Cross-Frequency Brain Network Dynamics Support Pitch Change Detection

Abstract

Processing auditory sequences involves multiple brain networks and is crucial to complex perception associated with music appreciation and speech comprehension. We used time-resolved cortical imaging in a pitch change detection task to detail the underlying nature of human brain network activity, at the rapid time scales of neurophysiology. In response to tone sequence presentation to the participants, we observed slow inter-regional signaling at the pace of tone presentations (2-4 Hz) that was directed from auditory cortex toward both inferior frontal and motor cortices. Symmetrically, motor cortex manifested directed influence onto auditory and inferior frontal cortices via bursts of faster (15-35 Hz) activity. These bursts occurred precisely at the expected latencies of each tone in a sequence. This expression of interdependency between slow/fast neurophysiological activity yielded a form of local cross-frequency phase-amplitude coupling in auditory cortex, which strength varied dynamically and peaked when pitch changes were anticipated. We clarified the mechanistic relevance of these observations in relation to behavior by including a group of individuals afflicted by congenital amusia, as a model of altered function in processing sound sequences. In amusia, we found a depression of inter-regional slow signaling toward motor and inferior frontal cortices, and a chronic overexpression of slow/fast phase-amplitude coupling in auditory cortex. These observations are compatible with a misalignment between the respective neurophysiological mechanisms of stimulus encoding and internal predictive signaling, which was absent in controls. In summary, our study provides a functional and mechanistic account of neurophysiological activity for predictive, sequential timing of auditory inputs.SIGNIFICANCE STATEMENT Auditory sequences are processed by extensive brain networks, involving multiple systems. In particular, fronto-temporal brain connections participate in the encoding of sequential auditory events, but so far, their study was limited to static depictions. This study details the nature of oscillatory brain activity involved in these inter-regional interactions in human participants. It demonstrates how directed, polyrhythmic oscillatory interactions between auditory and motor cortical regions provide a functional account for predictive timing of incoming items in an auditory sequence. In addition, we show the functional relevance of these observations in relation to behavior, with data from both normal hearing participants and a rare cohort of individuals afflicted by congenital amusia, which we considered here as a model of altered function in processing sound sequences.

Keywords: audition; congenital amusia; neural oscillations; phase-amplitude coupling; pitch discrimination; predictive coding.