throughout the cortex, with persistent activity of high-gamma oscillations. On the contrary, neural oscillations do not outlast low-frequency acoustic dynamics. We interpret our results as reflecting harmonic oscillator properties - a model ubiquitous in physics but rarely used in neuroscience.