Neuronal Avalanches in Naturalistic Speech and Music Listening

Abstract Neuronal avalanches are cascade-like events ubiquitously observed across imaging modalities and scales. Aperiodic timing and topographic distribution of these events have been related to the systemic physiology of brain states. However, it is still unknown whether neuronal avalanches are correlates of cognition, or purely reflect physiological properties. In this work, we investigate this question by analyzing intracranial recordings of epileptic participants during rest and passive listening of naturalistic speech and music stimuli. During speech or music listening, but not rest, participants’ brains “tick” together, as the timing of neuronal avalanches is stimulus-driven and hence correlated across participants. Auditory regions are strongly participating in coordinated neuronal avalanches, but also associative regions, indicating both the specificity and distributivity of cognitive processing. The subnetworks where such processing takes place during speech and music largely overlap, especially in auditory regions, but also diverge in associative cortical sites. Finally, differential pathways of avalanche propagation across auditory and non-auditory regions differentiate brain network dynamics during speech, music and rest. Overall, these results highlight the potential of neuronal avalanches as a neural index of cognition. Author’s summary Neuronal avalanches consist of collective network events propagating across the brain in short-lived and aperiodic instances. These salient events have garnered a great interest for studying the physics of cortical dynamics, and bear potential for studying brain data also in purely neuroscientific contexts. In this work we investigated neuronal avalanches to index cognition, analyzing an intracranial stereo electroencephalography (iEEG) dataset during speech, music listening and resting state in epileptic patients. We show that neuronal avalanches are consistently driven by music and speech stimuli: avalanches co-occur in participants listening to the same auditory stimulus; avalanche topography differs from resting state, presenting partial similarities during speech and music; avalanche propagation changes during speech, music, and rest conditions, especially along the pathways between auditory and non auditory regions. Our work underlines the distributed nature of auditory stimulus processing, supporting neuronal avalanches as a valuable and computationally advantageous framework for the study of cognition in humans.