Brain network interconnectivity dynamics explain metacognitive differences in listening behavior

Abstract

AbstractComplex auditory scenes pose a challenge to attentive listening, rendering listeners slower and more uncertain in their perceptual decisions. How can we explain such behaviors from the dynamics of cortical networks that pertain to control of listening behavior? We here follow up on the hypothesis that listeners’ ability to flexibly adapt to challenging listening situations is supported by modular reconfiguration of auditory-control networks in a sample of N=40 participants who underwent resting-state and task functional magnetic resonance imaging (fMRI). Individual titration of a spatial selective auditory attention task maintained an average accuracy of ∼70% but yielded considerable inter-individual differences in listeners’ response speed and reported confidence in own decisions. Whole-brain network modularity increased from rest to task by reconfiguring auditory, cinguloopercular, and dorsal attention networks. Specifically, interconnectivity between nodes of auditory network and ciguloopercular network decreased during the task relative to resting state. Additionally, interconnectivity between nodes of dorsal attention network and cinguloopercular network increased. These interconnectivity dynamics were predictive of individual differences in response speed and confidence, the degree of which was more pronounced after incorrect judgments. Our findings uncover the behavioral relevance of functional crosstalk between auditory and attentional-control networks during metacognitive assessment of own perception in challenging listening situations and suggest two functionally dissociable cortical networked systems that shape the considerable metacognitive differences between individuals.Significance StatementThe ability to communicate in challenging listening situations varies not only objectively but also subjectively between individuals. Using fMRI and a challenging auditory task, we here show that this variability in metacognitive judgments of own listening behavior manifests in an adaptive, modular reconfiguration of brain networks. This reconfiguration involves auditory and attentional-control networks. Task-related modulations of brain interconnectvity suggest two dissociable cortical networked systems - one auditory and cinguloopercular; one auditory and dorsal-attention - that shape individual metacognitive performance during adaptive listening behavior. These findings promise new opportunities to better understand and ultimately intervene on deficits of auditory perception such as age-related sensorineural hearing loss or auditory hallucinations.